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ZOOTAXA
1600

Anatomy of anuran tadpoles from lentic water bodies:


systematic relevance and correlation with feeding habits
M. FLORENCIA VERA CANDIOTI

Magnolia Press
Auckland, New Zealand

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M. FLORENCIA VERA CANDIOTI


Anatomy of anuran tadpoles from lentic water bodies: systematic relevance and correlation
with feeding habits
(Zootaxa 1600)
175 pp.; 30 cm.
28 Sept. 2007
ISBN 978-1-86977-157-7 (paperback)
ISBN 978-1-86977-158-4 (Online edition)

FIRST PUBLISHED IN 2007 BY


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2007 Magnolia Press


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ISSN 1175-5326

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ISSN 1175-5334

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2 Zootaxa 1600 2007 Magnolia Press

VERA CANDIOTI

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ISSN 1175-5326 (print edition)

Copyright 2007 Magnolia Press

ISSN 1175-5334 (online edition)

ZOOTAXA

Anatomy of anuran tadpoles from lentic water bodies: systematic relevance and
correlation with feeding habits
M. FLORENCIA VERA CANDIOTI
CONICET, Instituto de Herpetologa, Fundacin Miguel Lillo, Miguel Lillo 251, Tucumn, Argentina. florivc@yahoo.com

Table of contents
ABSTRACT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
MATERIALS AND METHODS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
Specimens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
Chondrocranium and hyobranchial skeleton. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
Gut content . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
Data analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
Morphological variation. Geometric morphometrics. Relative warp analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
Gut content variation. Correspondence analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
Gut content-morphology relationship. Partial canonical phylogenetic ordination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
RESULTS
Morphological descriptions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
Bufonidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
Chaunus arenarum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
Chaunus spinulosus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
Ceratophryidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
Ceratophrys cranwelli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
Lepidobatrachus llanensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32
Telmatobius cf. atacamensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37
Hylidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
Dendropsophus microcephalus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
Dendropsophus nanus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49
Hypsiboas rosenbergi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54
Lysapsus limellum. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
Phyllomedusa hypochondrialis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67
Phyllomedusa sauvagii . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72
Pseudis paradoxus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78
Scinax boulengeri . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
Scinax nasicus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89
Leiuperidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96
Physalaemus santafecinus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96
Microhylidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
Chiasmocleis panamensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
Dermatonotus muelleri . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107
Elachistocleis bicolor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113
Pipidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119
Xenopus laevis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119
Morphological variation. Geometric morphometrics. Relative warp analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 124
Gut content variation. Correspondence analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 128
Gut content-morphology relationship. Partial canonical phylogenetic ordination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130

Accepted by M. Vences: 3 Aug. 2007; published: 28 Sept. 2007

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DISCUSSION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132
Interspecific variation. Morphology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132
Interspecific variation. Diet . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 144
Ecomorphological considerations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147
CONCLUSIONS AND PERSPECTIVES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162
ACKNOWLEDGMENTS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 166
REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 166

Index of Figures per species


Figure 4. Chaunus arenarum. Chondrocranium and hyobranchial skeleton. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
Figure 5. Chaunus arenarum. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
Figure 6. Chaunus arenarum. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
Figure 7. Chaunus spinulosus. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
Figure 8. Chaunus spinulosus. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
Figure 9. Chaunus spinulosus. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
Figure 10. Chaunus spinulosus. Oral apparatus and buccopharyngeal cavity. SEM micrographies. . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
Figure 11. Ceratophrys cranwelli. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
Figure 12. Ceratophrys cranwelli. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
Figure 13. Ceratophrys cranwelli. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30
Figure 14. Ceratophrys cranwelli. Oral apparatus and buccopharyngeal cavity. SEM micrographies. . . . . . . . . . . . . . . . . . . . . . . . . . 31
Figure 15. Lepidobatrachus llanensis. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32
Figure 16. Lepidobatrachus llanensis. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35
Figure 17. Lepidobatrachus llanensis. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36
Figure 18. Lepidobatrachus llanensis. Oral apparatus and buccopharyngeal cavity. SEM micrographies . . . . . . . . . . . . . . . . . . . . . . 37
Figure 19. Telmatobius cf. atacamensis. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
Figure 20. Telmatobius cf. atacamensis. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
Figure 22. Telmatobius cf. atacamensis. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
Figure 23. Dendropsophus microcephalus. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44
Figure 24. Dendropsophus microcephalus. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47
Figure 25. Dendropsophus microcephalus. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48
Figure 26. Dendropsophus nanus. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49
Figure 27. Dendropsophus nanus. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52
Figure 28. Dendropsophus nanus. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53
Figure 29. Dendropsophus nanus. Oral apparatus and buccopharyngeal cavity. SEM micrographies . . . . . . . . . . . . . . . . . . . . . . . . . 54
Figure 30. Hypsiboas rosenbergi. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55
Figure 31. Hypsiboas rosenbergi. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58
Figure 32. Hypsiboas rosenbergi. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59
Figure 33. Hypsiboas rosenbergi. Oral apparatus and buccopharyngeal cavity. SEM micrographies . . . . . . . . . . . . . . . . . . . . . . . . . . 60
Figure 34. Lysapsus limellum. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
Figure 35. Lysapsus limellum. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65
Figure 36. Lysapsus limellum. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66
Figure 37. Phyllomedusa hypochondrialis. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68
Figure 38. Phyllomedusa hypochondrialis. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69
Figure 39. Phyllomedusa hypochondrialis. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72
Figure 40. Phyllomedusa sauvagii. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
Figure 41. Phyllomedusa sauvagii. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76
Figure 42. Phyllomedusa sauvagii. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
Figure 43. Pseudis paradoxus. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79
Figure 43. Pseudis paradoxus. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
Figure 45. Pseudis paradoxus. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
Figure 46. Scinax boulengeri. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 84
Figure 47. Scinax boulengeri. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
Figure 48. Scinax boulengeri. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
Figure 49. Scinax boulengeri. Oral apparatus and buccopharyngeal cavity. SEM micrographies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89
Figure 50. Scinax nasicus. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90
Figure 51. Scinax nasicus. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93
Figure 52. Scinax nasicus. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94
Figure 53. Scinax nasicus. Oral apparatus and buccopharyngeal cavity. SEM micrographies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
Figure 54. Physalaemus santafecinus. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96
Figure 55. Physalaemus santafecinus. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
Figure 56. Physalaemus santafecinus. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
Figure 57. Physalaemus santafecinus. Oral apparatus and buccopharyngeal cavity. SEM micrographies . . . . . . . . . . . . . . . . . . . . . 101

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Figure 58. Chiasmocleis panamensis. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
Figure 59. Chiasmocleis panamensis. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
Figure 60. Chiasmocleis panamensis. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
Figure 61. Chiasmocleis panamensis. Oral apparatus and buccopharyngeal cavity. SEM micrographies . . . . . . . . . . . . . . . . . . . . . . 107
Figure 62. Dermatonotus muelleri. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108
Figure 63. Dermatonotus muelleri. Musculature. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111
Figure 64. Dermatonotus muelleri. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 112
Figure 66. Elachistocleis bicolor. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 114
Figure 67. Elachistocleis bicolor. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 117
Figure 68. Elachistocleis bicolor. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118
Figure 69. Xenopus laevis. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119
Figure 70. Xenopus laevis. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122
Figure 71. Xenopus laevis. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123

Abstract
I studied anatomy, gut content, and the relationship among these traits in a set of anuran tadpoles. Larval stages (mainly
Gosner stages 3136) of nineteen species from various lentic environments were selected. Morphological characters
from the skeleton, musculature, oral apparatus and buccopharyngeal cavity were recorded, and a gut content analysis was
performed, with emphasis on food size distribution. Ordination techniques were applied in order to find patterns of similarity in morphology and gut content. Canonical ordination methods were used to investigate the relationship among gut
content, morphology, and phylogeny in the species considered. The results show that several skeletal, muscular, and buccal characters are relatively maintained within genera. Other features, which have appeared independently in different
lineages, reflect convergence phenomena in some cases related to ecological aspects. The configuration of the hyobranchial skeleton, the development of the buccal floor depressor and levator muscles, and mouth gape width correlate with
prey size. In some species, morphology is clearly related with feeding. Tadpoles that ingest large food particles relative to
their body length present morphological traits attributable to macrophagy. Taxonomically unrelated tadpoles of Dendropsophus nanus, D. microcephalus and Ceratophrys cranwelli possess hyobranchial skeletons with robust, rostrocaudally
long ceratohyals and reduced branchial baskets with short ceratobranchials devoid of lateral projections and spicules.
Lepidobatrachus llanensis tadpoles have laterally extended ceratohyals which, along with the lateral extension of the
jaws, result in a very wide oral apparatus and an ample buccopharyngeal cavity that allows the tadpole to ingest large and
whole prey; the branchial basket, although its ceratobranchials lack lateral projections and spicules, is slightly reduced in
area. The four species mentioned have a noticeable development of the buccal floor depressor muscles, and buccal cavities with scarce filtering and entrapping structures. In Elachistocleis bicolor, Dermatonotus muelleri, Chiasmocleis panamensis, and Xenopus laevis tadpoles, the branchial basket occupies >70% of the total hyobranchial skeleton area, and
the hypobranchial plates are highly reduced; the buccal floor levator muscles are well-developed, with an increased site
of attachment on the ventral expansion of the lateral process of the ceratohyal; the scarcity of the filtering structures in
the buccopharyngeal cavity are balanced with the great development of the branchial filters and secretory zones; all these
features relate to a diet based on small particles not significantly different from those of most other species; however,
experimental studies show that species with similar hyobranchial apparatus and muscles are the most efficient when
retaining minute particles. Finally, a large group of species present generalized morphological characters, such as a branchial basket occupying about 50% of the total hyobranchial apparatus, intermediate values of mouth gape width and buccal floor levator / depressor muscles ratio, and abundant filtering structures in the buccopharyngeal cavity; these species
feed frequently on food particles between 130% of the tadpole body length; however, in some of the species, macrophagous diets are also reported in the literature, indicating that this morphology is flexible in more ample prey size ranges.
Key words: tadpoles; chondrocranium; hyobranchial skeleton; musculature; oral apparatus; buccopharyngeal cavity; gut
content; interspecific variation; ecomorphology

Introduction
Morphological diversity in anuran larvae and its relationship with spatial and trophic features lead to convergence phenomena, and this allowed researchers to group some species according to morphological and eco-

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logical parameters. Altig and Johnston (1989; updated in McDiarmid & Altig 1999) considered that, among
exotrophic species from lotic and lentic environments, there exist several categories defined on the basis of
general morphological characters, such as body shape, eye position, and configuration and orientation of the
oral disc. Lentic larvae include groups such as benthic, nektonic, neustonic, arboreal, carnivores, macrophagous, suspension-rasper, and suspension feeder tadpoles. Most of these categories are based on morphological
similarity and on known or presumable information about larval feeding and ecology. Other researchers have
found that not only external, but internal features can be related to anuran larvae ecology. Thus, some studies
inquire into the relation between buccal or musculoskeletal features and feeding habits (Wassersug 1980;
Satel & Wassersug 1981; Hall et al. 2002; Alcalde & Rosset 2003; Vera Candioti & Haas 2004; Vera Candioti
et al. 2004; Vera Candioti 2005) and between internal morphology and microhabitat (Noble 1929; Haas &
Richards 1998).
Ecomorphological studies are based on the analysis of morphological and ecological variables and the
relationship between them. The hypothesis that underlies such an approach holds that morphological variation
corresponds with ecological variation (Harmon et al. 2005). In other words, linked to certain ecological
aspects, there appear to be morphological characters capable of determining ranges of resource intake in some
of the environment dimensions: temporal, spatial or trophic. To address an ecomorphological approach, variation should be quantified first. As regards morphology, most of studies on tadpoles are qualitative in nature
(Larson 2002), and interspecific variation studies often inherit the qualitative character of particular descriptions. In skeletal morphology, geometric morphometric methods offer an approach complementary to qualitative studies, and combined with several statistical multivariate tests, allow for quantitative study of shape
variation. In zoology, these methods have been employed to describe shape change associated to ontogeny and
allometry (e.g., Monteiro & Abe 1997; Monteiro et al. 1999; Larson 2002, 2005), variation among populations, sexes, species (e.g., Rohlf 1993; Fink & Zelditch 1995; Swiderski et al. 1998; Zelditch & Fink 1998;
Monteiro & Abe 1999; Corti et al. 2000; Marcus et al. 2000; Baylac et al. 2003; Frie 2003; Giri & Collins
2004; Zelditch et al. 2004; Anderson & Roopnarine 2005; Beszteri et al. 2005; Stayton 2005; Vera Candioti et
al. 2007), and morphological variation related to ecological features (e.g., Adams and Rohlf 2000; Claude et
al. 2004; Dayton et al. 2005). On the other hand, in several studies that analyze the morphology-ecology relation, although morphology is exhaustively examined, ecological variables are described qualitatively or
inferred from morpho-functional aspects. Some studies, however, quantify both sets of variables, and perform
statistical tests to investigate the relation among them; studies of this kind have been carried out mainly on
fishes (e.g., Motta et al. 1995b; Wainwright & Richard 1995; Shoup & Hill 1997; Clifton & Motta 1998; Huysentruyt et al. 2004).
Studies on lentic tadpoles include many aspects, such as taxonomy, morphology, histology, physiology,
ecology and ethology. In the Argentine fauna, a particular emphasis has been put on morphological characters
of the cartilaginous skeleton, oral apparatus and buccopharyngeal cavity (e.g., Fiorito de Lpez & Echeverra
1984; 1989; Lavilla 1987; 1991; 1992a,b; Lavilla & Fabrezi 1987; 1992; Echeverra 1992; 1997a,b; Fabrezi &
Lavilla 1992; 1993; Fabrezi & Garca 1994; Lavilla & Langone 1995; Fabrezi & Vera 1997; Lavilla & Vaira
1997; Alcalde & Rosset 1998; 2003; Lavilla & De S 1999; Perotti & Cspedez 1999; Echeverra & Lavilla
2000; Sandoval 2000; Alcalde 2001). Muscle studies were long ignored, but in recent years interest has been
revived; there are some studies on individual species and comparative approaches (e.g., Palavecino 1997;
1999; 2000; Vera Candioti 2004; Vera Candioti & Haas 2004; Alcalde 2005; Alcalde & Barg 2006). Larval
morphology is proving useful in the reconstruction of phylogenetic relationships (e.g., Larson & De S 1998;
Maglia et al. 2001; Haas 2003; Pgener et al. 2003), and comprehensive studies, at supraspecific levels, are an
interesting contribution to help resolve relationships in understudied groups. As to feeding, this issue is
addressed in papers on diet, digestive tract morphology, and behavior of some species (e.g., Lavilla 1983a;
Tern & Michel de Cerasuolo, 1988; Lajmanovich 1994; 1997; 1998; Lajmanovich & Fernndez 1995; Vera
Candioti & Lajmanovich 1998; Arias et al. 2002). Despite the abundance of data, very few studies integrate

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the aforementioned aspects (e.g., Ruibal & Thomas 1988; Vera Candioti 2004; 2005).
For all of the above, it is of interest to investigate the internal morphology in anuran larvae and its relationship with the feeding habits. I selected a set of lentic exotrophic species that may be assigned to the ecomorphological guilds proposed by Altig and Johnston (1989) and Altig and McDiarmid (1999a,b); the study
of internal morphology and a quantitative analysis of gut content composition may afford additional information to help redefine these categories. Most larvae I studied are common inhabitants from varied regions from
Argentina, and five species from other geographic regions have been included. Chaunus arenarum, C. spinulosus, Telmatobius cf. atacamensis, Hypsiboas rosenbergi, and Physalaemus santafecinus are generalized
pond tadpoles that live mostly at or near the bottom; Lysapsus limellum, Phyllomedusa hypochondrialis, P.
sauvagii, Pseudis paradoxus, Scinax boulengeri, and S. nasicus larvae live somewhere within the water column and feed by filtering suspended particles and rasping submerged surfaces; Ceratophrys cranwelli and
Lepidobatrachus llanensis are carnivorous tadpoles that inhabit temporary ponds in arid regions from Northwestern Argentina; Dendropsophus nanus and D. microcephalus are small hylid tadpoles, known to be midwater macrophagous forms; Chiasmocleis panamensis, Dermatonotus muelleri, Elachistocleis bicolor, and
Xenopus laevis tadpoles feed by floating in the water column and pumping water through buccopharyngeal
structures to entrap suspended particles. First in this work, I provide basic information about anatomy and gut
content of these nineteen species; regarding morphology, I included descriptions of the chondrocranium, hyobranchial skeleton, associated musculature, oral apparatus and buccopharyngeal cavity, recording some traits
from which it is possible to infer functional mechanisms, related to prey capture and handling; regarding feeding, I studied gut content composition, including its vegetal and animal contents, and prey size distribution.
Second, I analyzed interspecific variation in morphology and gut content in order to discern patterns that can
be later correlated. Results are finally compared to ecomorphological groups proposed by other researchers.
This work supplies data that could be useful to several fields; at the same time, numerous questions which
could be addressed from multiple disciplines such as developmental biology, systematics and ecology arise.

Materials and Methods


Specimens
I studied tadpoles of nineteen species from lentic environments. I selected Gosner stages 3136 (Gosner
1960; Period V, according to Fabrezi 1988), and when these stages were not available, I analyzed the adjacent
younger and older tadpoles. Species were selected according to the guilds mentioned by Altig and Johnston
(1989) and Altig and McDiarmid (1999a,b). The species analyzed and the corresponding guilds are shown in
Table 1 and Figure 1. Larvae were collected with a net, fixed with 10% formalin, and then processed for further analyses. All dissections and drawings were made with a stereomicroscope and a camera lucida. Species
naming is that employed in Frost (2007). In the case of Chaunus species, results in the recent paper by Chaparro et al. (2007) suggest that most species groups of South American toads should wear the precedent name
Rhinella; in the present work, the name Chaunus is maintained waiting for further systematic studies on the
family.
Chondrocranium and hyobranchial skeleton
Specimens were cleared and stained following the Wassersug (1976a) protocol. Measurements were
recorded from digital images, with the software Image Tool (Wilcox et al. 1995). Skeletal terminology is that
employed by Haas (2003). Latin terms are used only if English terms were not available.

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FIGURE 1. Tadpoles of 19 species studied, grouped according to the ecomorphological guilds of Altig & Johnston (1989). CA Chaunus arenarum, CC Ceratophrys cranwelli, CP Chiasmocleis panamensis CS Chaunus spinulosus, DM Dendropsophus microcephalus,
DN Dendropsophus nanus, DRM Dermatonotus muelleri, EB Elachistocleis bicolor, HR Hypsiboas rosenbergi, LL Lysapsus limellum, LLL Lepidobatrachus llanensis, PH Phyllomedusa hypochondrialis, PHS Phyllomedusa sauvagii, PP Pseudis paradoxus, PS
Physalaemus santafecinus, SB Scinax boulengeri, SN Scinax nasicus, TA Telmatobius cf. atacamensis, XL Xenopus laevis. Scale lines
= 1 mm.

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TABLE 1. Studied species and guilds assigned according to Altig and Johnston (1989) and Altig and McDiarmid
(1999a,b).
Site

Date

Guild

Chaunus arenarum

Salta, Argentina

December 2003

15

benthic

Chaunus spinulosus

Jujuy, Argentina

November 2001

15

benthic

Salta, Argentina

December 2003

15

carnivore

Salta, Argentina

January 1996

10

Lepidobatrachus llanensis

Salta, Argentina

November 1996

carnivore

Telmatobius cf. atacamensis

Salta, Argentina

November 2003

benthic

Dendropsophus microcephalus

Gamboa, Panam

July-August 2001

macrophagous

Dendropsophus nanus

Santa Fe, Argentina

January-February 2001

15

macrophagous

Hypsiboas rosenbergi

Gamboa, Panam

July-August 2001

benthic

Lysapsus limellum

Santa Fe, Argentina

January-February 2001

nektonic

Phyllomedusa hypochondrialis

Formosa, Argentina

January 2004

suspension-rasper

Phyllomedusa sauvagii

Salta, Argentina

January 2005

10

suspension-rasper

Pseudis paradoxus

Formosa, Argentina

January 2004

nektonic

Scinax boulengeri

Gamboa, Panam

July-August 2001

suspension-rasper

Scinax nasicus

Santa Fe, Argentina

January-February 2001

15

suspension-rasper

Santa Fe, Argentina

January-February 2001

15

benthic

Chiasmocleis panamensis

Gamboa, Panam

July-August 2001

15

suspension-feeder

Dermatonotus muelleri

Salta, Argentina

January 2005

15

suspension-feeder

Elachistocleis bicolor

Santa Fe, Argentina

January-February 2001

15

suspension-feeder

Captive population

December 2005

10

suspension-feeder

BUFONIDAE

CERATOPHRYIDAE
Ceratophrys cranwelli

HYLIDAE

LEIUPERIDAE
Physalaemus santafecinus
MICROHYLIDAE

PIPIDAE
Xenopus laevis

Musculature
Specimens were treated with Wassersugs protocol, with the procedure interrupted before immersion in
glycerol and then colored with lugol solution (Bck & Shear 1972; Lavilla pers. comm.). Muscle nomenclature is that employed by Haas (2003). Muscles responsible for the raising and lowering of the buccal floor,
mm. interhyoideus (ih) and orbitohyoideus (oh) were removed, and their volumes were estimated from linear
dimensions. The ih/oh ratio was calculated in order to evaluate buccal pumping abilities. According to Satel
and Wassersug (1981), buccal floor levator muscles in microphagous tadpoles are more developed than the
depressors, which results in a high ih/oh ratio. Macrophagous tadpoles exhibit larger depressor muscles, and
thus a low ih/oh ratio.
Oral apparatus and buccopharyngeal cavity
Gape width was estimated from suprarostral cartilage width, and then relativized to tadpole body length.
The buccopharyngeal cavity was exposed according to Wassersugs (1976b) method, and structures were
stained with methyl blue. Oral and buccal terminology follows that of Wassersug (1976), Altig and McDiarmid (1999a), Viertel and Richter (1999), and Altig (2007). Specimens of some species were prepared for
scanning electron microscopy according to Fiorito de Lpez and Echeverra (1984). The observations and
micrographs were made with a JEOL 35 CF scanning electron microscope.
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Gut content
Tadpole gut content was studied from specimens collected in the field. Xenopus laevis tadpoles were
reared from embryos in a tank filled with pool water until they reached Gosner stages 3136; they were next
fixed to analyze their digestive content. Digestive tracts were removed, and their contents were extracted,
diluted and homogenized in a formalin-erythrosine 3:1 solution (Lajmanovich 1994); the erythrosine is a food
dye similar to eosin Y, and it stains organic material with a conspicuous cherry-pink color. Three drops of
digestive content per tadpole were analyzed. Each food item was identified at a general taxonomic level (diatoms, chlorophytes, rotifers, etc.) and then measured with a micrometric ocular to analyze the distribution of
food item sizes. In order not to overemphasize the contribution of small prey taken in large amounts, volumes
were estimated from linear dimensions by comparison with the three-dimensional shape each item most
closely resembled (Hyslop 1980). The contribution of each item is then expressed as a percentage of the overall volume consumed. In order to define food size categories comparable among different sized-predators,
absolute food sizes were transformed to values relative to tadpole body length (distance from the tip of the
snout to the end of the body). As a result of the quantification of gut contents of all the species, a food type
matrix and a food size matrix were constructed. In these matrices, each variable (column) is a qualitative food
item or size category (size expressed as a percentage of the predator body size). Each case (row) is a species,
thus, values in cells are averages from individuals analyzed per species.
Data analysis
Morphological variation. Geometric morphometrics. Relative warp analysis. To quantify variation in the
shape of the skeletons across species, I applied the landmark-based geometric morphometric method
described in Rohlf and Bookstein (1990). On the right half of the chondrocrania and hyobranchial skeletons, a
set of landmarks was marked and digitized with the software tpsDig2 (Rohlf 2005). A requirement of geometric morphometrics method is that landmarks selected must be defined across all the specimens considered;
thus is not possible to deal with origination and elimination of structures. In the chondrocrania studied, the
wide shape variation includes appearances, losses and fusion of structures (e.g., posterolateral process of the
palatoquadrate in microhylids, fusion of trabecular horns and suprarostral cartilage in Xenopus laevis), and
this makes possible the definition of only a few comparable landmarks. Twelve landmarks in the chondrocranium and 16 in the hyobranchial skeleton are as follows (Fig. 2): Chondrocranium: (1) point of maximum
width of the base of the trabecular horns; (2) medial point of the palatoquadrate-Meckels cartilage articulation; (3) most anterior point of the quadratocranial commissure; (4) most anterior point of the muscular process of the palatoquadrate; (5) most dorsal point of the muscular process; (6) most lateral, medial point of the
muscular process; (7) most posterior point of the muscular process; (8) most anterior point of the subocular
fenestra; (9) most anterior point of the otic capsule; (10) most lateral point of the otic capsule; (11) most posterior point of the otic capsule; (12) most medial point of the otic capsule; Hyobranchial skeleton: (1) anterior
margin of pars reuniens; (2) tip of the anterior process; (3) tip of anterolateral process; (4) articular condyle;
(5) most lateral internal point of branchial basket; (6) most posterior point of branchial slit I; (7) most posterior point of branchial slit II; (8) most caudal and medial point of ceratobranchial III; (9) most rostral and
medial point of ceratobranchial IV; (10) most caudal point of hypobranchial plates junction; (11) most caudal
point of basibranchial; (12) lateral point of hypobranchial plate - basibranchial junction; (13) tip of the posterior process; (14) most caudal point of ceratobranchial I - hypobranchial plate junction; (15) most caudal point
of ceratobranchial II - hypobranchial plate junction; (16) most caudal point of ceratobranchial III hypobranchial plate junction.
The configurations of landmarks were next translated, standarized to centroid size = 1, and aligned
through the generalized Procrustes analysis (GPA) to produce a consensus configuration, with tpsRelw (Rohlf
2003). A relative warp analysis (RWA, i.e., principal component analysis on the residuals from superimposition) was performed to obtain a plot of specimens scattered in a space defined by variation axes (the relative

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warps). Variation in shapes was depicted with thin-plate spline deformation grids which reveal the modified
shape compared to the consensus configuration, using tpsSplin (Rohlf 2004). For detailed explanations on this
methodology, see Rohlf and Bookstein (1990), Bookstein (1991), Fink and Zelditch (1995), Monteiro and
Furtado dos Reis (1999), Adams et al. (2004), and Zelditch et al. (2004).

FIGURE 2. Landmarks recorded on the chondrocranium, dorsal view (left), and hyobranchial skeleton, ventral view (right) of tadpoles of each species. A lateral portion of the ceratohyal, B ceratohyal width, CB ceratobranchials area, CH ceratohyal area, HP hypobranchial area. Landmarks, see definition in text.

For comparative purposes, some measurements with functional correlations with feeding were recorded
for the hyobranchial skeletons: in-lever arm proportion: lateral portion of the ceratohyal (distance between the
tip of the lateral process and the articular condyle) projected on the total width of the ceratohyal; ceratohyal
area, defined by the landmarks 14, 1113; hypobranchial area, defined by the landmarks 4, 916; and ceratobranchial area, defined by the landmarks 49, 1416 (Fig. 2). The in-lever arm proportion gives an idea of the
mechanical advantage of the ceratohyals during the lowering and raising of the buccal floor, and the hyobranchial areas indicate the relative importance of the suction and filtering processes. The measurements were
taken from drawings or photographs, with Image Tool (Wilcox et al. 1995).
Gut content variation. Correspondence analysis. As was the case with morphological variables, an ordination technique was applied to food variables. Correspondence analysis (CA) is suitable to analyze census
matrices, where ordination is based on the common proportions of the variables considered (Jongman et al.
1995; Giannini 1999). In this case, two matrices were considered, and values on the matrices were the abundance of food particles of each type or size in each tadpole. The interpretation of the output and plots of CA is
similar to that of other indirect ordination techniques.
Gut content-morphology relationship. Partial canonical phylogenetic ordination. In the data matrix, there
are two independence problems which violate the basic assumption of any subsequent statistical test. Firstly,
to work with species as sample units requires one to consider the phylogenetic relationships among them.
Giannini (2003) proposed a phylogenetic comparative method by which the set of species is codified in a phylogenetic structure matrix (assigning 0s and 1s according to their belonging to monophyletic clades); this
matrix can then be employed as an external or covariate matrix in statistical tests. I worked with the phylogenetic hypothesis proposed for Anura by Frost et al. (2006), and in the case of microhylids, the phylogeny by
Donnelly et al. (1990) was considered (Fig. 3). Secondly, the use of ordination axes (PCs, RWs, etc.) as variables in statistical tests implies a problem of non-independence of the scores on the axes. This can be treated
with permutation methods, which test the significance of variables through resampling.
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FIGURE 3. Phylogenetic hypothesis for Anura based in Frost et al. (2006) and Donnelly et al. (1990), employed for phylogenetic
canonical ordination method (Giannini 2003).

I tested the relationship between food size, predator morphological characters, and phylogeny by performing a partial canonical phylogenetic ordination (pCPO; Giannini 2003), a variant of the canonical correspondence analysis (CCA). The CCA combines a correspondence analysis with a multiple regression (Ter Braak
1986; Jongman et al. 1995; McGarigal et al. 2000) so that given two sets of variables (main and external
matrices), it ordinates the first set on axes that are linear combinations of variables of the second set. In this
way, the analysis extracts the major gradients in the data that can be accounted for by explanatory variables. If
a second external matrix is included (partial CCA pCCA or partial CPO if a phylogenetic matrix is
involved), variation can be partitioned and percentages exclusive and shared by each external matrices are
obtained. In this study, the main matrix includes food data; variables are the percentages of food sizes
expressed as a percentage of tadpole body length. The first external matrix joins morphological variables from
the hyobranchial skeleton, musculature and buccopharyngeal cavity; variables are: hyobranchial skeleton
shape (summarized as the scores of specimens on the first relative warps resulting from hyobranchial skeleton
RWA; the number of warps retained is such that at least 90% of variation is accumulated), ih/oh ratio, mouth
gape, and total number of filtering structures inside the buccal cavity. The chondrocranium shape, quantified
through landmark-based geometric morphometrics, was not included, because the landmarks selected are not
representative of the total shape variation; they exclude important shape changes associated with appearance,
disappearance and fusion of structures. Additionally, information supplied by these landmarks is partially
redundant with that provided by other variables included in the analysis (e.g., size of muscular process of the
palatoquadrate, described by landmarks 47, is usually associated with the development of the m. orbitohyoideus; the articulation between Meckels cartilage and the palatoquadrate, described by landmark 2, gives an
approximate idea of mouth gape). Morphological variables were standarized to fulfill the non-dimensionality
required by linear combination. Finally, the second external matrix is a phylogenetic matrix constructed by
Giannini (2003) method, considering the anuran phylogeny of Frost et al. (2006). The significance of morphological variables and taxonomic groups was tested through a Monte Carlo permutation test. Including the sig-

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nificant variables, a pCPO was performed, to identify variation explained by morphology, by phylogeny, and
the shared variation. The pCPO was performed adding variables successively (forward stepwise), which
yielded an economic model to explain the variation in the main matrix with a minimum of external variables.
The graphic output of these analyses is a triplot, an ordination plot where tadpole species, food and morphological variables are placed in a space defined by ordination axes.
Ordination and canonical ordination analyses were performed with CANOCO 4.5 (Ter Braak & Smilauer
1997); statistical analyses were performed with SPSS 9.0 (1998) and STATISTICA 6.0 (2001).

Results
Morphological descriptions
In order to present equivalent information for each taxon and to consign data not supplied or different from
those that appear in previous studies, complete descriptions for each species are included, as well as a list of
previous publications.

BUFONIDAE
Chaunus arenarum. Previous literature on the skeleton and musculature of this species includes Fabrezi and
Vera (1997) and Haas (2003); the oral apparatus was described in Fiorito de Lpez and Echeverra (1984;
1989). Lajmanovich (1998) studied the qualitative composition of the diet.
Chondrocranium and hyobranchial skeleton (N = 5, stages 3336. Fig. 4). The chondrocranium of these
larvae represents 43% of the body length. The maximum width is at the level of posterior part of the subocular
bar. The suprarostral cartilage has a single, U-shaped corpus that is fused dorsally to the alae. The alae are
well-defined, ventrally rounded, and bear a well-developed processus dorsalis posterior. The trabecular horns
are long (24% of the total length of the chondrocranium) and narrow, and diverge from the ethmoid plate.
They show relatively straight anterior margins, and on the lateroventral margin, the processus lateralis trabeculae is slightly outlined. The cranial floor is completely cartilaginous, with thin cartilage in the central area.
The carotid and craniopalatine foramina are not clearly identifiable because of the light chondrification of the
intertrabecular plate. In the posterior margin of the cranial floor, the notochordal canal reaches 20% of the
chondrocranium length. The lateral walls of the chondrocranium are formed by the orbital cartilages. The
chondrocranium is open dorsally, and the frontoparietal fenestra is bordered on both sides by the taeniae tecti
marginales. The otic capsules are ovoid, occupy nearly 29% of the chondrocranium total length, and bear an
acute anterolateral process. A large fenestra ovalis (45% of capsule length) is located ventrolaterally on each
otic capsule. The otic capsules are dorsally joined by the tectum synoticum. The palatoquadrate is long and
relatively narrow. It has a long, thin articular process, and a wide, dorsally rounded muscular process. The
subocular bar has a smooth margin and it is posterolaterally rounded. The palatoquadrate attaches to the braincase via three points: the quadratocranial commissure, the quadratoorbital commissure, and the ascending process. The quadratocranial commissure is thin and bears a well-developed, triangular quadratoethmoid process.
The ascending process attaches to the braincase ventral and posterior to the oculomotor foramen (low attachment). The lower jaw includes the Meckels and infrarostral cartilages joined by a cartilaginous intermandibular commissure. Meckels cartilages are sigmoid, with dorsomedial and ventromedial processes, and articulate
with the articular process via the retroarticular process. The infrarostral cartilages are short, rectangular and
independent. In the hyobranchial skeleton, the ceratohyals are long and have a tall anterior process, a rounded
anterolateral process, an acute lateral process, and a large and wide posterior process; the articular condyle is
a rounded, robust projection visible from a dorsal view. The ceratohyals are joined medially by the pars reuANATOMY OF ANURAN TADPOLES

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niens that is shorter than the basibranchial. The basihyal is small, visible as a narrow sliver of cartilage, and
the basibranchial is long and bears a short urobranchial process (18% of the basibranchial length). The hypobranchial plates are flat and triangular, and they articulate medially leaving a posterior ovoid gap. The ceratobranchials are long, thin, and have numerous lateral projections. They are distally joined by terminal
commissures. Four cartilaginous spicules arise dorsally from each ceratobranchial.

FIGURE 4. Chaunus arenarum, stage 34. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B) Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral cartilage. A ala, ALPC anterolateral process of ceratohyal, ALPO anterolateral process of otic capsule, APC anterior process of ceratohyal,
ARP articular process, ASP ascending process, BB basibranchial, BH basihyal, C corpus, CB(I-IV) ceratobranchial, CH ceratohyal,
FF frontoparietal fenestra, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral cartilage, LPC lateral process of ceratohyal, LPT
lateral process of trabecular horn, MC Meckels cartilage, MP muscular process, NC notochordal canal, OC otic capsule, PDP processus dorsalis posterior, PPC posterior process of ceratohyal, PR pars reuniens, QCC quadratocranial commissure, QOC quadratoorbital
commissure, QP quadratoethmoid process, RP retroarticular process, S spicule, SB subocular bar, SC suprarostral cartilage, SF subocular fenestra, TC terminal commissure, TH trabecular horn, TS tectum synoticum, TTM taenia tecti marginalis, UP urobranchial process. Scale lines = 1 mm.

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Musculature (N = 5, stages 3336. Table 2 and Fig. 5). Thirty-one muscles are present in this species.

TABLE 2. Chaunus arenarum, stages 3336. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

ventromedial region of Meckels cartilage lower lip of


the oral disc

it consists of a single slip,


corresponding to m. mandibulolabialis
inferior

Intermandibularis

medial region of Meckels cartilage


median aponeurosis

the whole structure is U-shaped, and


consists of a few fibers, loosely
disposed

Levator mandibulae longus


superficialis

external and posterior margin of the subocular bar


dorsomedial region of Meckels cartilage

Levator mandibulae longus


profundus

external margin of the subocular bar and part of the


ascending process of the palatoquadrate external margin
of the ala of the suprarostral

the area of origin is smaller than that


of the m. l. m. l. superficialis, and
insertion is through a well-developed,
long tendon

Levator mandibulae
internus

ventral surface of the ascending process distal edge of


Meckels cartilage

the insertion is via a long tendon

Levator mandibulae
externus superficialis

medial, inferior surface of the muscular process


mandibulosuprarostral ligament

the mandibular branch of the


trigeminal nerve (V3) runs ventrally to
this muscle

Levator mandibulae
externus profundus

medial, inferior surface of the muscular process


lateroventral margin of the ala
of the suprarostral

it originates ventrally regarding the


former muscle, and it is more
developed; its insertion is via a tendon
shared with the m. l. m. l. profundus

Levator mandibulae
articularis

inferior part of the medial surface of the muscular process


dorsal surface of the lateral edge of Meckels cartilage

Levator mandibulae
lateralis

articular process of the palatoquadrate dorsal, lateral


edge of the suprarostral

it is a short muscle, formed of a few


fibers, slightly more developed than
the m. l. m. e. superficialis

Suspensoriohyoideus

posterior descending margin of the muscular process


posterior surface of the lateral
process of the ceratohyal

it is a compact and well-developed


muscle

Orbitohyoideus

anterior, dorsal margin of the muscular process lateral


edge of the ceratohyal

Suspensorioangularis

inferior, lateral part of the descending margin


of the muscular process
retroarticular process of Meckels cartilage

the site of origin is concealed by the


m. orbitohyoideus; fibers occupy
approximately the lower quarter of the
muscular process

Quadratoangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

it is completely covered by the m.


hyoangularis

Hyoangularis

dorsal surface of the ceratohyal, anterior to the articular


condyle retroarticular process of Meckels cartilage

it is a thin muscle

Interhyoideus

ventral surface of the ceratohyal, near the


lateral edge median aponeurosis

it is formed of parallel, transverse


fibers, disposed in a plane nearly
perpendicular to the chondrocranial
longitudinal axis

Geniohyoideus

posterior, ventral surface of the infrarostral


hypobranchial plates
...... continued

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TABLE 2 (continued)
Muscle

Insertions

Comments

Levator arcuum
branchialium I

lateral margin of the subocular bar ceratobranchial I

it is the widest of the mm. l. a.


branchialium; its insertion onto the
ceratobranchial occupies a large
surface

Levator arcuum
branchialium II

subocular bar terminal commissure I

Levator arcuum
branchialium III

lateroventral part of the otic capsule terminal


commissure II

Levator arcuum
branchialium IV +
Tympanopharyngeus

the distinction between these two muscles is not clear;


from the posterolateral surface of the otic capsule, two
well-differentiated slips arise: the lateral slip inserts on the
medial margin of the ceratobranchial IV, and the medial
slip inserts on the medial margin of the ceratobranchial IV
and connective tissue of the pericardium

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process II terminal commissure I

Constrictor branchialis III

branchial process II terminal commissure II

it is disposed on the ceratobranchial II

Constrictor branchialis IV

branchial process II terminal commissure III

it is disposed on the ceratobranchial


III; in the insertion on the branchial
process II, fibers confuse with those of
the m. c. b. II

Subarcualis rectus I

three slips: lateral base of the posterior process of the


ceratohyal proximal part of the ceratobranchial I (dorsal
slip), branchial process II (ventral1 slip), and branchial
process III (ventral2 slip)

Subarcualis rectus II-IV

branchial process II proximal, ventral part of the


ceratobranchial IV

Subarcualis obliquus

urobranchial process branchial process II

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum branchial process III

Rectus abdominis

peritoneum pelvic griddle

in the anterior insertion, some fibers


are continuous with those of the
ventral2 slip of the m. s. r. I; some
lateral fibers diverge and insert
posteriorly, on the distal part of the
ceratobranchial IV

it is well-developed; it originates
almost at the level of the branchial
basket

FIGURE 5. Chaunus arenarum, stage 34. Musculature (A) Dorsal view, superficial plane, (B) Dorsal view, middle plane, (C) Dorsal
view, deep plane, (D) Ventral view, (E) Lateral view, superficial plane, (F) Lateral view, deep plane, (G) Ventral view, whole. CB(IIIV) constrictor branchialis, GH geniohyoideus, HA hyoangularis, IH interhyoideus, IM intermandibularis, LB(I-IV) levator arcuum
branchialium, LMA levator mandibulae articularis, LMEP levator mandibulae externus profundus, LMES levator mandibulae externus superficialis, LMI levator mandibulae internus, LML levator mandibulae lateralis, LMLP levator mandibulae longus profundus,
LMLS levator mandibulae longus superficialis, ML mandibulolabialis, OH orbitohyoideus, QA quadratoangularis, RA rectus abdominis, SA suspensorioangularis, SH suspensoriohyoideus, SO subarcualis obliquus, SRI subarcualis rectus I, SRII-IV subarcualis rectus
II-IV, TP tympanopharyngeus. Scale lines = 1 mm.

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FIGURE 6. Chaunus arenarum, stage 34. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B) Buccal roof, (C)
Buccal floor. BFA buccal floor arena, BFAP buccal floor arena papilla, BP buccal pocket, BRA buccal roof arena, BRAP buccal roof
arena papilla, C choana, DG dorsal gap, DV dorsal velum, GZ glandular zone, ILP infralabial papilla, IR infrarostrodont, LK lower
keratodonts, LP lingual papilla, LRP lateral ridge papilla, MP marginal papilla, MR median ridge, P pustulation, PNA prenarial arena,
PTNA postnarial arena, PTNP postnarial papilla, S spur, SR suprarostrodont, TA tongue anlage, UK upper keratodonts, VG ventral
gap, VV ventral velum. Scale lines = 1 mm.

Oral apparatus and buccopharyngeal cavity (N = 2, stage 35. Fig. 6). The width of the oral disc represents nearly 22% of the body length, and gape width reaches 22% of the body length. The oral disc is emarginate, with a simple papillar margin interrupted in wide dorsal and ventral gaps; there are a few submarginal
papillae in the commissural region. Papillae are conical, with smooth, rounded tips. The rostrodonts are welldeveloped and keratinized. The keratodonts are arranged in five rows, two upper (anterior) and three lower
(posterior), resulting in a labial tooth row formula LTRF 2(2)/3. Row A2 is interrupted by a wide, median
gap, and P3 is slightly shorter than the other rows. In the buccal roof, the prenarial arena has a quadrangular,
short and wide ridge. The choanae are large, obliquely arranged at an angle of 40 from the transversal line.
The anterior margin has small prenarial papillae, and the narial valve is visible. In the postnarial arena there
are four pairs of conical postnarial papillae, the two most anterior pairs smaller and closer to each other. The
lateral ridge papillae are well-developed and trifid, with pustulate tips. The median ridge is triangular, high,
wider at the base, and with an irregular free margin. The buccal roof arena is delimited on both sides by 45
tall, conical marginal papillae; numerous pustules are scattered among the papillae. The secretory pits are
arranged in a V-shaped display located near the posterior margin of the dorsal velum. The dorsal velum is
short and it has a smooth margin, without projections. In the buccal floor, posteriorly to the infrarostrodonts,
there is a pair of small, non-keratinized spurs, medially directed. The infralabial papillae are tall, bifid, and
with tips of unequal development, and they do not overlap each other in the middle line. On the tongue anlage,
there are four lingual papillae; they are tall, conical, and transversally aligned, and the medial pair is slightly

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shorter than the lateral one. The prepocket region, on the lateral portion of the ceratohyals, shows numerous
pustules and one pair of prepocket papillae. The buccal floor arena is delimited on both sides by 1214 tall
papillae accompanied by numerous pustules and small papillae. The buccal pockets are elongate and transversally arranged. The ventral velum is semicircular and supported by spicules. Three main marginal projections
appear on each side, over each filter plates; the median notch is absent, and secretory pits appear on the edge
of the velum.
Gut content (N = 8, stages 3436. Tables 21 and 22). The most frequent food items were diatoms
(41.39%), followed by ciliates and oligochaete remnants. Regarding food sizes, the highest percentages
ranged from below 1-2% of the tadpole body length. The abundance of sand-grains in the gut contents suggests bottom feeding.
Chaunus spinulosus. Ulloa Kreisel (2003) described the buccopharyngeal cavity of this species; the remaining
data are unpublished.
Chondrocranium and hyobranchial skeleton (N = 5, stages 34 and 36. Fig. 7). The chondrocranium of
these larvae represents 57% of the body length. The maximum width is at the level of posterior part of the subocular bar. The suprarostral cartilage has a single, U-shaped corpus dorsally fused to the alae. The alae are
well-defined, ventrally rounded, and bear an acute processus dorsalis posterior. The trabecular horns correspond to nearly 23% of the total length of the chondrocranium and diverge from the ethmoid plate. They have
relatively straight anterior margins, and on the lateroventral margin, the processus lateralis trabeculae is
slightly outlined. The cranial floor is completely cartilaginous with thin cartilage in the central area. The
carotid foramen is visible, but the craniopalatine foramen is not clearly identifiable, because of light chondrification of the intertrabecular plate. On the posterior margin of the cranial floor, the notochordal canal extends
19% of the chondrocranium length. The lateral walls of the chondrocranium are formed by the orbital cartilages. The optic foramen, posteroinferiorly placed, the oculomotor foramen, slightly smaller, and the trochlear
foramen, small and dorsally placed, are visible on the posterior part of the orbital cartilage. The chondrocranium is dorsally open through the frontoparietal fenestra lined on both sides by the taeniae tecti marginales. In
the stages analyzed, the taenia tectis transversalis and the taenia tectis medialis are also present. The otic capsules are ovoid, occupy nearly 27% of the chondrocranium total length, and bear an acute anterolateral process. A large fenestra ovalis (44% of the capsule length) is located ventrolaterally on each otic capsule. The
otic capsules are dorsally joined by the tectum synoticum. The palatoquadrate is long and relatively narrow. It
has a long and thin articular process, and a wide, dorsally rounded muscular process. The subocular bar has a
smooth margin, and it is posterolaterally wider and rounded. The palatoquadrate attaches to the braincase via
three points: the quadratocranial commissure, the quadratoorbital commissure, and the ascending process. The
quadratocranial commissure is thin and bears a well-developed, triangular quadratoethmoid process. The
ascending process attaches to the braincase ventrally and posteriorly to the oculomotor foramen (low attachment). The lower jaw includes Meckels and infrarostral cartilages, joined by a cartilaginous intermandibular
commissure. Meckels cartilages are sigmoid in shape and show well-developed ventromedial and retroarticular processes. The infrarostral cartilages are short, rectangular and independent. In the hyobranchial skeleton,
the ceratohyals are long and have a tall, triangular anterior process, a small, rounded anterolateral process, a
short and acute lateral process, and a large and wide posterior process; the articular condyle is a rounded,
robust projection visible from a dorsal view. The ceratohyals are joined medially by the pars reuniens nearly
as long as the basibranchial. The basihyal is small, visible as a narrow sliver of cartilage, and the basibranchial
is short and bears a short, quadrangular urobranchial process (23% of basibranchial length). The basibranchial
is fused to the hyobranchial plates. The hypobranchial plates are flat and triangular, and they articulate medially with a posterior triangular, narrow gap remaining. The ceratobranchials are long, thin, and have numerous
lateral projections. They are distally joined by terminal commissures. Four cartilaginous spicules arise dorsally from each ceratobranchial, the third one being reduced.

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FIGURE 7. Chaunus spinulosus, stage 34. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B) Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral cartilage. A ala, ALPC anterolateral process of ceratohyal, ALPO anterolateral process of otic capsule, APC anterior process of ceratohyal,
ARP articular process, ASP ascending process, BB basibranchial, BH basihyal, C corpus, CB(I-IV) ceratobranchial, CF carotid foramen, CH ceratohyal, FF frontoparietal fenestra, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral cartilage, IMC intermandibular commissure, LPC lateral process of ceratohyal, LPT lateral process of trabecular horn, MC Meckels cartilage, MP muscular
process, NC notochordal canal, OC otic capsule, OF oculomotor foramen, OPF optic foramen, PDP processus dorsalis posterior, PF
prootic foramen, PPC posterior process of ceratohyal, PR pars reuniens, QCC quadratocranial commissure, QOC quadratoorbital commissure, QP quadratoethmoid process, RP retroarticular process, S spicule, SB subocular bar, SC suprarostral cartilage, SF subocular
fenestra, TC terminal commissure, TF trochlear foramen, TH trabecular horn, TS tectum synoticum, TTM taenia tecti marginalis,
TTME taenia tecti medialis, TTT taenia tecti transversalis, UP urobranchial process. Scale lines = 1 mm.

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Musculature (N = 5, stages 34 and 36. Table 3 and Fig. 8). Thirty-two muscles appear in this species.
TABLE 3. Chaunus spinulosus, stages 34 and 36. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

ventromedial region of Meckels cartilage lower lip


of the oral disc

it consists of a single slip,


corresponding to m. mandibulolabialis
inferior

Submentalis

it is a short muscle that joins ventrally the


infrarostrals, without a median aponeurosis

Intermandibularis

medial region of Meckels cartilage


median aponeurosis

Levator mandibulae longus


superficialis

external and posterior margin of the subocular bar,


and part of the ascending process dorsomedial
region of Meckels cartilage

Levator mandibulae longus


profundus

external margin of the subocular bar, and part of the


ascending process external margin of the ala of the
suprarostral

the area of origin is smaller than that of


the m. l. m. l. superficialis, and insertion
is through a well-developed, long
tendon

Levator mandibulae internus

ventral surface of the ascending process distal edge


of Meckels cartilage

the insertion is via a long tendon

Levator mandibulae externus


superficialis

medial, inferior surface of the muscular process


dorsal, lateral edge of the suprarostral

it is scarcely developed, and the


mandibular branch of the trigeminal
nerve (V3) runs ventrally to it

Levator mandibulae externus


profundus

medial, inferior surface of the muscular process


ventral margin of the ala
of the suprarostral

it originates ventrally regarding the


former muscle, and it is more
developed; its insertion is via a tendon
shared with the m. l. m. l. profundus

Levator mandibulae
articularis

inferior part of the medial surface of the muscular


process dorsal surface of the lateral edge of
Meckels cartilage

Levator mandibulae lateralis

articular process of the palatoquadrate dorsal, lateral


edge of the suprarostral

it is a short muscle, formed of a few


fibers

Suspensoriohyoideus

posterior descending margin of the muscular process


posterior surface of the lateral
process of the ceratohyal

it is a compact and well-developed


muscle

Orbitohyoideus

anterior, dorsal margin of the muscular process


lateral edge of the ceratohyal

Suspensorioangularis

inferior, lateral part of the descending margin


of the muscular process
retroarticular process of Meckels cartilage

the site of origin is concealed by the m.


orbitohyoideus; fibers occupy
approximately the lower half of the
muscular process

Quadratoangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

it is completely covered by the mm.


suspensorioangularis and hyoangularis

Hyoangularis

dorsal surface of the ceratohyal, anterior to the


articular condyle retroarticular process of Meckels
cartilage

Interhyoideus

ventral surface of the ceratohyal, near the


lateral edge median aponeurosis

the whole structure is U-shaped, and in


the central region shows a thick,
resistant, alcianophilic connective tissue

it is formed of parallel, transverse


fibers, disposed in a plane nearly
perpendicular to the chondrocranial
longitudinal axis
...... continued

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TABLE 3 (continued)
Muscle

Insertions

Comments

Geniohyoideus

posterior, ventral surface of the infrarostral


hypobranchial plates, near the posterior edge

Levator arcuum branchialium


I

lateral margin of the subocular bar ceratobranchial I

Levator arcuum branchialium


II

subocular bar terminal commissure I

Levator arcuum branchialium


III

lateroventral part of the otic capsule terminal


commissure II

Levator arcuum branchialium


IV +
Tympanopharyngeus

the distinction between these two muscles is not clear; from the posterolateral surface of the otic
capsule, two well-differentiated slips arise: the lateral slip inserts on the medial margin of the
ceratobranchial IV, and the medial slip inserts on the medial margin of the ceratobranchial IV and
connective tissue of the pericardium

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process II terminal commissure I

Constrictor branchialis III

branchial process II terminal commissure II

it is disposed on the ceratobranchial II

Constrictor branchialis IV

branchial process II terminal commissure II

it is disposed on the ceratobranchial III

Subarcualis rectus I

three slips: lateral base of the posterior process of the


ceratohyal proximal part of the ceratobranchial I
(dorsal slip), branchial process II (ventral1 slip), and
branchial process III (ventral2 slip)

Subarcualis rectus II-IV

branchial process II proximal, ventral part of the


ceratobranchial IV

Subarcualis obliquus

urobranchial process branchial process II, or II and


III in some specimens

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum branchial process III

Rectus abdominis

peritoneum pelvic griddle

it is the widest of the mm. l. a.


branchialium; its insertion onto the
ceratobranchial occupies a large surface

in the anterior insertion, some fibers are


continuous with those of the ventral2
slip of the m. s. r. I; some lateral fibers
insert posteriorly, on the distal part of
the ceratobranchial IV

it is well-developed; it originates almost


at the level of the branchial basket

FIGURE 8. Chaunus spinulosus, stage 34. Musculature (A) Dorsal view, superficial plane, (B) Dorsal view, middle plane, (C) Dorsal
view, deep plane, (D) Ventral view, (E) Lateral view, superficial plane, (F) Lateral view, deep plane, (G) Ventral view, whole. CB(IIIV) constrictor branchialis, GH geniohyoideus, HA hyoangularis, IH interhyoideus, IM intermandibularis, LB(I-IV) levator arcuum
branchialium, LMA levator mandibulae articularis, LMEP levator mandibulae externus profundus, LMES levator mandibulae externus superficialis, LMI levator mandibulae internus, LML levator mandibulae lateralis, LMLP levator mandibulae longus profundus,
LMLS levator mandibulae longus superficialis, ML mandibulolabialis, OH orbitohyoideus, QA quadratoangularis, RA rectus abdominis, RC rectus cervicis, SA suspensorioangularis, SH suspensoriohyoideus, SM submentalis, SO subarcualis obliquus, SRI subarcualis
rectus I, SRII-IV subarcualis rectus II-IV, TP tympanopharyngeus. Scale lines = 1 mm.

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FIGURE 9. Chaunus spinulosus, stage 33. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B) Buccal roof,
(C) Buccal floor. BFA buccal floor arena, BFAP buccal floor arena papilla, BP buccal pocket, BRA buccal roof arena, BRAP buccal
roof arena papilla, C choana, DG dorsal gap, DV dorsal velum, ILP infralabial papilla, IR infrarostrodont, LK lower keratodonts, LP
lingual papilla, LRP lateral ridge papilla, MP marginal papilla, MR median ridge, NV narial valve, P pustulation, PNA prenarial arena,
PTNA postnarial arena, PTNP postnarial papilla, S spur, SR suprarostrodont, TA tongue anlage, UK upper keratodonts, VG ventral
gap, VV ventral velum. Scale lines = 1 mm.

Oral apparatus and buccopharyngeal cavity (N = 2, stages 31 and 33. Figs. 9 and 10). The oral disc width
represents nearly 24% of the body length, and gape width reaches 23% of the body length. The lateral margins
have deep indentations in the commissural region. The papillar margin is simple with wide dorsal and ventral
gaps; scarce submarginal papillae appear in the commissures. Papillae are large and conical, with smooth,
rounded tips. The rostrodonts are well-developed and keratinized. The serrations are triangular with sharp
points. The keratodonts are arranged in five rows, two upper (anterior) and three lower (posterior), resulting in
a LTRF 2(2)/3. The row A2 is interrupted by a wide, median gap, and P3 is slightly shorter than the other
rows. The keratodonts have an elongate and convex head with 1012 cusps and a sheath shorter and wider
than the head. In the buccal roof, the prenarial arena shows a small, quadrangular ridge accompanied by pustules. The choanae are large, obliquely arranged at an angle of 37 from the transversal line. The anterior margin has small prenarial papillae, and the narial valve is scarcely visible. In the postnarial arena there are four
pairs of conical or slightly bifid postnarial papillae. The lateral ridge papillae are well-developed, with three
or four pustulate tips. The median ridge is rectangular, twice as long as wide, and with an irregular free margin. The buccal roof arena is delimited on both sides by 34 tall, conical marginal papillae. Some pustules
appear anteriorly and posteriorly to the papillae. The secretory pits are arranged in a V-shaped array, located
near the posterior margin of the buccal roof. The dorsal velum is smooth and short. In the buccal floor, poste-

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rior to the infrarostrodonts, there is a pair of small non-keratinized spurs. The infralabial papillae are tall,
bifid, with points of unequal development, and they do not overlap to each other. On the tongue anlage, there
are four tall, conical, transversally arranged lingual papillae. The prepocket region, on the lateral portion of
the ceratohyal, has numerous pustules and 12 prepocket papillae. The buccal floor arena is delimited on both
sides by 45 peripheral, tall, conical papillae accompanied by pustules and small papillae. The buccal pockets
are elongate and transversally arranged. The ventral velum is long and supported by spicules; it has three main
pronounced marginal projections on each filter plate, and two small ones on each side of the middle line; the
median notch is absent, and secretory pits appear on the posterior edge of the velum.

FIGURE 10. Chaunus spinulosus, stage 33. Oral apparatus and buccopharyngeal cavity. SEM micrographies (A) Oral disc, frontal
view, (B) Detail of left commissure, (C) Detail of the spur, (D) Detail of the serrations of the suprarostrodont, (E) Detail of upper keratodonts, (F) Buccal roof, detail of choanae region. C choana, IR infrarostrodont, LK lower keratodonts, LRP lateral ridge papilla, MP
marginal papilla, MR median ridge, S spur.

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Gut content (N = 10, stages 3136. Tables 21 and 22). The preponderant food-category was diatoms
(99.33%) with a size range of 12% of the tadpole body length.
CERATOPHRYIDAE
Ceratophrys cranwelli. A description of the chondrocranium of this species was provided by Lavilla and Fabrezi (1992), Fabrezi and Garca (1994), and Wild (1997b). Palavecino (1999) studied part of the musculature.
Ulloa Kreisel (2003) described the buccopharyngeal cavity. In Vera Candioti (2005), the skeleton, musculature, oral apparatus, buccal cavity, and feeding of a new set of tadpoles were analyzed. Regarding this latter
paper, the disposition of the m. tympanopharyngeus is corrected.

FIGURE 11. Ceratophrys cranwelli, stage 33. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B)
Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral
cartilage. ALPC anterolateral process of ceratohyal, ANP antorbital process, APC anterior process of ceratohyal, ARP articular process, ASP ascending process, BB basibranchial, CB(I-IV) ceratobranchial, CH ceratohyal, FO fenestra ovalis, HP hypobranchial plate,
IC infrarostral cartilage, LOP larval otic process, LPC lateral process of ceratohyal, MC Meckels cartilage, MP muscular process, NC
notochordal canal, OC otic capsule, PF prootic foramen, PPC posterior process of ceratohyal, PR pars reuniens, QCC quadratocranial
commissure, QP quadratoethmoid process, RP retroarticular process, SB subocular bar, SC suprarostral cartilage, SF subocular fenestra, TC terminal commissure, TH trabecular horn, UP urobranchial process. Scale lines = 1 mm.

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Chondrocranium and hyobranchial skeleton (N = 5, stage 33. Fig. 11). The chondrocranium of these larvae represents 32% of the body length, and it shows a robust construction. The maximum width is at the plane
of posterior part of the subocular bar. The suprarostral cartilage is a single, posteriorly curved structure with a
median constriction. The region of articulation with the trabecular horns is represented by two dorsal depressions. In the middle, ventral part, there is a stout spike ventrally oriented. The trabecular horns are quadrangular, scarcely divergent, and very short (11% of the total length of the chondrocranium). In the ethmoid region,
the nasal septum, the tectum nasi, and the lamina orbitonasalis are differentiated. The cranial floor is completely cartilaginous, and on its posterior margin, the notochordal canal extends 15% of the chondrocranium
length. The lateral walls of the chondrocranium are formed by the orbital cartilages. The chondrocranium is
dorsally closed. The otic capsules are quadrangular, occupy nearly 25% of the chondrocranium total length,
and are fused to the posterior part of the cranial roof. The fenestra ovalis (27% of the capsule length) is located
ventrolaterally on each otic capsule. The palatoquadrate has a short and wide articular process, and a low,
robust muscular process. The subocular bar has a smooth margin, and it is posterolaterally rounded and
slightly wider. The palatoquadrate attaches to the braincase via three points: the quadratocranial commissure,
the ascending process, and the larval otic process. The quadratocranial commissure is very wide and bears a
well-developed quadratoethmoid process. The ascending process attaches to the braincase below the oculomotor foramen (low attachment). The lower jaw includes the Meckels and infrarostral cartilages, joined by a
cartilaginous intermandibular commissure. Meckels cartilages are short, polyhedral, robust, and articulate
with the articular process via the retroarticular process. The infrarostral cartilages are fused, constituting a
wedge-like structure. In the hyobranchial skeleton, the ceratohyals are robust and bear low and massive anterior, lateral, and posterior processes; the anterolateral process is slightly outlined, and the articular condyle is
rounded and robust. The ceratohyals are joined medially by a rectangular pars reuniens. The basihyal is
absent, and the basibranchial, fused to the pars reuniens, is posteriorly wider and bears a short, rounded urobranchial process. The hypobranchial plates are subquadrangular and articulate medially, remaining a posterior, ovoid gap. The ceratobranchials, distally joined by terminal commissures, are bar-like, devoid of lateral
projections and spicules.
Musculature (N = 5, stage 33. Table 4 and Fig. 12). Twenty-nine muscles appear in this species.
TABLE 4. Ceratophrys cranwelli, stage 33. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

medial edge of Meckels cartilage lower lip of the oral


disc

it consists of a single, cylindrical


slip, corresponding to m.
mandibulolabialis inferior

Submentalis

it is a short muscle that joins ventrally the infrarostrals

it has no median aponeurosis

Intermandibularis

lateral edge of Meckels cartilage median aponeurosis

it is a short and well-developed


muscles, with parallel fibers
grouped in two packs; the anterior
group is less developed and
acquires a semicircular shape; the
posterior group is rectangular

Levator mandibulae longus


superficialis

external and posterior margin of the subocular bar, and


ascending process dorsomedial surface of Meckels
cartilage

it is well-developed

Levator mandibulae longus


profundus

external margin of the subocular bar lateral edge of the


suprarostral

Levator mandibulae internus

ventral surface of the ascending process distal edge of


Meckels cartilage

the insertion is via a long tendon,


that reaches nearly half the muscle
...... continued

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TABLE 4 (continued)
Muscle

Insertions

Levator mandibulae externus


superficialis

medial, inferior surface of the muscular process lower


lip of the oral disc, near the commissure

Levator mandibulae externus


profundus

medial, inferior surface of the muscular process lateral


edge of the suprarostral

Levator mandibulae articularis

inferior part of the medial surface of the muscular process


dorsal surface of the lateral edge of Meckels cartilage

Orbitohyoideus

anterior, dorsal margin of the muscular process lateral


edge of the ceratohyal

it is well-developed

Suspensorioangularis

inferior, lateral part of the descending margin


of the muscular process
retroarticular process of Meckels cartilage

fibers occupy more than the lower


half of the muscular process

Hyoangularis

dorsal surface of the ceratohyal, anterior to the articular


condyle retroarticular process of Meckels cartilage

it is well-developed

Interhyoideus

ventral surface of the ceratohyal, near the


lateral edge median aponeurosis

Geniohyoideus

posterior, ventral surface of the infrarostral


hypobranchial plates

Levator arcuum branchialium I

lateral margin of the subocular bar ceratobranchial I

Levator arcuum branchialium II

larval otic process terminal commissure II

Levator arcuum branchialium


III

larval otic process terminal commissure III

Levator arcuum branchialium


IV

posterolateral part of the otic capsule ceratobranchial IV

Tympanopharyngeus

posterolateral surface of the otic capsule, with a common


insertion with the medial slip of the m. l. a. b. IV
connective tissue of the pericardium, anterior to the
glottis

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process II terminal commissure I

it is disposed on the
ceratobranchial I

Constrictor branchialis III

branchial process II terminal commissure II

it is disposed on the
ceratobranchial II

Constrictor branchialis IV

Branchial process II proximal, ventral part of the


ceratobranchial IV

Subarcualis obliquus

urobranchial process branchial process III

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum branchial process III

Rectus abdominis

peritoneum, posteriorly to the branchial basket pelvic


griddle

it has two slips, the lateral wider


than the medial

lateral base of the posterior process of the ceratohyal


branchial process III

Subarcualis rectus II-IV

the distinction between this and the


former muscle is no clear; from the
muscular process a single slip
arises, from which a few fibers
diverge far distally, toward the
suprarostral; the mandibular
branch of the trigeminal nerve runs
dorsal to both of mm. levatores
mandibulae externus

branchial process II terminal commissure III

Subarcualis rectus I

Comments

28 Zootaxa 1600 2007 Magnolia Press

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FIGURE 12. Ceratophrys cranwelli, stage 33. Musculature (A) Dorsal view, superficial
plane, (B) Dorsal view, middle plane, (C) Dorsal view, deep plane, (D) Ventral view, (E)
Lateral view, superficial plane, (F) Lateral view, deep plane, (G) Ventral view, whole.
CB(II-IV) constrictor branchialis, DB diaphragmatobranchialis, GH geniohyoideus, HA
hyoangularis, IH interhyoideus, IM intermandibularis, LB(IIV) levator arcuum branchialium, LMA levator mandibulae articularis, LMES+P levator mandibulae externus
superficialis + profundus, LMI levator mandibulae internus, LMLP levator mandibulae
longus profundus, LMLS levator mandibulae longus superficialis, ML mandibulolabialis, OH orbitohyoideus, RA rectus abdominis, RC rectus cervicis, SA suspensorioangularis, SO subarcualis obliquus, SRI subarcualis rectus I, SRII-IV subarcualis rectus II
IV, TP tympanopharyngeus. Scale lines = 1 mm.

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FIGURE 13. Ceratophrys cranwelli, stage 33. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B) Buccal
roof, (C) Buccal floor. BFA buccal floor arena, BP buccal pocket, C choana, G glottis, ILP infralabial papilla, IR infrarostrodont, LK
lower keratodonts, LP lingual papilla, MP marginal papilla, MR median ridge, P pustulation, PNA prenarial arena, PTNA postnarial
arena, PTNP postnarial papilla, SR suprarostrodont, TA tongue anlage, UK upper keratodonts, VV ventral velum. Scale lines = 1 mm.

Oral apparatus and buccopharyngeal cavity (N = 2, stage 33. Figs. 13 and 14). The oral disc (21% of the
body length) is circular with small indentations in the commissures. It has well-developed protruding lips with
conical marginal papillae sparsely dispersed. Gape width occupies 20% of the body length. The suprarostrodont is very thin, V-shaped, well-keratinized, with short, pointed serrations. The infrarostrodont is well-developed and wider than the suprarostrodont; serrations are similar, short and acute. The keratodonts are arranged
in eight upper and eight lower rows. The eight rows next to the rostrodonts are discontinuous, with gaps that
increase their length towards the rostrodonts. The length of the rows thus decreases towards the rostrodonts,
with the exception of the two lowest rows, which are respectively and shorter than the immediately anterior. The keratodonts have a short, cylindrical sheath, slightly wider than the head, which is conical, spikelike. The buccal roof is triangular and scarcely pigmented. The prenarial arena lacks any structure. The choanae are elongate and obliquely arranged at an angle of 38 from the transversal line; there are no prenarial
papillae on the anterior margin, and the narial valve is well-developed. Posteriorly, there is a pair of tall, laminar and trifurcate postnarial papillae. The median ridge is tall, thin and with an irregular margin. Lateral ridge
papillae are absent. The buccal roof arena is not defined, due the lack of papillae; it has only a few pustules.
Conspicuous groups of peritrich ciliates of the genus Vorticella are fixed on the papillae, the choanae and the
prenarial and postnarial arena. Finally, dorsal velum is highly reduced or absent. In the buccal floor, there are

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three pairs of tall, flat and multifid infralabial papillae, transversally aligned. The tongue anlage has one pair
of conical lingual papillae. The buccal floor arena is poorly defined, with scarce short, conical papillae
restricted to the lateral and posterior region. Several pustules are scattered among buccal floor papillae and on
the central area of the ventral velum. The buccal pockets are shallow, not perforated, and transversally
arranged. The ventral velum is short, without spicular support; its margin is smooth, without marginal projections, and on the middle region, the median notch is broad and shallow. Small secretory pits appear on the posterior margin of the velum.

FIGURE 14. Ceratophrys cranwelli, stage 33. Oral apparatus and buccopharyngeal cavity. SEM micrographies (A) Oral disc, frontal
view, (B) Detail of the infrarostrodont, (C) Lower keratodonts rows, (D) Detail of keratodonts, (E) Detail of the suprarostrodont, inferior view, (F) Detail of choanae region; (G) Detail of Vorticella sp. C choana, IR infrarostrodont, PTNP postnarial papillae, SR
suprarostrodont, UK upper keratodonts, VS Vorticella sp.

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Gut content (N = 7, stages 3537. Tables 21 and 22). The most frequent food-category were colonial algae
(Volvocales, 45.56%) followed by crustaceans and insects. The sizes distribute between 150% of the tadpole
body length, with modes around 4% and 20%. Furthermore, some Ceratophrys cranwelli tadpoles were kept
alive and fed on Pleurodema borelli tadpoles. Ceratophrys cranwelli has a sit-and-wait feeding mode and tadpoles are consumed whole, those of smaller sizes (up to 60% of the predator size), or captured and torn apart
before ingest.
Lepidobatrachus llanensis. The cartilaginous skeleton of these larvae was described by Lavilla and Fabrezi
(1992) and Wild (1997b). Part of the musculature was analyzed by Palavecino (1999). Ulloa Kreisel (2003)
described the buccopharyngeal cavity.

FIGURE 15. Lepidobatrachus llanensis, stage 33. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B)
Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral
cartilage, dorsal view. ALPO anterolateral process of otic capsule, APC anterior process of ceratohyal, ARP articular process, ASP
ascending process, BB basibranchial, CB(I-IV) ceratobranchial, CF carotid foramen, CH ceratohyal, CPF craniopalatine foramen, FF
frontoparietal fenestra, HP hypobranchial plate, IC infrarostral cartilage, LO lamina orbitonasalis, LPC lateral process of ceratohyal,
MC Meckels cartilage, MP muscular process, NC notochordal canal, OC otic capsule, OP otic process, PPC posterior process of ceratohyal, PR pars reuniens, QCC quadratocranial commissure, RP retroarticular process, SB subocular bar, SC suprarostral cartilage,
SF subocular fenestra, TC terminal commissure, TH trabecular horn, TS tectum synoticum, TTM taenia tecti marginalis, TTME taenia
tecti medialis, UP urobranchial process. Scale lines = 1 mm.

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Chondrocranium and hyobranchial skeleton (N = 5, stage 33. Fig. 15). The chondrocranium of these larvae represents 35% of the body length. The maximum width is at the level of the muscular process of the palatoquadrate. The suprarostral cartilage is a single, curved structure, articulated to the trabecular horns via a
thick articular region. The trabecular horns correspond to 33% of the total length of the chondrocranium and
are markedly divergent. The nasal septum and the lamina orbitonasalis are formed at the analyzed stages. The
cranial floor is completely cartilaginous and the carotid and craniopalatine foramina are visible. In the posterior margin of the cranial floor, the notochordal canal extends 29% of the chondrocranium length. The lateral
walls of the chondrocranium are formed by the orbital cartilages. The chondrocranium is open dorsally
through the frontoparietal fenestra bordered by the taeniae tecti marginales. The taenia tecti medialis is outlined. The otic capsules are quadrangular and small, occupy nearly 21% of the chondrocranium total length,
and bear a small anterolateral process. The otic capsules are dorsally joined by the tectum synoticum. The
palatoquadrates diverge anteriorly. The articular process is thin and short, and the muscular process is low and
thick, with two angular projections in its external margin. The subocular bar is short, thin and with uniform
width. The palatoquadrate attaches to the braincase via two points: the quadratocranial commissure curved,
longer than the subocular bar, devoid of processes, and the ascending process, thin and fused to the neurocranium above the oculomotor foramen. The lower jaw includes the Meckels and infrarostral cartilages, joined
by a cartilaginous intermandibular commissure. Meckels cartilages are bar-like, slightly distally wider, and
lack processes. The infrarostral cartilages are fused constituting a curve structure with rounded edges. In its
medial region, there is a triangular projection posteriorly oriented. In the hyobranchial skeleton, the ceratohyals are long and have conspicuous, quadrangular anterior and posterior processes; the anterolateral process is
a small protuberance near the distal edge, and the lateral process is very wide and flat: the articular condyle is
a robust protuberance visible from a dorsal view. The ceratohyals are medially joined by a V-shaped pars reuniens, with thin branches fused to the anterior processes. The basihyal is absent and the basibranchial is wide
and short, with the caudal edge showing a short and wide urobranchial process. The hypobranchial plates are
medially fused, forming a flat structure with concave posterior margin. The ceratobranchials are bar-like,
devoid of lateral projections and spicules, and are distally joined by terminal commissures.
Musculature (N = 5, stage 33. Table 5 and Fig. 16). Twenty-nine muscles appear in this species.
TABLE 5. Lepidobatrachus llanensis, stage 33. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Submentalis

it is a small muscle located in the middle line of the


ventral surface of the infrarostral cartilage

it lacks median aponeurosis, and it is


scarcely developed in the stage analyzed

Intermandibularis

medial region of Meckels cartilage median aponeurosis

it is formed of a single layer of loosely


disposed fibers; it is posteriorly joined to
the median aponeurosis of the m.
interhyoideus

Levator mandibulae
longus superficialis

external and posterior margin of the subocular bar and


part of the ascending process of the palatoquadrate
dorsomedial region of Meckels cartilage

the insertion is via a tendon common


with the m. l. m. externus superficialis

Levator mandibulae
longus profundus

external margin of the subocular bar dorsal part of the


edge of the suprarostral

Levator mandibulae
internus

ventral surface of the ascending process distal edge of


Meckels cartilage

the insertion is via a long tendon, nearly


1/3 of the whole muscle

Levator mandibulae
externus superficialis

medial, inferior surface of the muscular process dorsal


region of Meckels cartilage

it is scarcely developed, with few fibers,


the tendon of insertion is common with
that of the m. l. m. l. superficialis; the
mandibular branch of the trigeminal
nerve (V3) runs ventrally to this muscle
...... continued

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TABLE 5 (continued)
Muscle

Insertions

Comments

Levator mandibulae
externus profundus

medial, inferior surface of the muscular process


lateroventral margin the suprarostral

it integrated itself to the m. l. m. l.


profundus

Levator mandibulae
articularis

medial surface of the muscular process dorsal surface of


the lateral edge of Meckels cartilage

it is flat and short

Levator mandibulae
lateralis

dorsal, lateral edge of the suprarostral articular process


of the palatoquadrate

it is scarcely developed in the stage


analyzed

Orbitohyoideus

muscular process and anterior margin of the


quadratocranial commissure ventral surface of the edge
of the ceratohyal

it is well-developed

Suspensorioangularis

inferior, lateral part of the descending margin of the


muscular process retroarticular process of Meckels
cartilage

fibers occupy nearly the whole lateral


surface of the muscular process

Hyoangularis

dorsal surface of the ceratohyal, anterior to the articular


condyle retroarticular process of Meckels cartilage

Interhyoideus

anterior margin of the ceratohyal, posterior to the anterior


process median aponeurosis

Geniohyoideus

posterior, ventral surface of the infrarostral, near the


distal edge junction between the hypobranchial plates
and the ceratobranchial I

Levator arcuum
branchialium I

lateral margin of the subocular bar terminal commissure


I

Levator arcuum
branchialium II

ascending process terminal commissure II

Levator arcuum
branchialium III

ascending process terminal commissure III

Levator arcuum
branchialium IV

posterolateral part of the otic capsule medial margin of


the ceratobranchial IV, near its caudal edge

Tympanopharyngeus

posterolateral surface of the otic capsule medial margin


of the ceratobranchial IV and connective tissue of the
pericardium

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process II terminal commissure I

it is disposed on the ceratobranchial I

Constrictor branchialis III

branchial process II terminal commissure I

it is disposed on the ceratobranchial II

Constrictor branchialis IV

branchial process II terminal commissure III

Subarcualis rectus I

two slips: lateral base of the posterior process of the


ceratohyal proximal part of the ceratobranchial I (dorsal
slip), and branchial process II (ventral slip)

Subarcualis rectus II-IV

branchial process II proximal, ventral part of the


ceratobranchial IV

Subarcualis obliquus

urobranchial process branchial processes II and III

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum branchial processes III and IV

Rectus abdominis

peritoneum pelvic griddle

34 Zootaxa 1600 2007 Magnolia Press

it is fan-shaped

it is well-developed; it originates almost


at the level of the branchial basket

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FIGURE 16. Lepidobatrachus llanensis, stage 33. Musculature (A) Dorsal view,
superficial plane, (B) Dorsal view, middle plane, (C) Dorsal view, deep plane, (D)
Ventral view, (E) Lateral view, superficial plane, (F) Lateral view, deep plane, (G)
Ventral view, whole. CB(II-IV) constrictor branchialis, GH geniohyoideus, HA
hyoangularis, IH interhyoideus, IM intermandibularis, LB(I-IV) levator arcuum
branchialium, LMA levator mandibulae articularis, LMEP levator mandibulae
externus profundus, LMES levator mandibulae externus superficialis, LMI
levator mandibulae internus, LMLP levator mandibulae longus profundus, LMLS
levator mandibulae longus superficialis, OH orbitohyoideus, RA rectus
abdominis, RC rectus cervicis, SA suspensorioangularis, SO subarcualis
obliquus, SRI subarcualis rectus I, SRII-IV subarcualis rectus II-IV, TP
tympanopharyngeus. Scale lines = 1 mm.

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Oral apparatus and buccopharyngeal cavity (N = 2, stages 33 and 34. Figs. 17 and 18). The mouth is slitshaped, with a gape width that reaches almost 65% of the body length. The upper lip has two small lateral
flaps pending on the suprarostrodont. Small, regularly spaced papillae appear in a continuous margin surrounding the oral apparatus. The rostrodonts are very long and thin, represented by individual serrations without a common sheath; serrations are conical, acute, and larger in the infrarostrodont than in the
suprarostrodont. The buccal roof shows numerous small pustules scattered on the entire roof surface. The choanae are small, almost circular, and lack prenarial papillae and narial valve. All other structures, e.g., median
ridge, postnarial papillae, lateral ridge papillae, buccal roof papillae, are absent. The dorsal velum is absent.
The buccal floor shows one pair of conspicuous, short, irregular infralabial papillae and numerous pustules
scattered in front and behind them. The tongue anlage is scarcely visible and shows two small pustules on the
medial region. The buccal pockets are unperforated and slightly obliquely oriented. The buccal floor is nearly
naked, with small pustules on the lateral region and the ventral velum. The buccal floor arena is not defined,
due the lack of papillae. The ventral velum is very short, with an undulate margin, and lacks spicular support,
median notch, marginal projections, and a glandular epithelium.

FIGURE 17. Lepidobatrachus llanensis, stage 34. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B) Buccal
roof, (C) Buccal floor. BP buccal pocket, C choana, ILP infralabial papilla, IR infrarostrodont, MP marginal papilla, P pustulation, SR
suprarostrodont, TA tongue anlage, VV ventral velum. Scale lines = 1 mm.

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FIGURE 18. Lepidobatrachus llanensis, stage 34. Oral apparatus and buccopharyngeal cavity. SEM micrographies (A) Anterior
region of buccal roof, (B) Detail of serrations of the suprarostrodont, (C) Anterior region of the buccal floor, (D) Detail of infralabial
papillae, (E) Detail of ventral velum. C choana, ILP infralabial papillae, IR infrarostrodont, SR suprarostrodont.

Gut content (N = 4, stages 3136. Tables 21 and 22). The gut content of the specimens analyzed was composed of tadpoles and large crustaceans with sizes representing 90150% of the tadpole size.

Telmatobius cf. atacamensis. Lavilla (1983b) described the oral apparatus of this species. The remaining data
here presented are unpublished.

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FIGURE 19. Telmatobius cf. atacamensis, stage 36. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view,
(B) Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral cartilage. A ala, ADC adrostral cartilage, ALPC anterolateral process of ceratohyal, ANP antorbital process, APC anterior process
of ceratohyal, ARP articular process, ASP ascending process, BB basibranchial, C corpus, CB(I-IV) ceratobranchial, CF carotid foramen, CH ceratohyal, CPF craniopalatine foramen, FF frontoparietal fenestra, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral cartilage, LPC lateral process of ceratohyal, MC Meckels cartilage, MP muscular process, NC notochordal canal, NS nasal
septum, OC otic capsule, PPC posterior process of ceratohyal, PP pseudopterygoid process, PR pars reuniens, QCC quadratocranial
commissure, QP quadratoethmoid process, RP retroarticular process, S spicule, SB subocular bar, SC suprarostral cartilage, SF subocular fenestra, TC terminal commissure, TH trabecular horn, TS tectum synoticum, TTM taenia tecti marginalis, UP urobranchial process. Scale lines = 1 mm.

Chondrocranium and hyobranchial skeleton (N = 2, stages 34 and 36. Fig. 19). The chondrocranium of
these larvae represents 42% of the body length. The maximum width is at the plane of the posterior part of the
subocular bar. The suprarostral cartilage is tetrapartite, formed of a distinguishable corpus and dorsally articulated alae. Two rectangular cartilages ventrally wider form the corpus. The alae have a well-developed processus dorsalis posterior. Near the dorsal edge of each ala, there is a pair of small, polyhedral adrostral cartilages.
The trabecular horns correspond to 24% of the total length of the chondrocranium; they have relatively
straight anterior margins, and on the lateroventral margin, the processus lateralis trabeculae is well-developed.

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The cranial floor is completely cartilaginous and in its posterior margin, the notochordal canal extends 18% of
the chondrocranium length. The carotid and craniopalatine foramina are visible. The lateral walls of the chondrocranium are formed by the orbital cartilages. The chondrocranium is open dorsally through the frontoparietal fenestra lined by the taeniae tecti marginales. The nasal septum and the antorbital processes are welldeveloped, the latter approaching the dorsal tip of the muscular process. The otic capsules are ovoid, and
occupy nearly 28% of the chondrocranium total length. They bear developed anterolateral process, and are
dorsally joined by the tectum synoticum. The fenestra ovalis reaches 41% of the capsule length, and it is
located ventrolaterally on each otic capsule. The palatoquadrate has a wide articular process, a short, subtriangular muscular process and a subocular bar posteriorly wider and rounded. The palatoquadrate attaches to the
braincase via two points, the quadratocranial commissure and the ascending process. The quadratocranial
commissure bears a wide, well-developed quadratoethmoid process and a long and thin pseudopterygoid process. The ascending process attaches to the braincase below the oculomotor foramen. In the lower jaw,
Meckels cartilages are stout and elongate, with conspicuous ventromedial and retroarticular processes. The
infrarostral cartilages are short and oblong. In the hyobranchial apparatus, the ceratohyals are long and have a
wide, triangular anterior process, a thin, medially directed anterolateral process, an acute lateral process, and a
broad posterior process; the articular condyle is a rounded protuberance visible dorsally. The ceratohyals are
joined medially by the pars reuniens. The basihyal is absent and the basibranchial is longer than the pars reuniens, distally wider, and with a short, rounded urobranchial process (25% of the basibranchial length). The
hypobranchial plates are triangular and flat, and they articulate medially leaving a posterior ovoid gap. The
ceratobranchials are long, thin and have numerous lateral projections. They are distally joined by terminal
commissures. Four well-developed cartilaginous spicules arise dorsally from each ceratobranchial.
Musculature (N = 2, stages 34 and 36. Table 6 and Figs. 20 and 21). Thirty-one muscles appear in this species.
TABLE 6. Telmatobius cf. atacamensis, stages 34 and 36. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

ventromedial region of Meckels cartilage lower lip of


the oral disc

it consists of a single slip, corresponding


to m. mandibulolabialis inferior

Intermandibularis

medial region of the distal edge of Meckels cartilage


median aponeurosis

the whole structure is U-shaped, and


consists of a few fibers, loosely disposed

Levator mandibulae longus


superficialis

external and posterior margin of the subocular bar


dorsomedial region of Meckels cartilage

Levator mandibulae longus


profundus

external margin of the subocular bar and part of the


ascending process of the palatoquadrate external
margin of the ala of the suprarostral

the area of origin coincides with that of


the m. l .m. l. superficialis

Levator mandibulae
internus

ventral surface of the ascending process distal edge of


Meckels cartilage

the insertion is via a long tendon

Levator mandibulae
externus superficialis

medial, inferior surface of the muscular process lateral


edge of the ala of the suprarostral

it is scarcely developed, formed of 56


fibers; the mandibular branch of the
trigeminal nerve (V3) runs dorsally to this
muscle

Levator mandibulae
externus profundus

medial, inferior surface of the muscular process


lateroventral margin of the ala of the suprarostral

its insertion is via a tendon shared with


the m. l. m. l. profundus

Levator mandibulae
articularis

inferior part of the medial surface of the muscular


process dorsal surface of the lateral edge of Meckels
cartilage

it is scarcely developed

Levator mandibulae
lateralis

articular process of the palatoquadrate posterior face


of the adrostral cartilage

it is a very thin muscle, formed of a few


fibers
...... continued

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TABLE 6 (continued)
Muscle

Insertions

Comments

Suspensoriohyoideus

posterior descending margin of the muscular process


posterior surface of the lateral process of the ceratohyal

it shows a slight division into two slips

Orbitohyoideus

anterior, dorsal margin of the muscular process lateral


edge of the ceratohyal

Suspensorioangularis

inferior, lateral surface of the descending margin of the


muscular process retroarticular process of Meckels
cartilage

the site of origin is concealed by the m.


orbitohyoideus; fibers occupy
approximately the lower half of the
muscular process

Quadratoangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

it is completely covered by the m.


hyoangularis

Hyoangularis

dorsal surface of the ceratohyal, anterior to the articular


condyle retroarticular process of Meckels cartilage

Interhyoideus

ventral surface of the ceratohyal, near the lateral edge


median aponeurosis

Interhyoideus posterior +
Diaphragmatopraecordialis

I could not find these muscles; however, in T. ceiorum (not included in this study), two muscles are
present, in a distinctive pattern (Fig. 21): the lateral slip corresponds to the m. interhyoideus posterior,
in the typical location encircling the peribranchial chamber; the medial slip (that could be a second
slip of the m. interhyoideus posterior, the m. diaphragmatopraecordialis, or an unknown muscle)
originates ventral to the diaphragm, near the m. interhyoideus posterior, and it runs anteriorly to
insert, through a soft tendon, in connective tissue near the articular process of the palatoquadrate;
histological studies are needed to confirm this pattern in T. cf. atacamensis

Geniohyoideus

posterior, ventral surface of the infrarostral


hypobranchial plates

Levator arcuum
branchialium I

lateral margin of the subocular bar ceratobranchial I

Levator arcuum
branchialium II

subocular bar terminal commissure I

Levator arcuum
branchialium III

lateral part of the otic capsule terminal commissure II

Levator arcuum
branchialium IV

posterolateral part of the otic capsule medial margin of


the ceratobranchial IV

Tympanopharyngeus

posterolateral surface of the otic capsule connective


tissue of the pericardium

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process II terminal commissure I

Constrictor branchialis III

branchial process II terminal commissure II

Constrictor branchialis IV

branchial process III terminal commissure III

Subarcualis rectus I

two slips: lateral base of the posterior process of the


ceratohyal proximal part of the ceratobranchial I
(dorsal slip), and branchial process II (ventral slip)

Subarcualis rectus II-IV

branchial process II proximal, ventral part of the


ceratobranchial IV

Subarcualis obliquus

urobranchial process branchial process II

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum branchial process II

Rectus abdominis

peritoneum pelvic griddle

40 Zootaxa 1600 2007 Magnolia Press

two well-differentiated slips are present in


some specimens

it is well-developed; it originates almost


at the level of the branchial basket

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FIGURE 20. Telmatobius cf. atacamensis, stage 36. Musculature (A) Dorsal view,
superficial plane, (B) Dorsal view, middle plane, (C) Dorsal view, deep plane, (D) Ventral
view, (E) Lateral view, superficial plane, (F) Lateral view, deep plane, (G) Ventral view,
whole. CB(II-IV) constrictor branchialis, GH geniohyoideus, HA hyoangularis, IH
interhyoideus, IM intermandibularis, LB(I-IV) levator arcuum branchialium, LMA levator
mandibulae articularis, LMEP levator mandibulae externus profundus, LMI levator
mandibulae internus, LML levator mandibular lateralis, LMLP levator mandibulae longus
profundus, LMLS levator mandibulae longus superficialis, ML mandibulolabialis, OH
orbitohyoideus, QA quadratoangularis, RA rectus abdominis, RC rectus cervicis, SA
suspensorioangularis, SH suspensoriohyoideus, SO subarcualis obliquus, SRI subarcualis
rectus I, SRII-IV subarcualis rectus II-IV, TP tympanopharyngeus. Scale lines = 1 mm.

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FIGURE 21. Telmatobius ceiorum, stage 35. Detail of hyobranchial musculature, showing the distinctive pattern of muscles inserting
on the diaphragm. D diaphragm, IH interhyoideus, IHP interhyoideus posterior, MS medial slip = diaphragmatopraecordialis / second
slip of interhyoideus posterior / new muscle?, O operculum, OH orbitohyoideus, RA rectus abdominis. Scale line = 1 mm.

Oral apparatus and buccopharyngeal cavity (N = 1, stage 34. Fig. 22). The oral disc represents nearly
24% of the body length and lacks lateral constrictions. Gape width reaches 17% of the body length. The papillar margin is simple, interrupted in a dorsal gap, and it is accompanied by large submarginal papillae in the
commissures and lower lip. The rostrodonts are well-developed and keratinized. The keratodonts are arranged
in five rows, two upper (anterior) and three lower (posterior), resulting in a LTRF 2(2)/3(1). In the buccal roof,
the prenarial arena is naked. The choanae are large and obliquely arranged at an angle of 41 from the transversal line. Prenarial papillae are absent, and the narial valve is developed. The postnarial arena shows three
pairs of tall, conical papillae; the medial pair is the largest. Several pustules distribute among these papillae.
The lateral ridge papillae are well-developed, with three or four pustulate points. The median ridge is triangular, high, with an irregular free margin. The buccal roof arena is delimited on both sides by 78 tall, conical
papillae, accompanied by several pustules and short papillae. Posterolaterally to the lateral ridge papillae,
there appear 2-3 short, conical or bifid papillae. The glandular zone is well-developed and shows large secretory pits. The dorsal velum is large and smooth, and it is broadly interrupted medially. In the buccal floor, posteriorly to the infrarostrodonts, there is a pair of small, scarcely prominent, keratinized, bicuspidate spurs.
Posteriorly, there are two pairs of infralabial papillae: the medial ones are short and conical, and the lateral
ones are well-developed, tall, flat and multifid. The tongue anlage is small, and bears one pair of simple, conical lingual papillae. The buccal floor arena shows numerous papillae symmetrically arranged on the lateral
and central regions. The marginal papillae are the tallest, conical and thin, in a number of 2025 on each side;
the papillae placed medially to the buccal pockets are flat, wide and bifid. In the prepocket region, there are 6
7 small papillae. The buccal pockets are elongate and transversally oriented. The ventral velum is long and
supported by spicules, and it has three pronounced, medially directed marginal projections on the filter plates
and a deep median notch surrounded by rounded projections; large secretory pits appear on the posterior margin of the velum.

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FIGURE 22. Telmatobius cf. atacamensis, stage 34. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B) Buccal roof, (C) Buccal floor. BFA buccal floor arena, BFAP buccal floor arena papilla, BP buccal pocket, BRA buccal roof arena, BRAP
buccal roof arena papilla, C choana, DG dorsal gap, DV dorsal velum, GZ glandular zone, ILP infralabial papilla, IR infrarostrodont,
LK lower keratodonts, LP lingual papilla, LRP lateral ridge papilla, MP marginal papilla, MR median ridge, P pustulation, PNA prenarial arena, PPP prepocket papilla, PTNA postnarial arena, PTNP postnarial papilla, S spur, SMP submarginal papilla, SR suprarostrodont, TA tongue anlage, UK upper keratodonts, VV ventral velum. Scale lines = 1 mm.

Gut content (N = 4, stages 2536. Tables 21 and 22). The gut content was mainly composed of insects
with sizes that represent up to 20% of tadpole size.

HYLIDAE
Dendropsophus microcephalus. Previous literature for this species includes descriptions of cartilaginous skeleton, part of the musculature, and oral apparatus (Duellman & Fouquette, 1968; Duellman 1970; Wassersug &
Hoff 1979; Wassersug & Rosenberg 1979; Satel & Wassersug 1981; Haas 1996a). The results in this study
complete the information on musculature, buccopharyngeal cavity and gut content.

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FIGURE 23. Dendropsophus microcephalus, stage 28. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view,
(B) Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral cartilage. APC anterior process of ceratohyal, ARP articular process, ASP ascending process, BB basibranchial, CB(I-IV) ceratobranchial, CF carotid foramen, CH ceratohyal, FF frontoparietal fenestra, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral
cartilage, LPC lateral process of ceratohyal, LOP larval otic process, MC Meckels cartilage, MP muscular process, NC notochordal
canal, OC otic capsule, OPF optic foramen, PF prootic foramen, PPC posterior process of ceratohyal, PR pars reuniens, QCC quadratocranial commissure, RP retroarticular process, SB subocular bar, SC suprarostral cartilage, SF subocular fenestra, TC terminal commissure, TH trabecular horn, TS tectum synoticum, TTM taenia tecti marginalis. Scale lines = 1 mm.

Chondrocranium and hyobranchial skeleton (N = 5, stages 25 and 28. Fig. 23). The chondrocranium of
these larvae represents 47% of the body length. Maximum widths are at the level of the muscular process of
the palatoquadrate and the otic capsules. The suprarostral cartilage is a single, crescent-shaped structure that
articulates syndesmotically with the trabecular horns. The trabecular horns are proportionately short (17% of
the total length of the chondrocranium) and acuminate. The cranial floor is lightly chondrified, with thin cartilage in the central area. The carotid foramen is visible at the posterior region; the craniopalatine foramen is not
clearly identifiable. In the posterior margin of the cranial floor, the notochordal canal extends 22% of the
chondrocranium length. The lateral walls of the chondrocranium are formed by the orbital cartilages. The
chondrocranium is dorsally open through the frontoparietal fenestra lined by the taeniae tecti marginales. The
otic capsules are quadrangular and dorsally joined by the tectum synoticum; they reach 28% of the chondrocranium length. In the palatoquadrate, the articular process is long and thin. The muscular process is large, qua-

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drangular, wide and convex, and its dorsal margin contacts the lamina orbitonasalis. The subocular bar is very
thin, with a smooth margin. The palatoquadrate attaches to the braincase via three points: the quadratocranial
commissure, the ascending process, and the larval otic process. The quadratocranial commissure is wide and
devoid of processes. The ascending process is attached to cranial floor. The lower jaw includes the Meckels
and infrarostral cartilages joined by a cartilaginous intermandibular commissure. Meckels cartilages are sigmoid and articulate with the articular process via the retroarticular process. The infrarostral cartilages are
short and posteriorly joined. In the hyobranchial skeleton, the ceratohyals are triangular and robust, and have
a wide, rounded anterior process, a scarcely evident anterolateral process, a rounded lateral process, and a
wide and robust posterior process; the articular condyle is very robust. The basihyal is absent and the basibranchial is long and devoid of urobranchial process. The pars reuniens has no definite limits and it is almost
vestigial, making the ceratohyals appear contiguous. The branchial basket is reduced. The hypobranchials are
well-developed, quadrangular, and medially articulated, leaving a small, triangular posterior gap. The ceratobranchials are bar-like, and lack lateral projections; terminal commissures connect the ceratobranchials I, II
and III, whereas the fourth one remains free. The spicules are absent.
Musculature (N = 5, stages 25 and 28. Table 7 and Fig. 24). Thirty-one muscles appear in this species.

TABLE 7. Dendropsophus microcephalus, stages 25 and 28. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

ventromedial region of Meckels cartilage lower surface of


the oral tube

it consists of a single slip,


corresponding to m.
mandibulolabialis inferior

Intermandibularis

medial region of Meckels cartilage median aponeurosis

Levator mandibulae longus


superficialis

external and posterior margin of the subocular bar and part


of the ascending process of palatoquadrate dorsomedial
region of Meckels cartilage

Levator mandibulae longus


profundus

external margin of the subocular bar and part of the


ascending process of the palatoquadrate external margin of
the suprarostral

the insertion is through a welldeveloped, long tendon

Levator mandibulae
internus

ventral surface of the ascending process distal edge of


Meckels cartilage

the insertion is via a long tendon

Levator mandibulae
externus superficialis

medial, inferior surface of the muscular process


mediodorsal surface of Meckels cartilage

the mandibular branch of the


trigeminal nerve (V3) runs ventrally
to this muscle

Levator mandibulae
externus profundus

medial, inferior surface of the muscular process ventral


margin of the edge of the suprarostral

it originates ventrally regarding the


former muscle, and its insertion is
via a tendon shared with the m. l. m.
l. profundus

Levator mandibulae
articularis

inferior part of the medial surface of the muscular process


dorsal surface of the lateral edge of Meckels cartilage

Levator mandibulae
lateralis

articular process of the palatoquadrate nasal sac

Suspensoriohyoideus

posterior descending margin of the muscular process


posterior surface of the lateral process of the ceratohyal

Orbitohyoideus

anterior and dorsal margins of the muscular process lateral


edge of the ceratohyal

it is the most developed muscle in


this species

Suspensorioangularis

ventral margin of the muscular process retroarticular


process of Meckels cartilage

the site of origin is concealed by the


m. orbitohyoideus

it is a short, flat muscle

...... continued

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TABLE 7 (continued)
Muscle

Insertions

Comments

Quadratoangularis

ventral surface of the palatoquadrate retroarticular process


of Meckels cartilage

it is completely covered by the m.


hyoangularis

Hyoangularis

anterior surface of the edge of the ceratohyal retroarticular


process of Meckels cartilage

Interhyoideus

ventral surface of the ceratohyal, near the lateral edge


median aponeurosis

Interhyoideus posterior +
Diaphragmatopraecordialis

I could not find these muscles; since they are both present in a related species (Dendropsophus
ebraccatus Haas, 2003), but very hard to detect, it would be necessary to apply histological
techniques to confirm their presence

Geniohyoideus

posterior, ventral surface of the infrarostral hypobranchial


plates, near the anterior edge

Levator arcuum
branchialium I

lateral margin of the subocular bar ceratobranchial I

it is the widest of the mm. l. a.


branchialium; its insertion onto the
ceratobranchial occupies a large
surface

Levator arcuum
branchialium II

larval otic process terminal commissure I and


ceratobranchial II

it is separated of the former muscle


by a narrow gap, less evident at the
insertion on the palatoquadrate

Levator arcuum
branchialium III

lateral part of the otic capsule ceratobranchial III

Levator arcuum
branchialium IV

posterolateral part of the otic capsule ceratobranchial IV


and hypobranchial plate

it has two slips, the medial one welldeveloped, and inserted on part of
the ceratobranchial IV and the
hypobranchial plate

Tympanopharyngeus

lateral part of the otic capsule connective tissue anterior to


the glottis

it is formed of a group of fibers that


diverge from the medial slip of the
m. l. a. b. IV, and contact with those
of the opposite muscle, anteriorly to
the glottis

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process II terminal commissure I

Constrictor branchialis III

branchial process II terminal commissure II

Constrictor branchialis IV

fibers are continuous with those of the anterior part of the m. subarcualis rectus II-IV; they insert on
the terminal commissure II and the distal part of the ceratobranchial III

Subarcualis rectus I

two slips: lateral part of the posterior process of the


ceratohyal proximal, lateral part of the ceratobranchial I
(dorsal slip) and branchial process III (ventral slip)

the dorsal slip is less developed, and


its fibers adopt an oblique
orientation

Subarcualis rectus II-IV

two slips: anterolateral part of the ceratobranchial I


branchial process III (anterior slip) and branchial process III
ventromedial part of the ceratobranchial IV (posterior slip)

some fibers of the anterior slip are


continuous with those of the m.
subarcualis rectus II-IV and those of
the m. constrictor branchialis IV

Subarcualis obliquus

posterior edge of the basibranchial branchial process II


and III

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum branchial process III

Rectus abdominis

peritoneum pelvic griddle

46 Zootaxa 1600 2007 Magnolia Press

it is well-developed; it originates
almost at the level of the branchial
basket

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FIGURE 24. Dendropsophus microcephalus, stage 28. Musculature (A) Dorsal view,
superficial plane, (B) Dorsal view, middle plane, (C) Dorsal view, deep plane, (D)
Ventral view, (E) Lateral view, superficial plane, (F) Lateral view, deep plane, (G)
Ventral view, whole. CB(II-IV) constrictor branchialis; GH geniohyoideus, HA
hyoangularis, IH interhyoideus, IM intermandibularis, LB(I-IV) levator arcuum
branchialium, LMA levator mandibulae articularis, LMEP levator mandibulae externus
profundus, LMES levator mandibulae externus superficialis, LMI levator mandibulae
internus, LML levator mandibulae lateralis, LMLP levator mandibulae longus
profundus, LMLS levator mandibulae longus superficialis, ML mandibulolabialis, OH
orbitohyoideus, RA rectus abdominis, RC rectus cervicis, SA suspensorioangularis, SH
suspensoriohyoideus, SO subarcualis obliquus, SRI subarcualis rectus I, SRII-IV(a-p)
subarcualis rectus II-IV (anterior posterior), TP tympanopharyngeus. Scale lines = 1
mm.

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Oral apparatus and buccopharyngeal cavity (N = 2, stages 25 and 28. Fig. 25). The oral disc is modified
in an oral tube whose width reaches 13% of the body length. It is devoid of marginal papillae and keratodonts,
and the rostrodonts are finely serrated. Gape width is very small (11% of the body length). In the buccal roof,
the prenarial arena shows no distinct features. The choanae are small, oriented at an angle of about 52 from
the transversal line, and lack narial valve. The postnarial arena has one pair of small pustules in the medial
region. The lateral ridge papillae are short, flat, slightly wider at the base, and have pustulate tips. The median
ridge is low and with an uneven margin; some pustules scatter between the ridge and the dorsal velum. The
buccal roof arena is not defined; buccal roof arena papillae are absent. The dorsal velum is very short and
smooth, and no secretory pits are observed with light microscope. In the buccal floor, the infralabial papillae
are globose, well-developed, with uneven margins. The tongue anlage is comparatively large, devoid of lingual papillae; some pustules appear near its margins. The buccal floor arena is not defined and numerous pustules are distributed on the central region. The buccal pockets are small, shallow, unperforated, transversally
oriented, and they locate far posteriorly on the buccal floor. The ventral velum is not supported by spicules,
and it has a semicircular, smooth margin; in the median region there appears a small median notch, and the
glandular epithelium on the ventral surface of the velum is absent.

FIGURE 25. Dendropsophus microcephalus, stage 28. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B)
Buccal roof, (C) Buccal floor. BP buccal pocket, C choana, DV dorsal velum, ILP infralabial papilla, IR infrarostrodont, LRP lateral
ridge papilla, MR median ridge, P pustulation, PNA prenarial arena, PTNA postnarial arena, SR suprarostrodont, TA tongue anlage,
VV ventral velum. Scale lines = 1 mm.

Gut content (N = 9, stages 2528. Tables 21 and 22). The gut content of the dissected specimens was composed mainly by whole and fragmented oligochaetes of the genus Dero with sizes between 2090% of the tadpole body length.

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Dendropsophus nanus. Morphological features and gut content of this species were described by Lavilla
(1990), Fabrezi and Lavilla (1992), Lajmanovich (1998), Vera Candioti and Haas (2004), Vera Candioti et al.
(2004). Regarding Vera Candioti and Haas (2004), the disposition of the m. tympanopharyngeus is corrected.

FIGURE 26. Dendropsophus nanus, stage 31. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B)
Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral
cartilage. APC anterior process of ceratohyal, ARP articular process, ASP ascending process, BB basibranchial, CB(I-IV) ceratobranchial, CF carotid foramen, CH ceratohyal, CPF craniopalatine foramen, FF frontoparietal fenestra, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral cartilage, LPC lateral process of ceratohyal, LOP larval otic process, MC Meckels cartilage, MP muscular
process, NC notochordal canal, OC otic capsule, OPF optic foramen, PDP processus dorsalis posterior, PPC posterior process of ceratohyal, PR pars reuniens, QCC quadratocranial commissure, RP retroarticular process, SB subocular bar, SC suprarostral cartilage, SF
subocular fenestra, TC terminal commissure, TH trabecular horn, TS tectum synoticum, TTM taenia tecti marginalis. Scale lines = 1
mm.

Chondrocranium and hyobranchial skeleton (N = 5, stage 31. Fig. 26). The chondrocranium of these larvae represents 32% of the body length. The maximum width is at the plane of the muscular process and the
otic capsules. The suprarostral cartilage is a single, crescent-shaped structure that articulates syndesmotically
with the trabecular horns. The trabecular horns are proportionately short (13% of the total length of the chondrocranium) and acuminate. The cranial floor is lightly chondrified, with thin cartilage in the central area. The
craniopalatine and carotid foramina are clearly identifiable. In the posterior margin of the cranial floor, the
notochordal canal extends 21% of the chondrocranium length. The lateral walls of the chondrocranium are
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formed by the orbital cartilages. The chondrocranium is open dorsally, and the frontoparietal fenestra is bordered by the taeniae tecti marginales. The otic capsules are quadrangular and small, and are dorsally joined by
the tectum synoticum. In the palatoquadrate, the articular process is long and thin. The muscular process is
quadrangular, wide, convex, and its dorsal margin contacts the lamina orbitonasalis. The subocular bar has a
smooth margin. The palatoquadrate attaches to the braincase via three points: the quadratocranial commissure,
the ascending process, and the larval otic process. The quadratocranial commissure is wide and devoid of processes. The ascending process is attached to the cranial floor. The lower jaw includes the Meckels and infrarostral cartilages joined by a cartilaginous intermandibular commissure. Meckels cartilages are sigmoid and
articulate with the articular process via the retroarticular process. The infrarostral cartilages are short and
independent. In the hyobranchial skeleton, the ceratohyals are triangular and robust, and have rounded anterior process, scarcely visible anterolateral process, wide and rounded lateral process, and robust posterior process; the articular condyle is rounded and robust. The basihyal is absent and the basibranchial is long and
devoid of urobranchial process. The pars reuniens has no definite limits and it is almost vestigial, making the
ceratohyals appear contiguous. The branchial basket is reduced. The hypobranchials are well-developed, quadrangular, and medially articulated, leaving a small, triangular posterior gap. The ceratobranchials lack lateral
projections and have terminal commissures connecting the ceratobranchials I, II and III; the fourth remains
free in some specimens. The spicules are absent.
Musculature (N = 5, stages 31 and 36. Table 8 and Fig. 27). Thirty-one muscles appear in this species.
TABLE 8. Dendropsophus nanus, stages 31 and 36. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

ventromedial region of Meckels cartilage lower


surface of the oral tube

it consists of a single slip, corresponding to m. mandibulolabialis inferior

Intermandibularis

medial region of Meckels cartilage median


aponeurosis

Levator mandibulae longus


superficialis

external and posterior margin of the subocular bar and


part of the ascending process of palatoquadrate
dorsomedial region of Meckels cartilage

Levator mandibulae longus


profundus

external margin of the subocular bar and part of the


ascending process of the palatoquadrate external
margin of the suprarostral

the insertion is through a welldeveloped, long tendon

Levator mandibulae internus

ventral surface of the ascending process distal edge


of Meckels cartilage

the insertion is via a long tendon

Levator mandibulae externus


superficialis

medial, inferior surface of the muscular process


mediodorsal surface of Meckels cartilage

the mandibular branch of the


trigeminal nerve (V3) runs ventrally to
this muscle

Levator mandibulae externus


profundus

medial, inferior surface of the muscular process


ventral margin of the edge of the suprarostral

it originates ventrally regarding the


former muscle, and its insertion is via
a tendon shared with the m. l. m. l.
profundus

Levator mandibulae articularis

inferior part of the medial surface of the muscular


process dorsal surface of the lateral edge of
Meckels cartilage

Levator mandibulae lateralis

articular process of the palatoquadrate nasal sac

Suspensoriohyoideus

posterior descending margin of the muscular process


posterior surface of the lateral process of the
ceratohyal

Orbitohyoideus

anterior and dorsal margins of the muscular process


lateral edge of the ceratohyal

it is a short, flat muscle

it is the most developed muscle in this


species
...... continued

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TABLE 8 (continued)
Muscle

Insertions

Comments

Suspensorioangularis

ventral margin of the muscular process retroarticular


process of Meckels cartilage

the site of origin is concealed by the


m. orbitohyoideus

Quadratoangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

it is completely covered by the m.


hyoangularis

Hyoangularis

anterior surface of the edge of the ceratohyal


retroarticular process of Meckels cartilage

Interhyoideus

ventral surface of the ceratohyal, near the lateral edge


median aponeurosis

Interhyoideus posterior +
Diaphragmatopraecordialis

I could not find these muscles; since they are both present in a related species (Dendropsophus
ebraccatus Haas, 2003), but very hard to detect, it would be necessary to apply histological
techniques to confirm their presence

Geniohyoideus

posterior, ventral surface of the infrarostral


hypobranchial plates, near the anterior edge

Levator arcuum branchialium I

lateral margin of the subocular bar ceratobranchial I

it is the widest of the mm. l. a.


branchialium; its insertion onto the
ceratobranchial occupies a large
surface

Levator arcuum branchialium II

larval otic process terminal commissure I and


ceratobranchial II

it is separated of the former muscle by


a narrow gap, less evident at the
insertion on the palatoquadrate

Levator arcuum branchialium III

lateral part of the otic capsule ceratobranchial III

Levator arcuum branchialium


IV

posterolateral part of the otic capsule


ceratobranchial IV and hypobranchial plate

it has two slips, the medial one welldeveloped, and inserted on part of the
ceratobranchial IV and the
hypobranchial plate

Tympanopharyngeus

lateral part of the otic capsule connective tissue


anterior to the glottis

it is formed of a group of fibers that


diverge from the medial slip of the m.
l. a. b. IV, and contact with those of
the opposite muscle, anteriorly to the
glottis

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process II terminal commissure I

Constrictor branchialis III

branchial process II terminal commissure II

Constrictor branchialis IV

fibers are continuous with those of the anterior part of the m. subarcualis rectus II-IV; they insert
on the terminal commissure II and the distal part of the ceratobranchial III

Subarcualis rectus I

two slips: lateral part of the posterior process of the


ceratohyal proximal, lateral part of the
ceratobranchial I (dorsal slip) and branchial process
III (ventral slip)

the dorsal slip is less developed, and


its fibers adopt an oblique orientation

Subarcualis rectus II-IV

two slips: anterolateral part of the ceratobranchial I


branchial process III (anterior slip) and branchial
process III ventromedial part of the ceratobranchial
IV (posterior slip)

some fibers of the anterior slip are


continuous with those of the m.
subarcualis rectus II-IV and those of
the m. constrictor branchialis IV

Subarcualis obliquus

posterior edge of the basibranchial branchial process


II and III

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum branchial process III

Rectus abdominis

peritoneum pelvic griddle

ANATOMY OF ANURAN TADPOLES

it is well-developed; it originates
almost at the level of the branchial
basket

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FIGURE 27. Dendropsophus nanus, stage 31. Musculature (A) Dorsal view,
superficial plane, (B) Dorsal view, middle plane, (C) Dorsal view, deep plane,
(D) Ventral view, (E) Lateral view, superficial plane, (F) Lateral view, deep
plane, (G) Ventral view, whole. CB(II-IV) constrictor branchialis, GH geniohyoideus, HA hyoangularis, IH interhyoideus, IM intermandibularis, LB(I-IV) levator arcuum branchialium, LMA levator mandibulae articularis, LMEP levator
mandibulae externus profundus, LMES levator mandibulae externus superficialis, LMI levator mandibulae internus, LML levator mandibulae lateralis, LMLP
levator mandibulae longus profundus, LMLS levator mandibulae longus superficialis, ML mandibulolabialis, OH orbitohyoideus, RA rectus abdominis, RC rectus cervicis, SA suspensorioangularis, SH suspensoriohyoideus, SO subarcualis
obliquus, SRI subarcualis rectus I, SRII-IV(a-p) subarcualis rectus II-IV (anterior posterior), TP tympanopharyngeus. Scale lines = 1 mm.

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Oral apparatus and buccopharyngeal cavity (N = 2, stages 31 and 36. Figs. 28 and 29). The oral disc is
modified in an oral tube (13% of the body length). It is devoid of marginal papillae and keratodonts, and the
rostrodonts are finely serrated. Gape width is very small (11% of the body length). In the buccal roof, the choanae are small, arranged at an angle of 57 from the transversal line, and lack narial valve. There are no other
distinct structures on the buccal roof, excepting some few pustules. The posterior margin is pigmented and
devoid of secretory epithelium, and the dorsal velum is very short. In the buccal floor, the infralabial papillae
are paired and globose. The tongue anlage is comparatively large, devoid of lingual papillae, and it shows
some pustules on the posterior region. The buccal floor arena is not defined, and a few pustules are scattered
on the medial surface of the ceratohyals. The buccal pockets are small, shallow, unperforated, and far caudally
located. The ventral velum is semicircular and smooth, with a small median notch; it lacks spicular support,
marginal projections and secretory pits on the ventral surface.

FIGURE 28. Dendropsophus nanus, stage 31. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B) Buccal roof,
(C) Buccal floor. C choana, DV dorsal velum, ILP infralabial papilla, IR infrarostrodont, P pustulation, SR suprarostrodont, TA tongue
anlage, VV ventral velum. Scale lines = 1 mm.

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FIGURE 29. Dendropsophus nanus, stage 31. Oral apparatus and buccopharyngeal cavity. SEM micrographies (A) Oral apparatus,
frontal view, (B) Detail of the suprarostrodont, (C) Detail of infralabial papillae, (D) Buccal roof, detail of choanae region, (E) Detail
of ventral velum. C choana, IR infrarostrodont, LL lower lip.

Gut content (N = 10, stages 31 37. Tables 21 and 22). The most conspicuous items were oligochaetes
belonging to 10 neustonic and pleustonic species. Individuals were found intact inside the manicotto glandulare. Smaller items only accumulate 0.04% of the digestive content. The size of the oligochaetes represents
90130% of the tadpole body length.

Hypsiboas rosenbergi. The cartilaginous skeleton and part of the musculature has been previously studied by
Haas (1996a). The oral apparatus was described by Duellman (1970). Remaining data are unpublished.

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FIGURE 30. Hypsiboas rosenbergi, stage 33. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B)
Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral
cartilage. A ala, ALPC anterolateral process of ceratohyal, ALPO anterolateral process of otic capsule, APC anterior process of ceratohyal, ARP articular process, ASP ascending process, BB basibranchial, C corpus, CB(I-IV) ceratobranchial, CF carotid foramen, CH
ceratohyal, FF frontoparietal fenestra, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral cartilage, LO lamina orbitonasalis,
LPC lateral process of ceratohyal, MC Meckels cartilage, MP muscular process, NC notochordal canal, OC otic capsule, PDA processus dorsalis anterior PDP processus dorsalis posterior, PPC posterior process of ceratohyal, PR pars reuniens, QCC quadratocranial
commissure, RP retroarticular process, S spicule, SB subocular bar, SC suprarostral cartilage, SF subocular fenestra, TC terminal commissure, TH trabecular horn, TS tectum synoticum, TTM taenia tecti marginalis, UP urobranchial process. Scale lines = 1 mm.

Chondrocranium and hyobranchial skeleton (N = 2, stages 33 and 34. Fig. 30). The chondrocranium of
these larvae represents 53% of the body length. The maximum width is at the level of posterior part of the subocular bar, and the anterolateral process of the otic capsule. The suprarostral cartilage has a single, V-shaped
corpus that is dorsally articulated to the alae. The alae are well-defined, ventrally rounded, and bear developed
processus dorsalis anterior and posterior. The trabecular horns are long (25% of the total length of the chondrocranium) and diverge from the ethmoid plate. The lamina orbitonasalis are formed in the stages analyzed.
The cranial floor is lightly chondrified, with thin cartilage in the central area. The carotid foramen is visible on
the posterior region, and the craniopalatine foramen is not clearly identifiable, because of the light chondrification of the intertrabecular plate. In the posterior margin of the cranial floor, the notochordal canal extends
19% of the chondrocranium length. The orbital cartilages are not formed. The chondrocranium is open dorANATOMY OF ANURAN TADPOLES

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sally, and the frontoparietal fenestra is lined by the taeniae tecti marginales. The otic capsules are quadrangular, and bear an acute and long anterolateral process that nearly reaches the subocular bar. A large fenestra
ovalis (50% of the capsule length) is located ventrolaterally on each otic capsule. The otic capsules are joined
dorsally by the tectum synoticum. The palatoquadrate is long and relatively narrow. It has a long articular process and a high, triangular muscular process. The subocular bar has a smooth margin and it is posterolaterally
rounded. The palatoquadrate attaches to the braincase via two points: the quadratocranial commissure and the
ascending process. The quadratocranial commissure is thin and devoid of processes. The lower jaw includes
the Meckels and infrarostral cartilages joined by a cartilaginous intermandibular commissure. Meckels cartilages are L-shaped with three processes, dorsomedialis, ventromedialis and retroarticular. The infrarostral cartilages are short, rectangular and independent. In the hyobranchial skeleton, the ceratohyals are long and have
a triangular anterior process, a tall, tin and acute anterolateral process, a rounded lateral process, and a wide
posterior process; the articular condyle is a rounded, robust protuberance on the dorsal surface. The ceratohyals are joined medially by the pars reuniens, longer than wide. The basihyal is absent and the basibranchial is
twice as long as the pars reuniens, and bears a relatively long urobranchial process (30% of the basibranchial
length). The hypobranchial plates are flat and subquadrangular, and they articulate medially leaving a posterior, narrow gap. The ceratobranchials are long, thin, and have numerous, long lateral projections. They are
distally joined by terminal commissures. Three spicules are well-developed, and the fourth one is scarcely visible.
Musculature (N = 2, stage 35. Table 9 and Fig. 31). Thirty-three muscles are present on the species.
TABLE 9. Hypsiboas rosenbergi, stage 35. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

two slips: ventromedial region of Meckels cartilage


lower lip of the oral disc (mandibulolabialis inferior) and
commissural region and part of the upper lip
(mandibulolabialis superior)

Intermandibularis

medial region of Meckels cartilage median


aponeurosis

the whole structure is U-shaped

Levator mandibulae longus


superficialis

external and posterior margin of the subocular bar and


ascending process of the palatoquadrate dorsomedial
region of Meckels cartilage

it is well-developed, and its


insertion is via a wide tendon

Levator mandibulae longus


profundus

external margin of the subocular bar and part of the


ascending process of the palatoquadrate external
margin of the ala of the suprarostral

the area of origin is smaller than


that of the m. l. m. l. superficialis,
and insertion is through a welldeveloped, long tendon

Levator mandibulae internus

ventral surface of the ascending process and otic capsule


distal edge of Meckels cartilage

the insertion is via a long tendon

Levator mandibulae externus


superficialis

medial, inferior surface of the muscular process distal


edge of the ala of the suprarostral

it is scarcely developed

Levator mandibulae externus


profundus

medial, inferior surface of the muscular process


lateroventral margin of the ala of the suprarostral

it originates ventrally regarding


the former muscle, and it is more
developed; the mandibular branch
of the trigeminal nerve (V3) runs
dorsally to this muscle

Levator mandibulae articularis

inferior part of the medial surface of the muscular


process dorsal surface of the lateral edge of Meckels
cartilage

Levator mandibulae lateralis

articular process of the palatoquadrate dorsal, lateral


edge of the suprarostral

it is a short muscle, formed of a


few fibers
...... continued

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TABLE 9 (continued)
Muscle

Insertions

Comments

Suspensoriohyoideus

posterior descending margin of the muscular process


posterior surface of the lateral process of the ceratohyal

Orbitohyoideus

anterior and dorsal margins of the muscular process


lateral edge of the ceratohyal

Suspensorioangularis

inferior, lateral part of the descending margin of the


muscular process retroarticular process of Meckels
cartilage

fibers occupy approximately the


lower half of the muscular process

Quadratoangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

it is completely covered by the


mm. hyoangularis and
suspensorioangularis

Hyoangularis

dorsal surface of the ceratohyal, anterior to the articular


condyle retroarticular process of Meckels cartilage

Interhyoideus

ventral surface of the ceratohyal, near the lateral edge


median aponeurosis

Interhyoideus posterior

fibers loosely disposed ventral to the peribranchial


chamber, in the region of the anterior ceratobranchials

Diaphragmatopraecordialis

connective tissue near the insertion of the fibers of the m.


interhyoideus posterior connective tissue dorsal to the
pericardium

Geniohyoideus

posterior, ventral surface of the infrarostral


hypobranchial plates

Levator arcuum branchialium I

lateral margin of the subocular bar ceratobranchial I

Levator arcuum branchialium II

anterolateral process of the otic capsule terminal


commissure I

Levator arcuum branchialium III

lateroventral part of the otic capsule terminal


commissure II

Levator arcuum branchialium


IV

posterolateral part of the otic capsule medial margin of


the ceratobranchial IV

it has two slips of similar


configuration

Tympanopharyngeus

posterolateral surface of the otic capsule connective


tissue anterior to the glottis

fibers diverge from the medial slip


of the m. l. a. b. IV, and insert near
the fibers of the opposite muscle

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process II terminal commissure I

it is disposed on the
ceratobranchial I

Constrictor branchialis III

branchial process II terminal commissure II

it is disposed on the
ceratobranchial II

Constrictor branchialis IV

branchial process II terminal commissure II

it is disposed on the
ceratobranchial III

Subarcualis rectus I

two slips: lateral base of the posterior process of the


ceratohyal proximal part of the ceratobranchial I
(dorsal slip), and branchial process II (ventral slip)

Subarcualis rectus II-IV

branchial process II branchial process III and proximal


part of the ceratobranchial IV

Subarcualis obliquus

urobranchial process branchial process II and III

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum branchial process III and connective tissue


near the ceratobranchial IV

Rectus abdominis

peritoneum pelvic griddle

ANATOMY OF ANURAN TADPOLES

the slips diverge near the insertion


on the urobranchial process

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FIGURE 31. Hypsiboas rosenbergi, stage 35. Musculature (A) Dorsal view,
superficial plane, (B) Dorsal view, middle plane, (C) Dorsal view, deep plane, (D)
Ventral view, (E) Lateral view, superficial plane, (F) Lateral view, deep plane, (G)
Ventral view, whole. CB(II-IV) constrictor branchialis, DB diaphragmatobranchialis,
GH geniohyoideus, HA hyoangularis, IH interhyoideus, IM intermandibularis, LB(IIV) levator arcuum branchialium, LMA levator mandibulae articularis, LMEP levator
mandibulae externus profundus, LMES levator mandibulae externus superficialis,
LMI levator mandibulae internus, LML levator mandibulae lateralis, LMLP levator
mandibulae longus profundus, LMLS levator mandibulae longus superficialis, OH
orbitohyoideus, QA quadratoangularis, RA rectus abdominis, RC rectus cervicis, SA
suspensorioangularis, SH suspensoriohyoideus, SO subarcualis obliquus, SRI
subarcualis rectus I, SRII-IV subarcualis rectus II-IV, TP tympanopharyngeus. Scale
lines = 1 mm.

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FIGURE 32. Hypsiboas rosenbergi, stage 32-33. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B) Buccal
roof, (C) Buccal floor. BFA buccal floor arena, BFAP buccal floor arena papilla, BP buccal pocket, C choana, DG dorsal gap, DV dorsal velum, GZ glandular zone, ILP infralabial papilla, IR infrarostrodont, LK lower keratodonts, LP lingual papilla, LRP lateral ridge
papilla, MP marginal papilla, MR median ridge, NV narial valve, P pustulation, PNA prenarial arena, PPP prepocket papilla, PTNA
postnarial arena, PTNP postnarial papilla, SR suprarostrodont, TA tongue anlage, UK upper keratodonts, VV ventral velum. Scale
lines = 1 mm.

Oral apparatus and buccopharyngeal cavity (N = 2, stages 33 and 35. Figs. 32 and 33). The oral disc represents nearly 30% of the body length and it is anteroventrally located. Gape width reaches 22% of the body
length. The oral disc is completely surrounded by a simple papillar margin, double in part of the upper and
lower lips. The dorsal gap is narrow. The rostrodonts have wide serrations. The keratodonts are arranged in a
2(2)/4(1) LTRF. The rows P2 and P3 are the longest, and P4 may appear complete or divided into several fragments and it is shorter than the remaining rows. The keratodonts have a scarcely marked body, and the head is
slightly convex, with 1214 cusps. The keratodonts of the lowest row are slightly shorter than in the other
rows. The buccal roof is well-pigmented, mainly in the posterior region. The prenarial arena shows small pustules, and a low, pustulate, rectangular ridge. The choanae are large, very ornate, and obliquely arranged at an
angle of about 33 from the transversal line; in the anterior margin, small pustules and prenarial papillae are
aligned, and in the posterior margin, the narial valve is well-developed, pustulate and thick. The postnarial
arena shows two pairs of conical, low and thin postnarial papillae, and several pustules. The lateral ridge
papillae are flat, well-developed, and with pustulate margin. The median ridge is pentagonal, with a free pustulate margin. The buccal roof arena is not defined, and the central region shows numerous pustules uniformly
arranged. The glandular zone shows large secretory pits. The dorsal velum is relatively long and smooth. In
the buccal floor, posterior to the infrarostrodonts, there are three pairs of infralabial papillae: the two anterior

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pairs include small, conical papillae; the third pair, located on the Meckels cartilage, consists of tall, pustulate
and multifid papillae that overlap to each other in the middle line. On the tongue anlage, there is one pair of
simple lingual papillae accompanied by pustules. The buccal floor arena is delimited by 6 pairs of tall, bilaterally arranged papillae. The two papillae medial to the buccal pockets are wide, flat and multifid; the remaining
ones are conical, of varied sizes. In the entire region posterior to the tongue anlage, including the prepocket
region, pustules and small papillae are distributed. The buccal pockets are narrow and transversally arranged.
The ventral velum is supported by spicules, and it shows three pronounced marginal projections on the filter
plates; the median notch is absent, and secretory pits appear on the posterior ventral surface of the velum.

FIGURE 33. Hypsiboas rosenbergi, stage 32-33. Oral apparatus and buccopharyngeal cavity. SEM micrographies (A) Oral disc, frontal view, (B) Detail of the suprarostrodont, (C) Detail of lower keratodonts, (D) Detail of keratodonts from the lowest row, (E) Buccal
floor, detail of lingual region, (F) Detail of ventral velum. ILP infralabial papillae, LK lower keratodonts, from the lowest row, LP lingual papillae, MP marginal papilla, SP secretory pit, TA tongue anlage.

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Gut content (N = 6, stages 3134. Tables 21 and 22). The animal fraction was well-represented, with
about 50% of crustaceans and 16% of ciliates. The prey sizes with highest values range between 16% of the
tadpole body size. Additionally, in the gut contents appeared an unusual number of keratodonts and serrations
of the rostrodonts probably ingested by the tadpole itself (keratodonts 15; serrations of the rostrodonts 6;
values are averages per drop of gut content analyzed).
Lysapsus limellum. Morphological characters of this species were described by Kehr and Basso (1990), Vera
Candioti (2004), and Alcalde and Barg (2006). Qualitative composition of the diet was analyzed by Lajmanovich (1998). Regarding Vera Candioti (2004), the disposition of the m. tympanopharyngeus is corrected.

FIGURE 34. Lysapsus limellum, stage 31. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B) Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral cartilage. A ala, ALPC anterolateral process of ceratohyal, APC anterior process of ceratohyal, ARP articular process, ASP ascending
process, BB basibranchial, C corpus, CB(I-IV) ceratobranchial, CF carotid foramen, CH ceratohyal, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral cartilage, LOP larval otic process, LPC lateral process of ceratohyal, MC Meckels cartilage, MP muscular
process, NC notochordal canal, OC otic capsule, PDA processus dorsalis anterior, PDP processus dorsalis posterior, PPC posterior
process of ceratohyal, PR pars reuniens, QCC quadratocranial commissure, QP quadratoethmoid process, RP retroarticular process, S
spicule, SB subocular bar, SC suprarostral cartilage, SF subocular fenestra, TC terminal commissure, TH trabecular horn, TS tectum
synoticum, TTM taenia tecti marginalis, UP urobranchial process. Scale lines = 1 mm.

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Chondrocranium and hyobranchial skeleton (N = 5, stages 3135. Fig. 34). The chondrocranium of these
larvae represents 60% of the body length. The maximum width is at the plane of the middle part of the subocular bar. The suprarostral cartilage has a single corpus with a dorsal, deep, V-shaped notch. The corpus is dorsally fused to the alae, which are still distinguishable and bear dorsalis anterior and posterior processes. The
trabecular horns correspond to 24% of the total length of the chondrocranium and are anteriorly wider. They
articulate with the suprarostral through a thickened surface. The cranial floor is not completely cartilaginous,
the central zone is occupied by a large basicranial fenestra that includes the craniopalatine foramina. The
carotid foramen is visible. In the posterior margin of the cranial floor, the notochordal canal extends 17% of
the chondrocranium length. The orbital cartilages are represented by a posterior chondrification (pila metoptica, according to Lavilla & De S, 1999). The taeniae tecti marginales are outlined in the posterolateral region
of what would constitute the frontoparietal fenestra. The otic capsules are quadrangular and occupy nearly
29% of the chondrocranium total length. The fenestra ovalis reaches 41% of the capsule length and it is
located ventrolaterally on each otic capsule. The otic capsules are dorsally joined by a thin tectum synoticum.
The palatoquadrate has a thin articular process, a tall, triangular, and medially curved muscular process. The
subocular bar is very wide at the middle portion, forming a flat, triangular projection. The palatoquadrate
attaches to the braincase via three points: the quadratocranial commissure, the ascending process, and the larval otic process. The quadratocranial commissure is thin and bears a quadratoethmoid process and a small
pseudopterygoid process. The ascending process attaches to the braincase floor (ultralow attachment). In the
lower jaw, Meckels and infrarostral cartilages are joined by a cartilaginous intermandibular commissure.
Meckels cartilages are sigmoid and bear rounded retroarticular and ventromedial processes. The infrarostral
cartilages are short, rectangular and curved, and are joined by an intramandibular commissure. In the hyobranchial skeleton, the ceratohyals are long and have a triangular anterior process, a small, pointed anterolateral
process, a rounded lateral process, and a tall, triangular posterior process; the articular condyle is a rounded
projection visible from a dorsal view. The ceratohyals are joined medially by the pars reuniens, shorter than
the basibranchial. The basihyal is absent and the basibranchial bears a short urobranchial process (17% of the
basibranchial length). The hypobranchial plates are triangular, and they articulate medially leaving a posterior
long gap. The ceratobranchials are long, thin, and have numerous lateral projections. They are distally joined
by terminal commissures. Dorsally, there appear two well-defined spicules, corresponding to ceratobranchials
I and II. The third and fourth spicules fuse forming a quadrangular, scarcely chondrified plate, continuous
with the hypobranchial plate.
Musculature (N = 5, stages 34 and 35. Table 10 and Fig. 35). Thirty-three muscles appear in this species.

TABLE 10. Lysapsus limellum, stages 34 and 35. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Mandibulolabialis

two slips: ventromedial region of Meckels


cartilage lower lip of the oral disc
(mandibulolabialis inferior), and commissural
region and part of the upper lip (mandibulolabialis
superior)

Intermandibularis

ventromedial region of Meckels cartilage


median aponeurosis

Levator mandibulae longus


superficialis

Comments

external and posterior margin of the subocular bar,


and ascending process of the palatoquadrate
dorsomedial region of Meckels cartilage
...... continued

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TABLE 10 (continued)
Muscle

Insertions

Comments

Levator mandibulae longus


profundus

external and posterior margins of the subocular


bar and ascending process of the palatoquadrate
ventral margin of the ala of the suprarostral

Levator mandibulae internus

ventral surface of the ascending process, and


anteroventral surface of the otic capsule distal
edge of Meckels cartilage

the insertion is via a long tendon

Levator mandibulae externus


superficialis

medial, inferior surface of the muscular process


mandibulosuprarostral ligament

it is scarcely developed; the mandibular


branch of the trigeminal nerve (V3) runs
dorsally to this muscle

Levator mandibulae externus


profundus

medial, inferior surface of the muscular process


medial region of the lateral margin of the ala of the
suprarostral

its insertion is via a tendon shared with


the m. l. m. l. profundus

Levator mandibulae articularis

inferior part of the medial surface of the muscular


process dorsal surface of the lateral edge of
Meckels cartilage

Levator mandibulae lateralis

articular process of the palatoquadrate nasal sac

Suspensoriohyoideus

posterior descending margin of the muscular


process posterior surface of the lateral process of
the ceratohyal

Orbitohyoideus

anterior, dorsal margin of the muscular process


lateral edge of the ceratohyal

Suspensorioangularis

inferior, lateral surface of the descending margin


of the muscular process retroarticular process of
Meckels cartilage

fibers occupy approximately the lower


half of the muscular process

Quadratoangularis

ventral surface of the palatoquadrate


retroarticular process of Meckels cartilage

it is completely covered by the m.


hyoangularis

Hyoangularis

dorsal surface of the ceratohyal retroarticular


process of Meckels cartilage

Interhyoideus

ventral surface of the ceratohyal, near the lateral


edge median aponeurosis

Interhyoideus posterior

fibers loosely disposed, ventral to the


peribranchial chamber, in the region of the
anterior ceratobranchials

Diaphragmatopraecordialis

connective tissue near the insertion of the fibers of


the m. interhyoideus posterior connective tissue
dorsal to the pericardium

Geniohyoideus

posterior, ventral surface of the infrarostral


hypobranchial plates

Levator arcuum branchialium I

lateral margin of the subocular bar


ceratobranchial I

Levator arcuum branchialium II

larval otic process terminal commissure I

Levator arcuum branchialium III

lateral part of the otic capsule terminal


commissure II
...... continued

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TABLE 10 (continued)
Muscle

Insertions

Comments

Levator arcuum branchialium IV

posterolateral part of the otic capsule


ceratobranchial IV

it is divided clearly into two slips,


separated from their origin on the otic
capsule

Tympanopharyngeus

posterolateral surface of the otic capsule


connective tissue anterior to the glottis

it is thin and short, and the fibers are


almost completely separated from those
of the m. l. a. b. IV

Dilatator laryngis

posterolateral surface of the otic capsule


arytenoid cartilage

Constrictor branchialis II

branchial process II terminal commissure I

it is disposed on the ceratobranchial I

Constrictor branchialis III

branchial process II terminal commissure II

it is disposed on the ceratobranchial II

Constrictor branchialis IV

proximal part of the ceratobranchial III terminal


commissure III

it is disposed on the ceratobranchial III

Subarcualis rectus I

three slips: lateral base of the posterior process of


the ceratohyal proximal part of the
ceratobranchial I (dorsal and ventral1 slips), and
branchial process III (ventral2 slip)

Subarcualis rectus IIIV

two slips: proximal part of the ceratobranchial I


branchial process III (anterior slip), and branchial
process III ventral part of the ceratobranchial IV
(posterior slip)

Subarcualis obliquus

urobranchial process branchial process III

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum branchial process III

Rectus abdominis

peritoneum pelvic griddle

FIGURE 35. Lysapsus limellum, stage 35. Musculature (A) Dorsal view, superficial plane, (B) Dorsal view, middle plane, (C) Dorsal
view, deep plane, (D) Ventral view, (E) Lateral view, superficial plane, (F) Lateral view, deep plane, (G) Ventral view, whole. CB(IIIV) constrictor branchialis, DB diaphragmatobranchialis, GH geniohyoideus, HA hyoangularis, IH interhyoideus, IM intermandibularis, LB(I-IV) levator arcuum branchialium, LMA levator mandibulae articularis, LMEP levator mandibulae externus profundus,
LMES levator mandibulae externus superficialis, LMI levator mandibulae internus, LML levator mandibulae lateralis, LMLP levator
mandibulae longus profundus, LMLS levator mandibulae longus superficialis, ML mandibulolabialis, OH orbitohyoideus, QA quadratoangularis, RA rectus abdominis, SA suspensorioangularis, SH suspensoriohyoideus, SO subarcualis obliquus, SRI subarcualis rectus
I, SRII-IV(a-p) subarcualis rectus II-IV (anterior posterior), TP tympanopharyngeus. Scale lines = 1 mm.

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FIGURE 36. Lysapsus limellum, stage 31. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B) Buccal roof, (C)
Buccal floor. BFA buccal floor arena, BFAP buccal floor arena papilla, BP buccal pocket, BRA buccal roof arena, BRAP buccal roof
arena papilla, C choana, GZ glandular zone, ILP infralabial papilla, IR infrarostrodont, LP lingual papilla, LRP lateral ridge papilla,
MP marginal papilla, MR median ridge, NV narial valve, P pustulation, PNA prenarial arena, PTNA postnarial arena, PTNP postnarial
papilla, SMP submarginal papilla, SR suprarostrodont, TA tongue anlage, VV ventral velum. Scale lines = 1 mm.

Oral apparatus and buccopharyngeal cavity (N = 2, stages 31 and 35. Fig. 36). The oral disc represents
nearly 20% of the body length, and gape width reaches 15% of the body length. The papillar margin is simple,
interrupted in a wide dorsal gap, and it is accompanied by scarce submarginal papillae in the commissural
regions. The rostrodonts are serrated, well-developed and keratinized. The keratodonts are arranged in five
rows, two upper (anterior) and three lower (posterior) resulting in a LTRF 2(2)/3. The row P3 is the shortest
one, with a length nearly 1/3 of A1. In the buccal roof, the prenarial arena shows a medial group of pustules.
The choanae are transversely arranged and have small prenarial papillae on the anterior margin and a welldeveloped narial valve. The postnarial arena shows two pairs of long, conical papillae and several pustules.
The lateral ridge papillae are long and conical. The median ridge is trapezoid with a pustulate free margin. The
buccal roof arena is not well-defined, and it shows two pairs of conical, short papillae, and scarce pustules.
The glandular zone shows small secretory pits. The dorsal velum is thin and short. In the buccal floor, poste-

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rior to the infrarostrodonts, there are groups of pustules transversely aligned on both sides of the longitudinal
axis. Posteriorly, there are three pairs of infralabial papillae: the most anterior pair consists of short, bifid
papillae; the second pair includes small, conical papillae; and the third pair, located on the Meckels cartilage,
includes tall, flat, multifid papillae that converge toward the middle axis. On the tongue anlage, there is one
pair of conical lingual papillae. The buccal floor arena is delimited by 7 pairs of conical, symmetrically
arranged papillae. The two anterior pairs are the smaller and locate posteriorly to the tongue anlage, anteroposteriorly aligned. The four following pairs are located at the level of the buccal pockets, and the remaining
pair locates far caudally. Several pustules scatter among the papillae. The buccal pockets are deep and transversely oriented. The ventral velum is semicircular and has a V-shaped median notch; marginal projections are
absent, and a secretory epithelium develops on the posterior ventral surface.
Gut content (N = 6, stages 2931. Tables 21 and 22). The gut content was mainly composed of crustaceans and diatoms, and the more represented sizes were those smaller to 6% of the tadpole size. Filamentous
chlorophytes were abundant.
Phyllomedusa hypochondrialis. Ulloa Kreisel (2003) described the buccopharyngeal cavity of this species.
Recently, Alcalde (2005) described cranial musculature. Remaining morphological data presented are unpublished. Lajmanovich (1998) and Vera Candioti and Lajmanovich (1998) studied qualitative composition of the
diet.
Chondrocranium and hyobranchial skeleton (N = 5, stages 3134. Fig. 37). The chondrocranium of these
larvae represents 74% of the body length. The maximum width is at the plane of the posterior part of the subocular bar and the larval otic process. The suprarostral cartilage has a single, U-shaped corpus that is dorsally
fused to the alae. These are well-defined, ventrally rounded, and bear well-defined dorsalis anterior and posterior processes. The trabecular horns correspond approximately to 19% of the total length of the chondrocranium and diverge from the ethmoid plate. The cranial floor is completely cartilaginous. The carotid and
craniopalatine foramina are visible. In the posterior margin of the cranial floor, the notochordal canal extends
17% of the chondrocranium length. The lateral walls of the chondrocranium are formed by the orbital cartilages. The chondrocranium is open dorsally, and the frontoparietal fenestra is bordered by the taeniae tecti
marginales. The otic capsules are ovoid and occupy nearly 28% of the chondrocranium total length. The
fenestra ovalis reaches 47% of the capsule length. The otic capsules are dorsally joined by the tectum synoticum. The palatoquadrate has a wide articular process, a triangular muscular process, and a subocular bar with
three lateral, triangular, flat projections. The palatoquadrate attaches to the braincase via three points: the
quadratocranial commissure, bearing a quadratoethmoid process; the ascending process, joined to the braincase floor; and the larval otic process. In the lower jaw, Meckels cartilages are long, with conspicuous ventromedial and retroarticular processes. The infrarostral cartilages are short, rectangular and independent. In the
hyobranchial apparatus, the ceratohyals are long and have a rounded anterior process, a small anterolateral
process, an acute lateral process, and a tall and wide posterior process; the articular condyle is a rounded,
robust protuberance on the dorsal surface. The ceratohyals are joined medially by a pars reuniens shorter than
the basibranchial. The basihyal is very small and the basibranchial is long and bears a long urobranchial process (about 50% of the basibranchial length). The hypobranchial plates are small, subquadrangular and flat,
and they articulate medially leaving a posterior ovoid gap. The ceratobranchials are long, thin, and have
numerous lateral projections. They are distally joined by terminal commissures. Four long cartilaginous spicules arise dorsally from each ceratobranchial.
Musculature (N = 5, stages 3134. Table 11 and Fig. 38). Thirty-three muscles are present in this species.

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FIGURE 37. Phyllomedusa hypochondrialis, stage 33. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view,
(B) Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral cartilage. A ala, ALPC anterolateral process of ceratohyal, APC anterior process of ceratohyal, ARP articular process, ASP
ascending process, BB basibranchial, BH basihyal, C corpus, CB(I-IV) ceratobranchial, CF carotid foramen, CH ceratohyal, CPF
craniopalatine foramen, FF frontoparietal fenestra, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral cartilage, LOP larval
otic process, LPC lateral process of ceratohyal, MC Meckels cartilage, MP muscular process, NC notochordal canal, OC otic capsule,
PDA processus dorsalis anterior, PDP processus dorsalis posterior, PPC posterior process of ceratohyal, PR pars reuniens, QCC
quadratocranial commissure, QP quadratoethmoid process, RP retroarticular process, S spicule, SB subocular bar, SC suprarostral cartilage, SF subocular fenestra, TC terminal commissure, TH trabecular horn, TS tectum synoticum, TTM taenia tecti marginalis, UP
urobranchial process. Scale lines = 1 mm.

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FIGURE 38. Phyllomedusa hypochondrialis, stage 33. Musculature (A) Dorsal view,
superficial plane, (B) Dorsal view, middle plane, (C) Dorsal view, deep plane, (D) Ventral
view, (E) Lateral view, superficial plane, (F) Lateral view, deep plane, (G) Ventral view,
whole. CB(II-IV) constrictor branchialis, GH geniohyoideus, HA hyoangularis, IH
interhyoideus, IM intermandibularis, LB(I-IV) levator arcuum branchialium, LMA levator
mandibulae articularis, LMEP levator mandibulae externus profundus, LMES levator
mandibulae externus superficialis, LMI levator mandibulae internus, LML levator
mandibulae lateralis, LMLP levator mandibulae longus profundus, LMLS levator
mandibulae longus superficialis, ML mandibulolabialis, OH orbitohyoideus, QA
quadratoangularis, RA rectus abdominis, RC rectus cervicis, SA suspensorioangularis, SH
suspensoriohyoideus, SO subarcualis obliquus, SRI subarcualis rectus I, SRII-IV
subarcualis rectus II-IV, TP tympanopharyngeus. Scale lines = 1 mm.

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TABLE 11. Phyllomedusa hypochondrialis, stages 3134. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

ventromedial region of Meckels cartilage lower lip


and part of the upper lip of the oral disc

the division into two slips is not


evident

Intermandibularis

medial region of Meckels cartilage median


aponeurosis

Levator mandibulae longus


superficialis

external margin of the subocular bar dorsomedial


region of Meckels cartilage

Levator mandibulae longus


profundus

external margin of the subocular bar ventral margin of


the ala of the suprarostral

the area of origin coincides with


that of the m. l. m. l. superficialis;
both muscles arise as a single
muscle that divides nearly the site
of insertion

Levator mandibulae internus

ventral surface of the ascending process distal edge of


Meckels cartilage

the insertion is via a long tendon,


approximately 1/2 the length of the
whole muscle

Levator mandibulae externus


superficialis

medial, inferior surface of the muscular process lateral


edge of the ala of the suprarostral

it is formed of few loose fibers,


and the mandibular branch of the
trigeminal nerve (V3) runs
ventrally to it

Levator mandibulae externus


profundus

medial, inferior surface of the muscular process


lateroventral margin of the ala of the suprarostral

its insertion is via a tendon shared


with the m. l. m. l. profundus

Levator mandibulae articularis

inferior part of the medial surface of the muscular


process dorsal surface of the lateral edge of Meckels
cartilage

Levator mandibulae lateralis

articular process of the palatoquadrate dorsal, lateral


edge of the suprarostral

Suspensoriohyoideus

posterior descending margin of the muscular process


posterior surface of the lateral process of the ceratohyal

Orbitohyoideus

anterior, dorsal margin of the muscular process lateral


edge of the ceratohyal

Suspensorioangularis

inferior, lateral part of the descending margin of the


muscular process retroarticular process of Meckels
cartilage

Quadratoangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

Hyoangularis

dorsal surface of the ceratohyal, anterior to the articular


condyle retroarticular process of Meckels cartilage

Interhyoideus

ventral surface of the ceratohyal, near the lateral edge


median aponeurosis

Interhyoideus posterior

fibers loosely disposed, ventral to the peribranchial


chamber, in the region of the anterior ceratobranchials

Diaphragmatopraecordialis

connective tissue near to the insertion of the fibers of the


m. interhyoideus posterior connective tissue dorsal to
the pericardium

Geniohyoideus

posterior, ventral surface of the infrarostral


hypobranchial plates

it is a short muscle, formed of a


few fibers

the site of origin is concealed by


the m. orbitohyoideus; fibers
occupy approximately the lower
third of the muscular process

it is formed of parallel, transverse


fibers, disposed in a plane nearly
perpendicular to the
chondrocranial longitudinal axis

...... continued

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TABLE 11 (continued)
Muscle

Insertions

Comments

Levator arcuum branchialium I

lateral margin of the subocular bar ceratobranchial I

it is the widest of the mm. l. a.


branchialium; its insertion onto the
ceratobranchial occupies a large
surface

Levator arcuum branchialium II

subocular bar terminal commissure I

Levator arcuum branchialium III

lateroventral part of the otic capsule terminal


commissure II

Levator arcuum branchialium IV

posterolateral part of the otic capsule medial margin of


the ceratobranchial IV

Tympanopharyngeus

posterolateral surface of the otic capsule connective


tissue of the pericardium

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process II terminal commissure I

Constrictor branchialis III

branchial process II terminal commissure II

it is disposed on the
ceratobranchial II

Constrictor branchialis IV

branchial process III terminal commissure III

it is disposed on the
ceratobranchial III

Subarcualis rectus I

two slips: lateral base of the posterior process of the


ceratohyal proximal part of the ceratobranchial I
(dorsal slip), and branchial process II (ventral slip)

Subarcualis rectus II-IV

branchial process II proximal, ventral part of the


ceratobranchial IV

Subarcualis obliquus

urobranchial process branchial process II

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum branchial process III

Rectus abdominis

peritoneum pelvic griddle

it has two distinguishable slips

it is well-developed; it originates
almost at the level of the branchial
basket

Oral apparatus and buccopharyngeal cavity (N = 2, stage 33. Fig. 39). The oral disc represents 21% of
the body length, and gape width reaches 18% of the body length. The oral disc is not emarginate. Marginal
papillae are arranged in a simple margin on the upper lip and commissures, and a double margin on the lower
lip; the dorsal gap is as long as the suprarostrodont length. Several submarginal papillae appear in the commissural region. The rostrodonts are well-developed and keratinized. The keratodonts are arranged in five
rows, two upper (anterior) and three lower (posterior), resulting in a LTRF 2(2)/3(1). The row A2 is interrupted by a wide, median gap; P1 is discontinuous as well, but the sections are very close to each other. The
row P3 is very short and in some specimens has a median gap. In the buccal roof, the prenarial arena shows a
well-developed ridge with two crescent-shaped, crenulate portions. The choanae are transversely arranged;
the anterior margin has small prenarial papillae, and the narial valves are scarcely developed. In the postnarial
arena there is one pair of bifid, medially oriented papillae. The lateral ridge papillae are flat and bifid. The
median ridge is low, slightly semicircular, and with an irregular free margin. The buccal roof arena is not
defined; the central region of the buccal roof has numerous pustules and few small papillae. The glandular
region appears as a posterior, V-shaped array with secretory pits. The dorsal velum is relatively long, curled,

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and medially interrupted in a wide gap. In the buccal floor, there is a pair of bifurcate infralabial papillae
medially directed. The tongue anlage shows two short, conical lingual papillae. The buccal floor arena is
delimited on both sides by two pairs of tall peripheral papillae, the anterior pair, bifid and flat, and the posterior pair, conical and shorter. Among them, and on the lateral portion of the ceratohyals, there appear numerous pustules. The buccal pockets are elongate and transversally oriented. The ventral velum is long and
supported by spicules; it has three pronounced marginal projections on the filer plates, and a triangular median
notch surrounded by a couple of acute projections. Secretory pits appear on the posterior ventral surface of the
velum.

FIGURE 39. Phyllomedusa hypochondrialis, stage 33. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B)
Buccal roof, (C) Buccal floor. BFA buccal floor arena, BFAP buccal floor arena papilla, BP buccal pocket, C choana, DG dorsal gap,
DV dorsal velum, GZ glandular zone, ILP infralabial papilla, IR infrarostrodont, LK lower keratodonts, LP lingual papilla, LRP lateral
ridge papilla, MP marginal papilla, MR median ridge, P pustulation, PNA prenarial arena, PTNA postnarial arena, PTNP postnarial
papilla, SR suprarostrodont, TA tongue anlage, UK upper keratodonts, VV ventral velum. Scale lines = 1 mm.

Gut content (N = 7, stages 3134. Tables 21 and 22). The gut content was mainly composed of diatoms
and rotifers with sizes mostly smaller to 2% of the tadpole size. Numerous filamentous chlorophytes and
debris, considered non-quantifiable, also appeared in the samples.
Phyllomedusa sauvagii. Previous literature for this species includes the studies by Fabrezi and Lavilla (1992)
and Fabrezi and Vera (1997).

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FIGURE 40. Phyllomedusa sauvagii, stage 33. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B)
Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral
cartilage. A ala, ALPC anterolateral process of ceratohyal, APC anterior process of ceratohyal, ARP articular process, ASP ascending
process, BB basibranchial, BH basihyal, C corpus, CB(I-IV) ceratobranchial, CF carotid foramen, CH ceratohyal, CPF craniopalatine
foramen, FF frontoparietal fenestra, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral cartilage, LOP larval otic process, LPC
lateral process of ceratohyal, MC Meckels cartilage, MP muscular process, NC notochordal canal, OC otic capsule, OF oculomotor
foramen, OPF optic foramen, PDA processus dorsalis anterior, PDP processus dorsalis posterior, PF prootic foramen, PPC posterior
process of ceratohyal, PR pars reuniens, QCC quadratocranial commissure, QP quadratoethmoid process, RP retroarticular process, S
spicule, SB subocular bar, SC suprarostral cartilage, SF subocular fenestra, TC terminal commissure, TH trabecular horn, TF trochlear
foramen, TS tectum synoticum, TTM taenia tecti marginalis, UP urobranchial process. Scale lines = 1 mm.

Chondrocranium and hyobranchial skeleton (N = 5, stages 3136. Fig. 40). The chondrocranium of these
larvae represents 45% of the body length. The maximum width is at the plane of the posterior part of the subocular bar and the larval otic process. The suprarostral cartilage has a single, U-shaped corpus dorsally fused
to the alae. These are well-defined, ventrally rounded, and bear developed dorsalis anterior and posterior processes. The trabecular horns correspond approximately to 22% of the total length of the chondrocranium and
diverge from the ethmoid plate. They show an irregular anterior margin, and on the lateroventral margin, the
processus lateralis trabeculae is slightly outlined. The cranial floor is completely cartilaginous. The carotid

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and craniopalatine foramina are clearly identifiable. In the posterior margin of the cranial floor, the notochordal canal extends 18% of the chondrocranium length. The lateral walls of the chondrocranium are formed
by the orbital cartilages. Three foramina are observed: the optic foramen, posteroinferiorly located, the oculomotor foramen, nearly 1/5 of the former foramen, and the trochlear foramen, very small and dorsally placed.
The chondrocranium is open dorsally through a frontoparietal fenestra lined by the taeniae tecti marginales.
The otic capsules are ovoid and occupy nearly 33% of the chondrocranium total length. The fenestra ovalis
represents 33% of the capsule length. The otic capsules are dorsally joined by the tectum synoticum; in the
anterior margin of the tectum, the taenia tecti medialis is outlined. The palatoquadrate is relatively narrow. It
shows a long and thin articular process, a high, triangular muscular process, and a subocular bar with three
long, triangular lateral projections. The palatoquadrate attaches to the braincase via three points: the quadratocranial commissure, which bears a quadratoethmoid process, the ascending process attached to the braincase
floor, and the larval otic process. In the lower jaw, Meckels cartilages are long and bear rounded ventromedial
and retroarticular processes. The infrarostral cartilages are short, rectangular and independent. In the hyobranchial skeleton, the ceratohyals are long and have a tall and rounded anterior process, a small anterolateral process, a rounded posterior process, and a wide and tall posterior process; the articular condyle is robust, visible
from a dorsal view. The ceratohyals are joined medially by a pars reuniens shorter than the basibranchial. The
basihyal is very small and the basibranchial is long and bears a long urobranchial process (30% of the basibranchial length). The hypobranchial plates are triangular and articulate medially leaving a posterior ovoid
gap. The ceratobranchials are long, thin, and have numerous lateral projections. They are distally joined by
terminal commissures. Four long cartilaginous spicules arise dorsally from each ceratobranchial.
Musculature (N = 5, stages 3136. Table 12 and Fig. 41). Thirty-three muscles are present in this species.

TABLE 12. Phyllomedusa sauvagii, stages 3136. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

ventromedial region of Meckels cartilage lower lip


and part of the upper lip of the oral disc

it is well-developed, but the


division into two slips is not
evident

Intermandibularis

anteromedial region of Meckels cartilage median


aponeurosis

Levator mandibulae longus


superficialis

external margin of the subocular bar dorsomedial


region of Meckels cartilage

Levator mandibulae longus


profundus

external margin of the subocular bar ventral margin of


the ala of the suprarostral

the area of origin is smaller than


that of the m. l. m. l. superficialis,
and insertion is through a welldeveloped, long tendon shared with
the m. l. m. externus profundus

Levator mandibulae internus

ventral surface of the ascending process distal edge of


Meckels cartilage

the insertion is via a long tendon

Levator mandibulae externus


superficialis

medial, inferior surface of the muscular process lateral


edge of the ala of the suprarostral

it is formed of a few loose fibers;


the mandibular branch of the
trigeminal nerve (V3) runs
ventrally to this muscle

Levator mandibulae externus


profundus

medial, inferior surface of the muscular process


lateroventral margin of the ala of the suprarostral

Levator mandibulae articularis

inferior part of the medial surface of the muscular


process dorsal surface of the lateral edge of Meckels
cartilage

Levator mandibulae lateralis

articular process of the palatoquadrate dorsal, lateral


edge of the suprarostral

it is a short muscle, formed of a


few fibers
...... continued

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TABLE 12 (continued)
Muscle

Insertions

Comments

Suspensoriohyoideus

posterior descending margin of the muscular process


posterior surface of the lateral process of the ceratohyal

it is formed of a few fibers, loosely


disposed

Orbitohyoideus

anterior, dorsal margin of the muscular process lateral


edge of the ceratohyal

Suspensorioangularis

inferior, lateral part of the descending margin of the


muscular process retroarticular process of Meckels
cartilage

Quadratoangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

Hyoangularis

dorsal surface of the ceratohyal, anterior to the articular


condyle retroarticular process of Meckels cartilage

it shows an incipient division in the


anterior portion

Interhyoideus

ventral surface of the ceratohyal, near the lateral edge


median aponeurosis

it is formed of parallel, transverse


fibers

Interhyoideus posterior

fibers loosely disposed, ventral to the peribranchial


chamber, in the region of the anterior ceratobranchials

Diaphragmatopraecordialis

connective tissue near to the insertion of the fibers of the


m. interhyoideus posterior connective tissue dorsal to
the pericardium

Geniohyoideus

posterior, ventral surface of the infrarostral


hypobranchial plates

Levator arcuum branchialium I

lateral margin of the subocular bar ceratobranchial I

Levator arcuum branchialium II

subocular bar terminal commissure I

Levator arcuum branchialium III

lateroventral part of the otic capsule terminal


commissure II

Levator arcuum branchialium


IV

posterolateral part of the otic capsule medial margin of


the ceratobranchial IV

Tympanopharyngeus

posterolateral surface of the otic capsule connective


tissue of the pericardium

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process II terminal commissure I

Constrictor branchialis III

branchial process II terminal commissure II

it is disposed on the
ceratobranchial II

Constrictor branchialis IV

branchial process II terminal commissure III

it is disposed on the
ceratobranchial III

Subarcualis rectus I

two slips: lateral base of the posterior process of the


ceratohyal proximal part of the ceratobranchial I
(dorsal slip), and branchial process II (ventral slip)

Subarcualis rectus II-IV

branchial process II proximal, ventral part of the


ceratobranchial IV

Subarcualis obliquus

urobranchial process branchial process II

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum pelvic griddle

it is the widest of the mm. l. a.


branchialium; its insertion onto the
ceratobranchial occupies a large
surface

it has two distinguishable slips

peritoneum branchial process III

Rectus abdominis

the site of origin is concealed by


the m. orbitohyoideus; fibers
occupy approximately the lower
half of the muscular process

ANATOMY OF ANURAN TADPOLES

it is well-developed; it originates
almost at the level of the branchial
basket

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FIGURE 41. Phyllomedusa sauvagii, stage 36. Musculature (A) Dorsal view, superficial plane, (B) Dorsal view, middle plane, (C)
Dorsal view, deep plane, (D) Ventral view, (E) Lateral view, superficial plane, (F) Lateral view, deep plane, (G) Ventral view, whole.
CB(II-IV) constrictor branchialis, DB diaphragmatobranchialis, GH geniohyoideus, HA hyoangularis, IH interhyoideus, IM intermandibularis, LB(I-IV) levator arcuum branchialium, LMA levator mandibulae articularis, LMEP levator mandibulae externus profundus,
LMES levator mandibulae externus superficialis, LMI levator mandibulae internus, LML levator mandibulae lateralis, LMLP levator
mandibulae longus profundus, LMLS levator mandibulae longus superficialis, ML mandibulolabialis, OH orbitohyoideus, QA quadratoangularis, RA rectus abdominis, RC rectus cervicis, SA suspensorioangularis, SH suspensoriohyoideus, SO subarcualis obliquus,
SRI subarcualis rectus I, SRII-IV subarcualis rectus II-IV, TP tympanopharyngeus. Scale lines = 1 mm.

FIGURE 42. Phyllomedusa sauvagii, stage 33. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B) Buccal
roof, (C) Buccal floor. BFA buccal floor arena, BFAP buccal floor arena papilla, BP buccal pocket, BRA buccal roof arena, BRAP
buccal roof arena papilla, C choana, DG dorsal gap, DV dorsal velum, GZ glandular zone, ILP infralabial papilla, IR infrarostrodont,
LK lower keratodonts, LP lingual papilla, LRP lateral ridge papilla, MP marginal papilla, MR median ridge, P pustulation, PNA prenarial arena, PTNA postnarial arena, PTNP postnarial papilla, SMP submarginal papilla, SR suprarostrodont, TA tongue anlage, UK
upper keratodonts, VV ventral velum. Scale lines = 1 mm.

Oral apparatus and buccopharyngeal cavity (N = 2, stages 33 and 36. Fig. 42). The oral disc represents
20% of the body length and gape width reaches 19% of the body length. The marginal papillae are large,
arranged in a simple margin, and interrupted in a dorsal gap. Several submarginal papillae appear in the commissural region. The rostrodonts are well-developed and keratinized. The keratodonts are arranged in five
rows, two upper (anterior) and three lower (posterior), resulting in a LTRF 2(2)/3(1). The row A2 is interrupted by a wide, median gap; the row P1 is also discontinuous, but sections are very close to each other. The
P3 is very short, approximately half the P2. In the buccal roof, the prenarial arena shows a well-developed
ridge, with two crescent-shaped portions with irregular margin. The choanae are transversely arranged; the
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anterior margin has small prenarial papillae, and the narial valve is scarcely developed. In the postnarial arena
there is one pair of bifid papillae, medially oriented. The lateral ridge papillae are flat and wide, with three
short tips. The median ridge is low, slightly triangular, and with a pustulate free margin. The buccal roof arena
is defined by three pairs of conical papillae; numerous pustules scatter on the central region. The glandular
region is a posterior, V-shaped array with secretory pits. The dorsal velum is long and curled, and interrupts
medially in a wide gap. Posteriorly, near the oesophagic funnel, there is a set of large pre-oesophagic papillae.
In the buccal floor, there is one pair of tall, multifid, non-overlapping infralabial papillae. The tongue anlage
has two tall, bifurcate lingual papillae. The buccal floor arena is delimited by 6 pairs of peripheral, tall, conical papillae. Among them, and on the lateral portion of the ceratohyals, numerous pustules there appear. The
buccal pockets are elongate and obliquely oriented. The ventral velum is long and supported by spicules; it
shows three pronounced marginal projections on the filter plates, and a median notch surrounded by two
rounded projections; secretory pits appear on the posterior ventral surface of the velum.
Gut content (N = 6, stages 3136. Tables 21 and 22). The gut content was almost completely composed of
small euglenoids with sizes smaller than 1% of the tadpole size.
Pseudis paradoxus. Characters of the chondrocranium and musculature of this species were described in Haas
(2003) and Alcalde and Barg (2006). The oral apparatus and buccopharyngeal cavity were described in Rada
and Bello (1988) and Ulloa Kreisel (2003). An analysis of the qualitative composition of the diet appeared in
Arias et al. (2002).
Chondrocranium and hyobranchial skeleton (N = 2, stages 31 and 35. Fig. 43). The chondrocranium of
these larvae represents 37% of the body length. The maximum width is at the plane of the middle portion of
the subocular bar. The suprarostral cartilage has a single corpus with a deep, narrow dorsal notch; the corpus
is completely fused to the alae. These bear developed dorsalis anterior and posterior processes. The trabecular
horns correspond approximately 21% of the total length of the chondrocranium and diverge from the ethmoid
plate. They show relatively straight anterior margins and are slightly wider anteriorly. The nasal septum and
small antorbital processes are developed. On the lateroventral margin, the processus lateralis trabeculae is
slightly outlined. The cranial floor is completely cartilaginous. The dermal primordium of the parasphenoid is
present and has an elongate, triangular shape. The carotid foramina are visible on both sides of the parasphenoid. In the posterior margin of the cranial floor, the notochordal canal extends 16% of the chondrocranium
length. The orbital cartilages are represented by a posterior chondrification (pila metoptica, according to
Lavilla & De S, 1999). The cranial roof is closed in the most posterior region, and the taeniae tecti marginales are well-developed. The otic capsules are small, quadrangular, and occupy nearly 19% of the chondrocranium total length. The fenestra ovalis reaches 55% of the capsule length and it is located ventrolaterally on
each otic capsule. The palatoquadrate has a thin and long articular process and a low, triangular, medially
curved muscular process. The subocular bar is very wide at the middle portion, forming a flat, triangular projection. The palatoquadrate attaches to the braincase via three points: the quadratocranial commissure, the
ascending process, and the larval otic process. The quadratocranial commissure is thin and bears a well-developed quadratoethmoid process and a large pseudopterygoid process. The ascending process attaches to the
braincase floor (ultralow attachment). In the lower jaw, Meckels and infrarostral cartilages are joined by a
cartilaginous intermandibular commissure. Meckels cartilages are sigmoid in shape and bear rounded retroarticular and ventromedial processes. The infrarostral cartilages are short, rectangular, curved, and are joined by
an intramandibular commissure. In the hyobranchial skeleton, the ceratohyals are long and have a triangular,
medially directed anterior process, a small and pointed anterolateral process, a rounded lateral process, and a
wide posterior process; the articular condyle is a rounded protuberance on the dorsal surface. The ceratohyals
are joined medially by a pars reuniens shorter than the basibranchial. The basihyal is absent and the basibranchial bears a rounded urobranchial process (30% of the basibranchial length). The hypobranchial plates are
quadrangular and medially continuous, excepting a small posterior gap. The ceratobranchials are long, thin,

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and with numerous lateral projections. They are distally joined by terminal commissures. The ceratobranchials II and III are joined by a conspicuous branchial bridge. Dorsally, there appear two well-defined spicules
corresponding to ceratobranchials I and II. The third and fourth spicules fuse to the posterior part of the hypobranchial plates forming a quadrangular, scarcely chondrified plate.

FIGURE 43. Pseudis paradoxus, stage 35. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B) Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral cartilage. A ala, ALPC anterolateral process of ceratohyal, ANP antorbital process, APC anterior process of ceratohyal, ARP articular
process, ASP ascending process, BB basibranchial, C corpus, CB(I-IV) ceratobranchial, CF carotid foramen, CH ceratohyal, CP crista
parotica, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral cartilage, LOP larval otic process, LPC lateral process of ceratohyal, MC Meckels cartilage, MP muscular process, NC notochordal canal, NS nasal septum, OC otic capsule, PDA processus dorsalis
anterior, PDP processus dorsalis posterior, PPC posterior process of ceratohyal, PP pseudopterygoid process, PR pars reuniens, PS
parasphenoid, QCC quadratocranial commissure, QP quadratoethmoid process, RP retroarticular process, S spicule, SB subocular bar,
SC suprarostral cartilage, SF subocular fenestra, TC terminal commissure, TH trabecular horn, TS tectum synoticum, TTM taenia tecti
marginalis, UP urobranchial process. Scale lines = 1 mm.

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Musculature (N = 2, stages 31 and 35. Table 13 and Fig. 44). Thirty-four muscles appear in this species.
TABLE 13. Pseudis paradoxus, stages 31 and 35. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

two slips: ventromedial region of Meckels cartilage


lower lip of the oral disc (mandibulolabialis inferior),
and commissural region and part of the upper lip
(mandibulolabialis superior)

Submentalis

this muscle joins the infrarostral cartilages


ventromedially

it is well-developed and does not


have a median aponeurosis

Intermandibularis

ventromedial region of Meckels cartilage median


aponeurosis

it is well-developed and ventrally


covered by alcianophylic
conjunctive tissue

Levator mandibulae longus


superficialis

external and posterior margin of the subocular bar


dorsomedial region of Meckels cartilage

Levator mandibulae longus


profundus

external and posterior margins of the subocular bar


ventral margin of the ala of the suprarostral

the origin surface is nearly as wide


that of the m. l. m. l. superficialis

Levator mandibulae internus

dorsal surface of the ascending process distal edge of


Meckels cartilage

the insertion is via a long tendon

Levator mandibulae externus


superficialis

medial, inferior surface of the muscular process lateral


edge of the ala of the suprarostral

it is scarcely developed, formed of


a few loose fibers; the mandibular
branch of the trigeminal nerve (V3)
runs dorsally to this muscle

Levator mandibulae externus


profundus

medial, inferior surface of the muscular process


ventral, lateral medial of the ala of the suprarostral

its insertion is via a tendon shared


with the m. l. m. l. profundus

Levator mandibulae articularis

inferior part of the medial surface of the muscular


process dorsal surface of the lateral edge of Meckels
cartilage

Levator mandibulae lateralis

articular process of the palatoquadrate nasal sac

Suspensoriohyoideus

posterior descending margin of the muscular process


posterior surface of the lateral process of the ceratohyal

Orbitohyoideus

anterior, dorsal margin of the muscular process lateral


edge of the ceratohyal

Suspensorioangularis

inferior, lateral surface of the descending margin of the


muscular process retroarticular process of Meckels
cartilage

fibers occupy less than the lower


half of the muscular process

Quadratoangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

it is completely covered by the m.


hyoangularis

Hyoangularis

dorsal surface of the ceratohyal retroarticular process


of Meckels cartilage

Interhyoideus

ventral surface of the ceratohyal, near the lateral edge


median aponeurosis

Interhyoideus posterior

fibers loosely disposed, ventral to the peribranchial


chamber, in the region of the anterior ceratobranchials

Diaphragmatopraecordialis

connective tissue near to the insertion of the fibers of the


m. interhyoideus posterior dorsal connective tissue of
the pericardium

Geniohyoideus

posterior, ventral surface of the infrarostral


hypobranchial plates

it is well-developed

fibers are disposed almost


perpendicular to the middle line

...... continued

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TABLE 13 (continued)
Muscle

Insertions

Comments

Levator arcuum branchialium I

lateral margin of the subocular bar ceratobranchial I

it is formed of fibers loosely


disposed, and it is the widest of the
mm. levatores branchialium

Levator arcuum branchialium II

larval otic process terminal commissure I

this, and the remaining mm.


levatores branchialium are thin
and compact muscles

Levator arcuum branchialium III

lateral part of the otic capsule terminal commissure II

Levator arcuum branchialium IV

posterolateral part of the otic capsule medial margin of


the ceratobranchial IV

Tympanopharyngeus

posterolateral surface of the otic capsule connective


tissue of the pericardium, anterior to the glottis

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process II terminal commissure I

it is disposed on the
ceratobranchial I

Constrictor branchialis III

branchial process II terminal commissure II

it is disposed on the
ceratobranchial II

Constrictor branchialis IV

branchial process III terminal commissure III

it is disposed on the
ceratobranchial III

Subarcualis rectus I

three slips: lateral base of the posterior process of the


ceratohyal proximal part of the ceratobranchial I
(dorsal slip), branchial process II (ventral1 slip), and
branchial process III (ventral2 slip)

the ventral2 slip is the more


developed

Subarcualis rectus II-IV

two slips: proximal part of the ceratobranchial I


branchial process III (anterior slip), and branchial
process III ventral part of the ceratobranchial IV
(posterior slip)

some fibers are continuous


between both slips

Subarcualis obliquus

urobranchial process branchial processes II and III

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum branchial process III

Rectus abdominis

peritoneum pelvic griddle

it has two clearly distinguishable


slips

Oral apparatus and buccopharyngeal cavity (N = 1, stage 35. Fig. 45). The oral disc width represents
nearly 14% of the body length. Gape width is small, reaching 13% of the body length. The oral disc is lined by
a double margin of marginal papillae grouped by pairs in the lower lip. Large submarginal papillae appear in
the commissural region. The marginal papillation interrupts in a wide dorsal gap. The rostrodonts are finely
serrated. The keratodonts are arranged in five rows, two upper (anterior) and three lower (posterior), resulting
in a LTRF 2(2)/3. The row P1 is the shortest one, with a length nearly 1/2 of P2. In the buccal roof, the prenarial arena shows no distinct features. The choanae are arranged at an angle of about 37 from the transversal
line, and have small prenarial papillae on the anterior margin and a well-developed narial valve. The postnarial arena shows four pairs of transversely arranged papillae. The lateral papillae are flat and bifurcate, whereas
the six medial papillae are low and conical. Some pustules are scattered among these papillae. The lateral
ridge papillae are paired, flat and multifid. The median ridge is wide and trapezoid, with a pustulate free margin. The buccal roof arena is defined by 67 papillae on both sides; among buccal roof papillae and on the
central region, there appear several pustules and short papillae. Secretory pits are present in a broad V-shape
array on the posterior region of the buccal roof. The dorsal velum is short, thin and smooth. In the buccal
floor, posterior to the infrarostrodonts, there are 34 conical or slightly bifid infralabial papillae, on both sides
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of the middle axis. The tongue anlage has a couple of conical lingual papillae. Seven pairs of symmetrically
arranged papilla delimit the buccal floor arena. Several pustules and short papillae scatter laterally on the ceratobranchial and on the posterior region of the arena. The buccal pockets are deep and transversely oriented.
Numerous pustules scatter on the lateral surface of the ceratohyals, the prepocket region, and the buccal floor
arena. The ventral velum is long, supported by spicules, semicircular, with slight undulations on the posterior
margin and a deep median notch. Secretory pits appear on the posterior ventral surface of the velum.

FIGURE 44. Pseudis paradoxus, stage 35. Musculature (A) Dorsal view, superficial plane, (B) Dorsal view, middle plane, (C) Dorsal
view, deep plane, (D) Ventral view, (E) Lateral view, superficial plane, (F) Lateral view, deep plane. CB(II-IV) constrictor branchialis,
DB diaphragmatobranchialis, GH geniohyoideus, HA hyoangularis, IH interhyoideus, IM intermandibularis, LB(I-IV) levator arcuum
branchialium, LMA levator mandibulae articularis, LMEP levator mandibulae externus profundus, LMES levator mandibulae externus superficialis, LMI levator mandibulae internus, LML levator mandibulae lateralis, LMLP levator mandibulae longus profundus,
LMLS levator mandibulae longus superficialis, ML mandibulolabialis, OH orbitohyoideus, QA quadratoangularis, RC rectus cervicis,
SA suspensorioangularis, SH suspensoriohyoideus, SO subarcualis obliquus, SRI subarcualis rectus I, SRII-IV(a-p) subarcualis rectus
II-IV (anterior posterior), TP tympanopharyngeus. Scale lines = 1 mm.

Gut content (N = 2, stage 35. Tables 21 and 22). Nearly 70% of the gut content was composed of insects,
followed by a lower percentage of macrophytes. For such a large tadpole, the size of these items only represent up to 20% of the tadpole body size.

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FIGURE 45. Pseudis paradoxus, stage 35. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B) Buccal roof,
(C) Buccal floor. BFA buccal floor arena, BRAP buccal floor arena papilla, BP buccal pocket, BRA buccal roof arena, BRAP buccal
roof arena papilla, C choana, DG dorsal gap, DV dorsal velum, GZ glandular zone, IR infrarostrodont, LK lower keratodonts, LP lingual papilla, LRP lateral ridge papilla, MP marginal papilla, MR median ridge, P pustulation, PNA prenarial arena, PTNA postnarial
arena, PTNP postnarial papilla, SMP submarginal papilla, SR suprarostrodont, TA tongue anlage, UK upper keratodonts, VV ventral
velum. Scale lines = 1 mm.

Scinax boulengeri. Previous information on this species includes the study by Duellman (1970), on the oral
apparatus. The remaining data are unpublished.
Chondrocranium and hyobranchial skeleton (N = 2, stages 29 and 31. Fig. 46). The chondrocranium of
these larvae represents 65% of the body length. The shape is quadrangular, with maximum width at the plane
of the muscular process and the larval otic process. The suprarostral cartilage is a single U-shaped structure
with acute lateral edges corresponding to the alae. The trabecular horns correspond nearly to 22% of the total
length of the chondrocranium and they show relatively straight anterior margins. The cranial floor is completely cartilaginous and in the posterior margin, the notochordal canal extends 17% of the chondrocranium
length. The carotid foramina are visible. The orbital cartilages are not completely chondrified in the stages
analyzed. The chondrocranium is open dorsally through the frontoparietal fenestra, which is lined by the taeniae tecti marginales. The otic capsules are ovoid and occupy nearly 30% of the chondrocranium total length.

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FIGURE 46. Scinax boulengeri, stage 31. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B) Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of jaws: left,
suprarostral cartilage, frontal view; right, lower jaw, ventral view. ALPC anterolateral process of ceratohyal, APC anterior process of
ceratohyal, ARP articular process, ASP ascending process, BB basibranchial, CB(I-IV) ceratobranchial, CF carotid foramen, CH ceratohyal, FF frontoparietal fenestra, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral cartilage, LOP larval otic process, LPC
lateral process of ceratohyal, MC Meckels cartilage, MP muscular process, NC notochordal canal, OC otic capsule, OF oculomotor
foramen, PPC posterior process of ceratohyal, PR pars reuniens, QCC quadratocranial commissure, RP retroarticular process, S spicule, SB subocular bar, SC suprarostral cartilage, SF subocular fenestra, TC terminal commissure, TH trabecular horn, TS tectum synoticum, TTM taenia tecti marginalis, UP urobranchial process. Scale lines = 1 mm.

FIGURE 47. Scinax boulengeri, stage 31. Musculature (A) Dorsal view, superficial plane, (B) Dorsal view, middle plane, (C) Dorsal
view, deep plane, (D) Ventral view, (E) Lateral view, superficial plane, (F) Lateral view, deep plane, (G) Ventral view, whole. CB(IIIV) constrictor branchialis, DB diaphragmatobranchialis, GH geniohyoideus, HA hyoangularis, IH interhyoideus, IM intermandibularis, LB(I-IV) levator arcuum branchialium, LMA levator mandibulae articularis, LMEP levator mandibulae externus profundus,
LMES levator mandibulae externus superficialis, LMI levator mandibulae internus, LML levator mandibulae lateralis, LMLP levator
mandibulae longus profundus, LMLS levator mandibulae longus superficialis, ML mandibulolabialis, OH orbitohyoideus, QA quadratoangularis, RA rectus abdominis, RC rectus cervicis, SA suspensorioangularis, SH suspensoriohyoideus, SO subarcualis obliquus,
SRI subarcualis rectus I, SRII-IV subarcualis rectus II-IV, TP tympanopharyngeus. Scale lines = 1 mm.

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The large fenestra ovalis reaches 34% of the capsule length and it is located ventrolaterally on each otic capsule. The otic capsules are dorsally joined by the tectum synoticum. The palatoquadrate is relatively narrow. It
has a short and wide articular process, a triangular muscular process, and a uniformly wide subocular bar. The
palatoquadrate attaches to the braincase via three points: the quadratocranial commissure; the ascending process, attached to the neurocranium above the oculomotor foramen; and the larval otic process. In the lower
jaw, Meckels cartilages are massive, short, L-shaped and bear three conspicuous processes: dorsomedial,
well-developed, tall and acute; ventromedial; and retroarticular, medially oriented. The infrarostral cartilages
are short, rectangular and independent. In the hyobranchial apparatus, the ceratohyals are long and have a tall,
triangular anterior process, a narrow and acute anterolateral process, a rounded lateral process, and a tall, wide
posterior process; the articular condyle is a rounded protuberance visible from a dorsal view. The ceratohyals
are joined medially by the pars reuniens, which is shorter than the basibranchial. The basihyal is absent and
the basibranchial bears an urobranchial process (29% of the basibranchial length). The basibranchial is fused
to the hypobranchial plates. The hypobranchial plates are flat and triangular and they articulate medially leaving a small, triangular posterior gap. The ceratobranchials are long, thin, and have numerous lateral projections. They are distally joined by terminal commissures. Four cartilaginous spicules arise dorsally from each
ceratobranchial, the fourth being slightly reduced.
Musculature (N = 2, stages 29 and 31. Table 14 and Fig. 47). Thirty-three muscles appear in this species.
TABLE 14. Scinax boulengeri, stages 29 and 31. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

two slips: ventromedial region of Meckels cartilage


lower lip of the oral disc (mandibulolabialis inferior), and
commissural region and part of the upper lip
(mandibulolabialis superior)

the lower slip is well-developed

Intermandibularis

medial region of the distal edge of Meckels cartilage


median aponeurosis

Levator mandibulae longus


superficialis

external and posterior margin of the subocular bar and


ascending process of the palatoquadrate dorsomedial
region of Meckels cartilage

Levator mandibulae longus


profundus

external margin of the subocular bar and part of the


ascending process of the palatoquadrate external
margin of the ala of the suprarostral

the area of origin is smaller than


that of the m. l. m. l. superficialis

Levator mandibulae internus

ventral surface of the ascending process and otic capsule


distal edge of Meckels cartilage

the insertion is via a long tendon

Levator mandibulae externus


superficialis

medial, inferior surface of the muscular process distal


edge of the ala of the suprarostral

it is scarcely developed; the


mandibular branch of the
trigeminal nerve (V3) runs dorsally
to this muscle

Levator mandibulae externus


profundus

medial, inferior surface of the muscular process


lateroventral margin of the ala of the suprarostral

the insertion is via a tendon shared


with the m. l. m. l. profundus

Levator mandibulae articularis

inferior part of the medial surface of the muscular process


dorsal surface of the lateral edge of Meckels cartilage

it is composed of a few fibers


loosely disposed

Levator mandibulae lateralis

articular process of the palatoquadrate dorsal, lateral


edge of the suprarostral

it is a short muscle, formed of a


few fibers

Suspensoriohyoideus

posterior descending margin of the muscular process


posterior surface of the lateral process of the ceratohyal

Orbitohyoideus

anterior, dorsal margin of the muscular process lateral


edge of the ceratohyal
...... continued

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TABLE 14 (continued)
Muscle

Insertions

Suspensorioangularis

inferior, lateral surface of the descending margin of the


muscular process retroarticular process of Meckels
cartilage

Quadratoangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

Hyoangularis

dorsal surface of the ceratohyal retroarticular process of


Meckels cartilage

Interhyoideus

ventral surface of the ceratohyal, near the lateral edge


median aponeurosis

Interhyoideus posterior

fibers loosely disposed, ventral to the peribranchial


chamber, in the region of the anterior ceratobranchials

Diaphragmatopraecordialis

connective tissue near to the insertion of the fibers of the


m. interhyoideus posterior dorsal connective tissue of
the pericardium

Geniohyoideus

posterior, ventral surface of the infrarostral


hypobranchial plates

Levator arcuum branchialium I

lateral margin of the subocular bar ceratobranchial I

Levator arcuum branchialium II

larval otic process terminal commissure I

Levator arcuum branchialium III

lateral part of the otic capsule terminal commissure II

Levator arcuum branchialium IV

posterolateral part of the otic capsule medial margin of


the ceratobranchial IV

it has two clearly distinguishable


slips

Tympanopharyngeus

posterolateral surface of the otic capsule connective


tissue of the pericardium, anterior to the glottis

it is formed of fibers that diverge


from the medial portion of the m. l.
a. b. IV, and contact with those of
the opposite muscle, anteriorly to
the glottis

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process II terminal commissure I

it is disposed on the
ceratobranchial I

Constrictor branchialis III

branchial process II terminal commissure II

it is disposed on the
ceratobranchial II

Constrictor branchialis IV

branchial process III terminal commissure III

it is disposed on the
ceratobranchial III

Subarcualis rectus I

two slips: lateral base of the posterior process of the


ceratohyal proximal part of the ceratobranchial I (dorsal
slip), and branchial process III (ventral slip)

Subarcualis rectus II-IV

branchial process II medioventral part of the


ceratobranchial IV

Subarcualis obliquus

urobranchial process branchial processes II and III

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum branchial process II

Rectus abdominis

peritoneum pelvic griddle

ANATOMY OF ANURAN TADPOLES

Comments

it is completely covered by the m.


hyoangularis

this, and the remaining mm.


levatores branchialium are thin and
compact muscles

the slips diverge near the insertion


on the urobranchial process

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FIGURE 48. Scinax boulengeri, stage 35. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B) Buccal roof, (C)
Buccal floor. BFA buccal floor arena, BFAP buccal floor arena papilla, BP buccal pocket, C choana, DG dorsal gap, DV dorsal velum,
GZ glandular zone, IR infrarostrodont, LA labial arm, LK lower keratodonts, LRP lateral ridge papilla, MP marginal papilla, MR
median ridge, NV narial valve, P pustulation, PNA prenarial arena, PTNA postnarial arena, PTNP postnarial papilla, SR suprarostrodont, TA tongue anlage, UK upper keratodonts, VG ventral gap, VV ventral velum. Scale lines = 1 mm.

Oral apparatus and buccopharyngeal cavity (N = 2, stages 31 and 36. Figs. 48 and 49). The oral disc
width represents nearly 25% of the body length, and gape width reaches 18% of the body length. The oral disc
is lined by a simple papillar margin and submarginal papillae on the commissural region. The papillation
interrupts forming dorsal and ventral gaps. The rostrodonts are wide, thick and finely serrated. The serrations
have a wide base and an acute tip. The keratodonts are arranged in five rows, two upper (anterior) and three
lower (posterior), resulting in a LTRF 2(2)/3. The row P3 is shorter than the remaining rows, nearly 1/3 of the
A1, and it is disposed on a labial arm. The keratodonts are slightly curve, spike-like, and longer in the lowest row than in the others. In the buccal roof, the prenarial arena lack distinct features. The choanae are large,
arranged at an angle of 39 from the transversal line; there are no prenarial papillae, and the narial valve is visible. The postnarial arena shows a couple of short papillae. The lateral ridge papillae are tall, flat and have a
pustulate tip. The median ridge is low and wide, with irregular margin. The buccal roof arena is not defined

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and numerous pustules are distributed in the entire region. Secretory pits appear in a V-shape array, on the
posterior region of the buccal roof. The dorsal velum is thin, short and smooth. In the buccal floor, infralabial
and lingual papillae are absent. The buccal floor arena is small, delimited by five pairs of papillae and several
pustules among them. The most anterior pair includes wide, flat, multifid papillae, and the remaining papillae
are bifid. The buccal pockets are elongate and transversally oriented. The ventral velum is supported by spicules, and it is semicircular, with a small V-shaped median notch; marginal projections are absent and secretory pits appear on the posterior ventral surface of the velum.

FIGURE 49. Scinax boulengeri, stage 35. Oral apparatus and buccopharyngeal cavity. SEM micrographies (A) Detail of upper keratodonts, (B) Detail of suprarostrodont, (C) Detail of buccal floor arena papillae, (D) Detail of ventral velum. SP secretory pit.

Gut content (N = 3, stages 2736. Tables 21 and 22). The gut content was almost completely composed of
filamentous chlorophytes. They could be quantified in this case, because they appeared fragmented in the gut
contents in sizes that represent up to 30% of the tadpole body size.

Scinax nasicus. Fabrezi and Vera (1997) described the cartilaginous skeleton of this species. Lajmanovich
(1998) studied the qualitative composition of the diet. Ulloa Kreisel (2003) presented a description of the buccopharyngeal cavity. Later, Vera Candioti et al. (2004) studied the skeleton, mandibular and hyoid musculature, oral apparatus and buccopharyngeal cavity, digestive tract and gut contents. More recently, Alcalde
(2005) described cranial musculature. In the present study, morphology of a new set of larvae is described,
and the gut content reanalyzed.
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FIGURE 50. Scinax nasicus, stage 32. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B) Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral cartilage.
A ala, ALPC anterolateral process of ceratohyal, APC anterior process of ceratohyal, ARP articular process, ASP ascending process,
BB basibranchial, BH basihyal, C corpus, CB(I-IV) ceratobranchial, CF carotid foramen, CH ceratohyal, CPF craniopalatine foramen,
FF frontoparietal fenestra, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral cartilage, LOP larval otic process, LPC lateral
process of ceratohyal, MC Meckels cartilage, MP muscular process, NC notochordal canal, OC otic capsule, OPF optic foramen, PDP
processus dorsalis posterior, PF prootic foramen, PPC posterior process of ceratohyal, PR pars reuniens, QCC quadratocranial commissure, RP retroarticular process, S spicule, SB subocular bar, SC suprarostral cartilage, SF subocular fenestra, TC terminal commissure, TH trabecular horn, TS tectum synoticum, TTM taenia tecti marginalis, UP urobranchial process. Scale lines = 1 mm.

Chondrocranium and hyobranchial skeleton (N = 5, stages 32 and 35. Fig. 50). The chondrocranium of
these larvae represents 40% of the body length. The maximum width is at the plane of the otic capsules. The
suprarostral cartilage has a simple corpus with a concave dorsal notch, fused to the alae. The alae are still distinguishable and bear a processus dorsalis posterior. The trabecular horns correspond nearly to 18% of the

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total length of the chondrocranium and they show acuminate anterior margins. The cranial floor is completely
cartilaginous, and in the posterior margin, the notochordal canal extends 13% of the chondrocranium length.
The carotid and craniopalatine foramina are visible. The orbital cartilages are well-developed and the optic
foramen is visible and large. The chondrocranium is open dorsally, and the frontoparietal fenestra is lined by
the taeniae tecti marginales. The otic capsules are ovoid and occupy nearly 33% of the chondrocranium total
length; they are dorsally joined by the tectum synoticum. The palatoquadrate shows a wide articular process, a
tall, triangular muscular process, and a subocular bar slightly wider caudally. The palatoquadrate attaches to
the braincase via three points: the quadratocranial commissure, the ascending process, attached to the neurocranium above the oculomotor foramen, and the larval otic process. In the lower jaw, Meckels cartilages are Lshaped and bear three conspicuous processes: dorsomedial, ventromedial, and retroarticular. The infrarostral
cartilages are short, rectangular and independent. In the hyobranchial apparatus, the ceratohyals are long and
have a wide, triangular anterior process, a pointed anterolateral process, an acute lateral process, and a tall, triangular posterior process; the articular condyle is a rounded protuberance visible from a dorsal view. The ceratohyals are joined medially by the pars reuniens, which is slightly shorter than the basibranchial. The
basihyal is small and elliptical and the basibranchial bears a short urobranchial process (22% of the basibranchial length). The hypobranchial plates are triangular and medially articulated. The ceratobranchials are long,
thin, and with numerous lateral projections. They are distally joined by terminal commissures. Four cartilaginous spicules arise dorsally from each ceratobranchial, being the fourth highly reduced.
Musculature (N = 5, stages 32 and 35. Table 15 and Fig. 51). Thirty-two muscles appear in this species.
TABLE 15. Scinax nasicus, stages 32 and 35. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

two slips: ventromedial region of Meckels cartilage


lower lip of the oral disc (mandibulolabialis inferior), and
commissural region and part of the upper lip
(mandibulolabialis superior)

the lower slip is well-developed

Intermandibularis

medial region of the distal edge of Meckels cartilage


median aponeurosis

the whole structure is U-shaped,


sometimes joined to the m.
interhyoideus aponeurosis

Levator mandibulae longus


superficialis

external and posterior margin of the subocular bar and


ascending process of the palatoquadrate dorsomedial
region of Meckels cartilage

Levator mandibulae longus


profundus

external margin of the subocular bar and part of the


ascending process of the palatoquadrate external
margin of the ala of the suprarostral

the area of origin is smaller than


that of the m. l. m. l. superficialis,
and the insertion is via a long
tendon

Levator mandibulae internus

ventral surface of the ascending process and otic capsule


distal edge of Meckels cartilage

the insertion is via a long tendon

Levator mandibulae externus


superficialis

medial, inferior surface of the muscular process distal


edge of the ala of the suprarostral

it is scarcely developed; the


mandibular branch of the
trigeminal nerve (V3) runs dorsally
to this muscle

Levator mandibulae externus


profundus

medial, inferior surface of the muscular process


lateroventral margin of the ala of the suprarostral

the insertion is via a tendon shared


with the m. l. m. l. profundus

Levator mandibulae articularis

inferior part of the medial surface of the muscular


process dorsal surface of the lateral edge of Meckels
cartilage

Suspensoriohyoideus

posterior descending margin of the muscular process


posterior surface of the lateral process of the ceratohyal
...... continued

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TABLE 15 (continued)
Muscle

Insertions

Orbitohyoideus

anterior, dorsal margin of the muscular process lateral


edge of the ceratohyal

Suspensorioangularis

inferior, lateral surface of the descending margin of the


muscular process retroarticular process of Meckels
cartilage

the fibers occupy nearly the lower


third of the muscular process

Quadratoangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

it is completely covered by the m.


hyoangularis

Hyoangularis

dorsal surface of the ceratohyal, anterior to the articular


condyle retroarticular process of Meckels cartilage

Interhyoideus

ventral surface of the ceratohyal, near the lateral edge


median aponeurosis

Interhyoideus posterior

fibers loosely disposed, ventral to the peribranchial


chamber, in the region of the anterior ceratobranchials

Diaphragmatopraecordialis

connective tissue near to the insertion of the fibers of the


m. interhyoideus posterior dorsal connective tissue of
the pericardium

Geniohyoideus

posterior, ventral surface of the infrarostral


hypobranchial plates

Levator arcuum branchialium I

lateral margin of the subocular bar ceratobranchial I

Levator arcuum branchialium II

larval otic process terminal commissure I

Levator arcuum branchialium III

lateral part of the otic capsule terminal commissure II

Levator arcuum branchialium IV

posterolateral part of the otic capsule medial margin of


the ceratobranchial IV

it has two distinguishable slips

Tympanopharyngeus

posterolateral surface of the otic capsule connective


tissue anterior to the glottis

it is formed of fibers that diverge


from the medial slip of the m. l. a.
b. IV, and contact with those of the
opposite muscle, anteriorly to the
glottis

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process II terminal commissure I

it is disposed on the
ceratobranchial I

Constrictor branchialis III

branchial process II terminal commissure II

it is disposed on the
ceratobranchial II

Constrictor branchialis IV

branchial process III terminal commissure II

it is disposed on the
ceratobranchial III

Subarcualis rectus I

two slips: lateral base of the posterior process of the


ceratohyal proximal part of the ceratobranchial I
(dorsal slip), and branchial process III (ventral slip)

Subarcualis rectus II-IV

branchial process II medioventral part of the


ceratobranchial IV

Subarcualis obliquus

urobranchial process branchial process II, or II and III

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum branchial process II and medial part of


ceratobranchial IV

Rectus abdominis

peritoneum pelvic griddle

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FIGURE 51. Scinax nasicus, stage 32. Musculature (A) Dorsal view, superficial plane,
(B) Dorsal view, middle plane, (C) Dorsal view, deep plane, (D) Ventral view, (E) Lateral
view, superficial plane, (F) Lateral view, deep plane, (G) Ventral view, whole. CB(II-IV)
constrictor branchialis, DB diaphragmatobranchialis, GH geniohyoideus, HA
hyoangularis, IH interhyoideus, IM intermandibularis, LB(I-IV) levator arcuum
branchialium, LMA levator mandibulae articularis, LMEP levator mandibulae externus
profundus, LMES levator mandibulae externus superficialis, LMI levator mandibulae
internus, LMLP levator mandibulae longus profundus, LMLS levator mandibulae longus
superficialis, ML mandibulolabialis, OH orbitohyoideus, QA quadratoangularis, RA
rectus abdominis, RC rectus cervicis, SA suspensorioangularis, SH suspensoriohyoideus,
SO subarcualis obliquus, SRI subarcualis rectus I, SRII-IV subarcualis rectus II-IV, TP
tympanopharyngeus. Scale lines = 1 mm.

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FIGURE 52. Scinax nasicus, stage 32. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B) Buccal roof, (C)
Buccal floor. BFA buccal floor arena, BFAP buccal floor arena papilla, BP buccal pocket, C choana, DG dorsal gap, DV dorsal velum,
GZ glandular zone, ILP infralabial papilla, IR infrarostrodont, LK lower keratodonts, LRP lateral ridge papilla, MP marginal papilla,
MR median ridge, P pustulation, PMR premedian ridge, PNA prenarial arena, PTNA postnarial arena, PTNP postnarial papilla, S spur,
SMP submarginal papilla, SR suprarostrodont, TA tongue anlage, UK upper keratodonts, VV ventral velum. Scale lines = 1 mm.

Oral apparatus and buccopharyngeal cavity (N = 2, stages 31 and 32. Figs. 52 and 53). The oral disc
width represents nearly 18% of the body length, and gape width reaches 22% of the body length. The oral disc
is lined by a simple papillar margin interrupted in a dorsal gap; small submarginal papillae appear in the commissures. The rostrodonts are wide and thick, well-developed and keratinized. The keratodonts are arranged in
five rows, two upper (anterior) and three lower (posterior), resulting in a LTRF 2(2)/3(1). The row P3 is
slightly shorter than the other rows. The keratodonts have three regions, sheath, body and head. The head is
convex, slightly spatulate, and with an average of 12 cusps. In the buccal roof, the prenarial arena has some
pustules transversally aligned. The choanae are oriented at an angle of 43 from the transversal line. The postnarial arena has a couple of trifurcate papillae and central pustules. The lateral ridge papillae are well-developed, flat and bifid. The median ridge is trapezoid, with a pustulate free margin. Between the postnarial arena
and the median ridge, a small, quadrangular premedian ridge there appears. The buccal roof arena is not
defined and lacks any papillae. Several pustules distribute on the entire region. Conspicuous secretory pits
appear in a V-shaped array, on the posterior region of the buccal roof. The dorsal velum is short and medially
interrupted. In the buccal floor, posteriorly to the infrarostrodonts, there is a pair of keratinized spurs, anteromedially oriented. Posteriorly, there appear several pustules transversely arranged. The infralabial papillae are

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paired, bifid and non-overlapping. The tongue anlage is devoid of lingual papillae. The buccal floor arena is
delimited on both sides by four conical or bifid papillae and pustules among them. The buccal pockets are
elongate and transversally oriented. The ventral velum is supported by spicules, semicircular, thick, and lacks
marginal projections and median notch. A conspicuous secretory epithelium develops on the posterior ventral
surface of the velum.
Gut content (N = 10, stages 3136. Tables 21 and 22). Gut contents were mainly composed of filamentous
algae (not quantified) and crustaceans, followed by epiphytic diatoms. The more frequent item-sizes were
those between <17% of the tadpole body size.

FIGURE 53. Scinax nasicus, stage 32. Oral apparatus and buccopharyngeal cavity. SEM micrographies (A) Detail of oral disc, frontal
view, (B) Detail of suprarostrodont, (C) Detail of upper keratodonts, (D) Detail of spurs, (E) Detail of ventral velum. SP secretory pit,
SR suprarostrodont, UK upper keratodonts.

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LEIUPERIDAE
Physalaemus santafecinus. Perotti and Cspedez (1999) described the oral apparatus and buccopharyngeal
cavity of this species.

FIGURE 54. Physalaemus santafecinus, stage 33. Chondrocranium and hyobranchial skeleton, (A) Chondrocranium, dorsal view, (B)
Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral
cartilage. A ala, ALPC anterolateral process of ceratohyal, ALPO anterolateral process of the otic capsule, APC anterior process of
ceratohyal, ARP articular process, ASP ascending process, BB basibranchial, C corpus, CB(I-IV) ceratobranchial, CF carotid foramen,
CH ceratohyal, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral cartilage, LPC lateral process of ceratohyal, MC Meckels
cartilage, MP muscular process, NC notochordal canal, OC otic capsule, PDA processus dorsalis anterior, PDP processus dorsalis posterior, PPC posterior process of ceratohyal, PR pars reuniens, QCC quadratocranial commissure, QOC quadratoorbital commissure,
QP quadratoethmoid process, RP retroarticular process, S spicule, SB subocular bar, SC suprarostral cartilage, SF subocular fenestra,
TC terminal commissure, TH trabecular horn, UP urobranchial process. Scale lines = 1 mm.

Chondrocranium and hyobranchial skeleton (N = 5, stages 32 and 33. Fig. 54). The chondrocranium of
these larvae represents 50% of the body length. The maximum width is at the plane of the posterior part of the
subocular bar. The suprarostral cartilage has a single, V-shaped corpus, which is dorsally fused to the alae.
These are well-defined, ventrally rounded, and bear well-developed dorsalis anterior and posterior processes.
The trabecular horns correspond approximately to 25% of the total length of the chondrocranium and diverge

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from the ethmoid plate. They are narrow and uniformly wide. The cranial floor is completely cartilaginous,
with thin cartilage in the central area. The carotid foramen is visible, whereas the craniopalatine is not identifiable because of the light chondrification of the intertrabecular plate. In the posterior margin of the cranial
floor, the notochordal canal extends 21% of the chondrocranium length. The orbital cartilages and the taeniae
tecti marginales are not developed in the stages analyzed. The otic capsules are ovoid, occupy nearly 26% of
the chondrocranium total length, and bear a small anterolateral process. The tectum synoticum is not developed. The palatoquadrate has a short and wide articular process, a tall, thin and triangular muscular process,
and a smooth subocular bar, slightly wider caudally. In some specimens there is a small non-chondrified portion in the posterior part of the bar. The palatoquadrate attaches to the braincase via three points: the quadratocranial commissure, with a long quadratoethmoid process, the quadratoorbital commissure, and the
ascending process, attached to the floor of the cranial cavity. In the lower jaw, Meckels cartilages are Lshaped, with three processes: dorsomedial, ventromedial, and retroarticular. The infrarostral cartilages are
short, rectangular and independent. In the hyobranchial skeleton, the ceratohyals are long and have a tall, triangular anterior process, a thin, pointed, medially directed anterolateral process, an acute lateral process, and
a wide, tall posterior process; the articular condyle is a quadrangular, robust protuberance visible on the dorsal
surface. The ceratohyals are joined medially by the pars reuniens. The basihyal is absent and the basibranchial
is short and bears a small urobranchial process (24% of the basibranchial length). The hypobranchial plates
are flat and subquadrangular, and they articulate medially leaving an ovoid posterior gap. The ceratobranchials are long, thin, and have numerous lateral projections. They are distally joined by terminal commissures.
Four cartilaginous spicules arise dorsally from each ceratobranchial, the fourth one being reduced.
Musculature (N = 5, stages 32 and 33. Table 16 and Fig. 55). Thirty-three muscles appear in this species.
TABLE 16. Physalaemus santafecinus, stages 32 and 33. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

ventromedial region of Meckels cartilage lower lip of


the oral disc

it consists of a single slip,


corresponding to m.
mandibulolabialis inferior

Intermandibularis

medial region of Meckels cartilage median


aponeurosis

Levator mandibulae longus


superficialis

external and posterior margin of the subocular bar, and


part of the ascending process dorsomedial region of
Meckels cartilage

Levator mandibulae longus


profundus

ascending process of the palatoquadrate ventral margin


of the ala of the suprarostral

Levator mandibulae internus

ventral surface of the ascending process, and medial part


of the ventral surface of the otic capsule distal edge of
Meckels cartilage

Levator mandibulae externus


superficialis

medial, inferior surface of the muscular process ventral


margin of the ala of the suprarostral

Levator mandibulae externus


profundus

medial, inferior surface of the muscular process dorsal,


lateral edge of the suprarostral

Levator mandibulae articularis

inferior part of the medial surface of the muscular


process dorsal surface of the lateral edge of Meckels
cartilage

Levator mandibulae lateralis

articular process of the palatoquadrate dorsal, lateral


edge of the suprarostral

Suspensoriohyoideus

posterior descending margin of the muscular process, and


part of the subocular bar posterior surface of the lateral
process of the ceratohyal

the mandibular branch of the


trigeminal nerve (V3) runs
ventrally to this muscle

it is a short muscle, formed of a


few fibers

...... continued

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TABLE 16 (continued)
Muscle

Insertions

Orbitohyoideus

anterior, dorsal margin of the muscular process lateral


edge of the ceratohyal

Suspensorioangularis

inferior, lateral part of the descending margin of the


muscular process retroarticular process of Meckels
cartilage

fibers occupy approximately the


lower half of the muscular process

Quadratoangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

it is completely covered by the


mm. suspensorioangularis and
hyoangularis

Hyoangularis

dorsal surface of the ceratohyal, anterior to the articular


condyle retroarticular process of Meckels cartilage

Interhyoideus

ventral surface of the ceratohyal, near the lateral edge


median aponeurosis

Interhyoideus posterior

fibers loosely disposed, ventral to the peribranchial


chamber, in the region of the anterior ceratobranchials

Diaphragmatopraecordialis

connective tissue near to the insertion of the fibers of the


m. interhyoideus posterior connective tissue dorsal to
the pericardium

Geniohyoideus

posterior, ventral surface of the infrarostral


hypobranchial plates

Levator arcuum branchialium I

lateral margin of the subocular bar ceratobranchial I

Levator arcuum branchialium II

subocular bar terminal commissure I

Levator arcuum branchialium III

lateral part of the otic capsule terminal commissure II

Levator arcuum branchialium IV

posterolateral part of the otic capsule ceratobranchial


IV

it is clearly divided into two slips,


with similar points of origin and
insertion

Tympanopharyngeus

posterolateral surface of the otic capsule insertion dorsal


on the connective tissue of the pericardium

in the origin, fibers diverge


distally from the m. dilatator
laryngis

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process II terminal commissure I

Constrictor branchialis III

branchial process II terminal commissure II

Constrictor branchialis IV

proximal part of the ceratobranchial III terminal


commissure III

Subarcualis rectus I

three slips: lateral base of the posterior process of the


ceratohyal proximal part of the ceratobranchial I
(dorsal slip), branchial process II (ventral1 slip), and
branchial process II, medially regarding the ventral1 slip
(ventral2 slip)

Subarcualis rectus II-IV

branchial process II proximal, ventral part of the


ceratobranchial IV

Subarcualis obliquus

urobranchial process branchial process II

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis

peritoneum branchial process III and medial part of the


ceratobranchial IV

Rectus abdominis

peritoneum pelvic griddle

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Comments

it is formed of parallel, transverse


fibers

it is the widest of the mm. l. a.


branchialium; its insertion onto the
ceratobranchial occupies a large
surface

it originates almost at the level of


half the abdomen

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FIGURE 55. Physalaemus santafecinus, stage 33. Musculature (A) Dorsal view,
superficial plane, (B) Dorsal view, middle plane, (C) Dorsal view, deep plane, (D)
Ventral view, (E) Lateral view, superficial plane, (F) Lateral view, deep plane, (G)
Ventral view, whole. CB(II-IV) constrictor branchialis, DB diaphragmatobranchialis,
GH geniohyoideus, HA hyoangularis, IH interhyoideus, IM intermandibularis, LB(IIV) levator arcuum branchialium, LMA levator mandibulae articularis, LMEP levator
mandibulae externus profundus, LMES levator mandibulae externus superficialis, LMI
levator mandibulae internus, LML levator mandibulae lateralis, LMLP levator
mandibulae longus profundus, LMLS levator mandibulae longus superficialis, ML
mandibulolabialis, OH orbitohyoideus, QA quadratoangularis, RA rectus abdominis,
RC rectus cervicis, SA suspensorioangularis, SH suspensoriohyoideus, SO subarcualis
obliquus, SRI subarcualis rectus I; SRII-IV subarcualis rectus II-IV, TP
tympanopharyngeus. Scale lines = 1 mm.

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FIGURE 56. Physalaemus santafecinus, stage 33. Oral apparatus and buccopharyngeal cavity (A) Oral disc, frontal view, (B) Buccal
roof, (C) Buccal floor. BFA buccal floor arena, BFAP buccal floor arena papilla, BP buccal pocket, BRA buccal roof arena, BRAP
buccal roof arena papilla, C choana, DG dorsal gap, DV dorsal velum, GZ glandular zone, ILP infralabial papilla, IR infrarostrodont,
LK lower keratodonts, LP lingual papilla, LRP lateral ridge papilla, MP marginal papilla, MR median ridge, NV narial valve, P pustulation, PNA prenarial arena, PTNA postnarial arena, PTNP postnarial papilla, SR suprarostrodont, TA tongue anlage, UK upper keratodonts, VV ventral velum. Scale lines = 1 mm.

Oral apparatus and buccopharyngeal cavity (N = 2, stages 32 and 33. Figs. 56 and 57). The oral disc
width represents 22% of the body length, and gape width reaches 19% of the body length. The lateral margins
have deep indentations in the commissural region. The papillar margin is simple and interrupts in a wide dorsal gap that occupies nearly the entire upper lip. Papillae are conical with smooth, rounded tips. The rostrodonts are well-developed and keratinized, thick, and finely serrated. The serrations of the suprarostral are
slightly shorter than those of the infrarostral. The keratodonts are arranged in four rows, two upper (anterior)
and two lower (posterior), resulting in a LTRF 2(2)/2(1). The first three rows have approximately the same
length, whereas P2 is slightly shorter. The keratodonts are long, with three distinctive regions, sheath, body
and head. The head is slightly convex, oblong and with 46 cusps. In the buccal roof, the prenarial arena
shows a bilobate ridge and groups of pustules. The choanae are large, elongate and obliquely oriented at an
angle of about 28 from the transversal line. The anterior margin has small prenarial papillae, and the narial
valve is thick and well-developed. The postnarial arena shows two pairs of flat, tall papillae, the medial pair
larger that one lateral one. The lateral ridge papillae are tall, wide, flat and trifurcate. The median ridge is trapezoid, with a pustulate free margin and small pustules on its ventral surface. The buccal roof arena is delimited
on both sides by 56 tall, conical marginal papillae. Numerous pustules scatter among the papillae. Large
secretory pits appear in a V-shaped array, on the posterior region of the buccal roof. The dorsal velum is short,
smooth, and medially interrupted. In the buccal floor, posterior to the infrarostrodonts, there are 68 pustules

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transversely aligned. Posteriorly, two pairs of infralabial papillae appear: the anterior pair, on the Meckels
cartilage, is hand-like and large, and the medial pair includes smaller, trifurcate papillae. On the tongue
anlage, there is a single conical lingual papilla. The buccal floor arena is delimited by 15 papillae, four paired
and seven odd; two pairs are bifid and the remaining, conical, with different heights. Numerous pustules are
scattered among the papillae. The buccal pockets are deep and transversally disposed. The ventral velum is
long and supported by spicules; it has three pronounced marginal projections on the filer plates, and it lacks a
median notch. Secretory pits appear on the posterior ventral surface of the velum.
Gut content (N = 10, stages 3235. Tables 21 and 22). The gut content was mainly composed of insects
remnants and desmids, and the more frequent prey sizes were those between <19% of the tadpole body size.

FIGURE 57. Physalaemus santafecinus, stage 33. Oral apparatus and buccopharyngeal cavity. SEM micrographies (A) Lower margin
of oral disc, frontal view, (B) Detail of lower keratodonts, (C) Detail of the infrarostrodont, (D) Buccal roof, detail of choanae region,
(E) Detail of dorsal velum. BRA buccal roof arena, C choana, LK lower keratodonts, LRP lateral ridge papilla, MP marginal papilla,
MR median ridge, NV narial valve, SP secretory pit.

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MICROHYLIDAE
Chiasmocleis panamensis. External and internal morphology of this species were described in Vera Candioti
(2006b); the name postnarial papilla is replaced with the most accurate name narial wall papilla, and the
lateral ridge papillae are considered absent, according to Wassersug (1980) and Chou and Lin (1997).

FIGURE 58. Chiasmocleis panamensis, stage 35. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B)
Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view. ALPC anterolateral process of ceratohyal, APC anterior process of ceratohyal, ARP articular process, ASP ascending process, BB basibranchial, BH basihyal,
CB(I-IV) ceratobranchial, CF carotid foramen, CH ceratohyal, CPF craniopalatine foramen, FF frontoparietal fenestra, FO fenestra
ovalis, HP hypobranchial plate, IC infrarostral cartilage, LOP larval otic process, LPC lateral process of ceratohyal, MC Meckels cartilage, MP muscular process, NC notochordal canal, OC otic capsule, PLP processus lateralis posterior, PPC posterior process of ceratohyal, PR pars reuniens, PS processus suboticus, QCC quadratocranial commissure, QP quadratoethmoid process, SB subocular bar,
SC suprarostral cartilage, SF subocular fenestra, TC terminal commissure, TH trabecular horn, TS tectum synoticum, TTM taenia tecti
marginalis, UP urobranchial process, VP ventrolateral process. Scale line = 1 mm.

Chondrocranium and hyobranchial skeleton (N = 5, stages 35 and 36. Fig. 58). The chondrocranium of
these larvae represents 58% of the body length. The maximum width is at the plane of the processus lateralis
posterior of the palatoquadrate. The suprarostral cartilage has corpus and alae fused in a single structure with
a curved anterior margin and a posterior margin bearing a medial projection. The suprarostral is fused to the
anterior margin of trabecular horns, and only the lateral part of the horns remains free. The trabecular horns
correspond approximately to 22% of the total length of the chondrocranium and are flat and distally wider.
Posteriorly, on the trabecular plate, the olfactory foramina are clearly distinguishable. The cranial floor is
completely cartilaginous, with thin cartilage in the central area. The carotid and craniopalatine foramina are

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visible, the latter elongate and larger than the former. In the posterior margin of the cranial floor, the notochordal canal extends 20% of the chondrocranium length. In the lateral walls of the chondrocranium, the
orbital cartilages are formed only marginally, and the central region is occupied by a large foramen that joins
the optic, oculomotor, trochlear and prootic foramina. The chondrocranium is open dorsally, and the frontoparietal fenestra is bordered by the taeniae tecti marginales. The otic capsules are quadrangular and occupy
nearly 31% of the chondrocranium total length. The fenestra ovalis (37% of the capsule length) is located ventrolaterally on each otic capsule. The otic capsules are dorsally joined by the tectum synoticum. In the palatoquadrate, the articular process is short and wide. The muscular process is scarcely developed and bears a small
ventrolateral process in its ventral surface. The subocular bar shows a uniform width, and in the most posterior part presents a long, rectangular, flat, posterolaterally directed processus lateralis posterior. In the ventral
surface of this process, the subotic process is present, as a chondrified, subcylindrical, bifurcated structure.
The palatoquadrate attaches to the braincase via three points: the quadratocranial commissure, bearing a small
quadratoethmoid process, the ascending process, attached to the cranial floor, and the larval otic process. The
lower jaw includes the Meckels and infrarostral cartilages. Meckels cartilages are bar-like, with dorsal and
retroarticular process conspicuous. The infrarostral cartilages are fused forming a ring-like structure with a
laminar projection arising from the medial, posterior margin. In the hyobranchial skeleton, the ceratohyals are
elongate and have a small, rounded anterior process, a tall, pointed anterolateral process, and a thin, triangular
posterior process, partially concealed by the ceratobranchial I; the lateral edge of the ceratohyal shows a wide
laminar projection posteriorly directed; the articular condyle outlines in the posterodorsal margin of the ceratohyal. The basihyal is a very thin, cartilaginous bar. The pars reuniens is continuous with the ceratohyals and
the basibranchial. The basibranchial is small, and bears a thin and long urobranchial process (1.7 times longer
than the basibranchial). The basibranchial is posteriorly fused to the hypobranchial plates, which are in turn
fused to each other. The ceratobranchials are fused to the hypobranchial plates and constitute a large, complexly reticulated branchial basket. Between the ceratobranchials II and III there is a closed branchial process.
Dorsally, three large spicules are differentiated, and the most lateral, wider than the others, apparently represents the complete fusion of spicules I and II.
Musculature (N = 5, stages 35 and 36. Table 17 and Fig. 59). Thirty muscles appear in this species.
TABLE 17. Chiasmocleis panamensis, stages 35 and 36. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

ventromedial region of Meckels cartilage


ventrolateral surface of the infrarostral

it is a cylindrical and compact muscle

Intermandibularis

anterior surface of Meckels cartilage median


aponeurosis

the whole muscle has the shape of an inverted


triangle, and it attaches to a median
aponeurosis common to the m. interhyoideus,
adopting the complete structure a distinctive
X-shape

Levator mandibulae longus


superficialis

posterior margin of the muscular process


posterior surface of Meckels cartilage

it is well-developed

Levator mandibulae longus


profundus

anterior, dorsal surface of the muscular process


lateral edge of the suprarostral

it is well-developed

Levator mandibulae internus

dorsal surface of the subocular bar, near the


medial margin lateral edge of Meckels
cartilage

the insertion is via a long tendon

Levator mandibulae externus

articular process of the palatoquadrate lateral


edge of the suprarostral

the insertion is through a common tendon


with the m. l. m. l. profundus; the mandibular
branch of the trigeminal nerve (V3) runs
ventrally to this muscle; there is no division
into mm. l. m. e. superficialis and profundus
...... continued

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TABLE 17 (continued)
Muscle

Insertions

Comments

Levator mandibulae articularis

dorsal surface of the muscular process lateral


edge of Meckels cartilage

it is a very short muscle

Suspensoriohyoideus

posterior part of the ventral surface of the


processus lateralis posterior dorsal surface of
the lateral process of the ceratohyal

it is formed of a few fibers, loosely disposed

Orbitohyoideus

anterior, dorsal margin of the muscular process


lateral edge of the ceratohyal

it is scarcely developed

Suspensorioangularis

ventral surface of the palatoquadrate


retroarticular process of Meckels cartilage

it is located laterally to the m.


quadratoangularis, and it is almost
indistinguishable from it

Quadratoangularis

ventral surface of the palatoquadrate


retroarticular process of Meckels cartilage

Hyoangularis

dorsal surface of the ceratohyal retroarticular


process of Meckels cartilage

it is scarcely developed

Interhyoideus

ventral surface of the lateral process of the


ceratohyal median aponeurosis

it is formed of parallel, fibers, transversally


and obliquely disposed

Interhyoideus posterior

it forms a continuous and extensive layer,


ventral to the peribranchial chamber

Geniohyoideus

posterior, ventral surface of the infrarostral


diffuse, near the thyroid gland

Levator arcuum branchialium I

ventral surface of the processus lateralis


posterior, near its lateral margin lateral surface
of the ceratobranchial I

Levator arcuum branchialium II

ventral surface of the otic capsule and ventral


surface of the processus lateralis posterior, near
its lateral margin ceratobranchials I and II

Levator arcuum branchialium


III

two slips: anterior and anterolateral points on


the ventral surface of the processus lateralis
posterior terminal commissure II and III

Levator arcuum branchialium


IV

ventral surface of the otic capsule medial


margin of the ceratobranchial IV

Dilatator laryngis

posterolateral surface of the otic capsule


arytenoid cartilage

Constrictor branchialis II

branchial process terminal commissure I

Constrictor branchialis III

branchial process terminal commissure II

Constrictor branchialis IV

branchial process terminal commissure III

Subarcualis rectus I

three slips: lateral base of the posterior process


of the ceratohyal spicule I (dorsal slip),
ceratobranchial I (ventral1 slip), and branchial
process (ventral2 slip)

Subarcualis rectus II-IV

ventromedial surface of the ceratobranchial IV


branchial process

Subarcualis rectus II-IV


lateralis

distal part of the ceratobranchial IV branchial


process

Subarcualis obliquus

urobranchial process branchial process

Diaphragmatobranchialis

peritoneum ceratobranchial III

Rectus cervicis

peritoneum branchial process

Rectus abdominis

the ventral2 slip is very long and thin, and


originates laterally to the base of the posterior
process, on a small process of the posterior
margin of the ceratohyal; the insertion of the
ventral1 slip on the ceratobranchial I is medial
regarding that of the dorsal slip

peritoneum, approximately at half the abdomen


level pelvic griddle

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FIGURE 59. Chiasmocleis panamensis, stage 35. Musculature, (A) Dorsal view, superficial
plane, (B) Dorsal view, middle plane, (C) Dorsal view, deep plane, (D) Ventral view, (E)
Lateral view, superficial plane, (F) Detail of the insertions of mm. levatores arcuum
branchialium, lateral view, (G) Ventral view, whole. CB(II-IV) constrictor branchialis, DB
diaphragmatobranchialis, HA hyoangularis, IH interhyoideus, IM intermandibularis, LB(IIV) levator arcuum branchialium, LMA levator mandibulae articularis, LME levator
mandibulae externus, LMI levator mandibulae internus, LMLP levator mandibulae longus
profundus, LMLS levator mandibulae longus superficialis, ML mandibulolabialis, OH
orbitohyoideus, QA+SA quadratoangularis + suspensorioangularis, RA rectus abdominis,
RC rectus cervicis, SH suspensoriohyoideus, SO subarcualis obliquus, SRI subarcualis
rectus I, SRII-IV subarcualis rectus II-IV, SRII-IVLAT subarcualis rectus II-IV lateralis.
Scale lines = 1 mm.

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FIGURE 60. Chiasmocleis panamensis, stage 36. Oral apparatus and buccopharyngeal cavity (A) Mouth, frontal view, (B) Buccal
roof, (C) Buccal floor. BFA buccal floor arena, BFAP buccal floor arena papilla, BP buccal pocket, C choana, DV dorsal velum, G
glottis, GZ glandular zone, MR median ridge, NLP narial lateral papillae, NWP narial wall papillae, P pustulation, PNA prenarial
arena, PNAP prenarial arena papilla, PPP prepocket papilla, TA tongue anlage, VV ventral velum. Scale lines = 1 mm.

Oral apparatus and buccopharyngeal cavity (N = 2, stage 36. Figs. 60 and 61). The mouth is terminal
with a wide oral slit devoid of papillae and keratinized structures. Gape width reaches 28% of the body length.
Two upper labial flaps hang covering the spatulate lower lip. The buccal roof is not pigmented. The prenarial
arena shows a single bifid papilla. The choanae are large, subcircular and unperforated. From the posterior
margin of each choana, a large, flat and multifid narial wall papilla arises. A bifid papilla projects medially
from the choana lateral margin, accompanied by scarce smaller papillae. The median ridge is three times
higher than wide, triangular, and with a pustulate margin. Lateral ridge papillae are absent. Posteriorly to the
median ridge, the buccal roof arena is poorly defined; some pustules and short papillae distribute on the central and lateral regions. Secretory pits appear in a broad array on the posterior region of the buccal roof. The
dorsal velum is comparatively long and smooth, without projections. In the buccal floor, the posterior surface
of Meckels cartilage has small pustules. The tongue anlage is small and devoid of lingual papillae. The buccal pockets are well-developed and have two prepocket papillae projecting from the anterior margin. The glottis is far anteriorly placed, on the posterior margin of the buccal floor arena. On both sides, tall, conical
papillae are arranged, approximately following a wide V-shape. Among them, small pustules are scattered.
The ventral velum is very long and posteriorly expanded; the margin has wide undulations and a small median
notch.

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FIGURE 61. Chiasmocleis panamensis, stage 35. Oral apparatus and buccopharyngeal cavity. SEM micrographies (A) Lower lip,
posterolateral view, (B) Buccal roof, detail of choanae region, (C) Buccal floor, detail of glottis region. BFAP buccal floor arena
papilla, C choana, G glottis, LL lower lip, MC Meckels cartilage, MR median ridge, NWP narial wall papillae, TA tongue anlage, VV
ventral velum.

Gut content (N = 7, stages 3436). In this species digestive tract, as in the other two microhylids examined, distinctive strings appear, coming from each side of the branchial basket, and then entering into the
oesophagus forming a conspicuous double-helix (Fig. 65). The digestive contents of the specimens analyzed
appear full of a very fine material impossible to quantify. The specimens come from the same pond but from
different collection dates, so it seems improbable that the tadpoles had not been feeding on both cases. It could
be suggested that this species diet include very small items to be detected with a different methodology. For
this reason, this species could not be included in the correspondence analysis of the gut contents, nor in the
canonical correspondence analysis later applied to morphological and food variables.
Dermatonotus muelleri. Previous literature for this species includes papers by Lavilla (1992b), Echeverra and
Lavilla (2000), and Ulloa Kreisel (2003). A revision on internal morphology appeared in Vera Candioti
(2006b).
Chondrocranium and hyobranchial skeleton (N = 5, stages 3436. Fig. 62). The chondrocranium of these
larvae represents 43% of the body length. The maximum width is at the level of the processus lateralis posterior of the palatoquadrate. The suprarostral cartilage has corpus and alae fused in a single structure with a
curved anterior margin and a posterior margin bearing a medial, triangular projection. The suprarostral is
fused to the anterior margin of trabecular horns, and only the lateral part remains free. The trabecular horns
correspond approximately to 21% of the total length of the chondrocranium and are flat and distally wider.

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FIGURE 62. Dermatonotus muelleri, stage 34. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B)
Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view. ALPC anterolateral process of ceratohyal, APC anterior process of ceratohyal, ARP articular process, ASP ascending process, BB basibranchial, BH basihyal,
CB (I-IV) ceratobranchial, CF carotid foramen, CH ceratohyal, CP crista parotica, CPF craniopalatine foramen, FF frontoparietal
fenestra, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral cartilage, LOP larval otic process, LPC lateral process of ceratohyal, MC Meckels cartilage, MP muscular process, NC notochordal canal, OC otic capsule, PLP processus lateralis posterior, PPC
posterior process of ceratohyal, PR pars reuniens, PS processus suboticus, QCC quadratocranial commissure, SB subocular bar, SC
suprarostral cartilage, SF subocular fenestra, TH trabecular horn, TS tectum synoticum, TTM taenia tecti marginalis, UP urobranchial
process. Scale line = 1 mm.

The cranial floor is lightly chondrified in the central area. The carotid and craniopalatine foramina are visible,
the latter elongate and larger than the former. In the posterior margin of the cranial floor, the notochordal canal
extends 15% of the chondrocranium length. In the lateral walls of the chondrocranium, the orbital cartilages
are formed only marginally, and the central region is occupied by a large foramen that joins the optic, oculomotor, trochlear and prootic foramina. The chondrocranium is open dorsally through the frontoparietal fenes-

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tra lined by the taeniae tecti marginales. The otic capsules are quadrangular and occupy nearly 27% of the
chondrocranium total length. The crista parotica appears as a scarcely chondrified, lateral and posteriorly
expanded plate that curves ventrally and overlaps to the lateral part of the branchial basket. The fenestra ovalis
(35% of the capsule length) is located ventrolaterally on each otic capsule. The otic capsules are dorsally
joined by the tectum synoticum. In the palatoquadrate, the articular process is short and wide, with three small
anterior processes. The muscular process is scarcely developed. The subocular bar shows a uniform width,
and in the most posterior part presents a long, rectangular, flat, and posterolaterally oriented processus lateralis posterior. In the ventral surface of this process, the subotic process is present. The palatoquadrate attaches
to the braincase via three points: the quadratocranial commissure, bearing a small quadratoethmoid process,
the ascending process, attached to the cranial floor, and the larval otic process, long and extended between the
posterior third of the processus lateralis posterior and the anterior part of the crista parotica. The lower jaw
includes the Meckels and the infrarostral cartilages. Meckels cartilages are bar-like, with dorsal and retroarticular processes. The infrarostral cartilages are fused forming a ring-like structure with a laminar projection
arising from the medial, posterior margin. In the hyobranchial skeleton, the ceratohyals are elongate and have
a low, rounded anterior process, a tall, thin, pointed and medially directed anterolateral process, and a tall, thin
posterior process, partially concealed by the ceratobranchial I; the lateral edge of the ceratohyal has a wide
laminar projection posteriorly directed; the articular condyle is outlined in the posterodorsal margin of the ceratohyal. The basihyal is a very thin, cartilaginous bar. The pars reuniens is continuous with the ceratohyals
and the basibranchial. The basibranchial is small and bears a thin and long urobranchial process (1.4 times
longer than the basibranchial). The basibranchial is posteriorly fused to the hypobranchial plates, which are in
turn fused to each other. The ceratobranchials are fused to the hypobranchial plates and form a voluminous
branchial basket. Between the ceratobranchials II and III there is a closed branchial process. Dorsally, three
large spicules are differentiated, and the most lateral, wider than the others, apparently represents the complete
fusion of spicules I and II.
Musculature (N = 5, stages 3436. Table 18 and Fig. 63). Twenty-nine muscles are present in this species.
TABLE 18. Dermatonotus muelleri, stages 3436. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

ventromedial region of Meckels cartilage ventrolateral


surface of the infrarostral

it is a cylindrical and compact


muscle

Intermandibularis

anterior surface of Meckels cartilage median


aponeurosis

the whole muscle has the shape of


an inverted triangle, and it attaches
to a median aponeurosis common
to the m. interhyoideus, adopting
the complete structure, a
distinctive X-shape

Levator mandibulae longus

anterior part of the dorsal surface, and posterior margin of


the muscular process dorsal surface of Meckels
cartilage

it is a compact and developed


muscle, without division into mm.
l. m. l. superficialis and profundus

Levator mandibulae internus

dorsal surface of the subocular bar, near the medial


margin lateral edge of Meckels cartilage

the insertion is via a long tendon

Levator mandibulae externus

articular process of the palatoquadrate lateral edge of


the suprarostral

the mandibular branch of the


trigeminal nerve (V3) runs
ventrally to this muscle; there is no
division into mm. l. m. e.
superficialis and profundus

Levator mandibulae articularis

dorsal surface of the muscular process lateral edge of


Meckels cartilage
...... continued

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TABLE 18 (continued)
Muscle

Insertions

Comments

Suspensoriohyoideus

posterior part of the ventral surface of the processus


lateralis posterior dorsal surface of the lateral process of
the ceratohyal

it is formed of a few fibers, loosely


disposed

Orbitohyoideus

anterior, dorsal margin of the muscular process lateral


edge of the ceratohyal

it is scarcely developed

Suspensorioangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

it is located laterally to the m.


quadratoangularis, and it is almost
indistinguishable from it

Quadratoangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

Hyoangularis

dorsal surface of the ceratohyal retroarticular process of


Meckels cartilage

it is scarcely developed

Interhyoideus

ventral surface of the lateral process of the ceratohyal


median aponeurosis

it is formed of parallel, fibers,


transversally and obliquely
disposed

Interhyoideus posterior

it forms a continuous and extensive layer, ventral to the


peribranchial chamber

Geniohyoideus

posterior, ventral surface of the infrarostral diffuse, near


thyroid gland

Levator arcuum branchialium I

ventral surface of the processus lateralis posterior, near its


lateral margin lateral surface of the ceratobranchial I

Levator arcuum branchialium II

lateroventral surface of the otic capsule ceratobranchials


I and II

Levator arcuum branchialium


III

two slips: anterior and anterolateral points on the ventral


surface of the processus lateralis posterior terminal
commissure II and III

Levator arcuum branchialium


IV

ventral surface of the otic capsule medial margin of the


ceratobranchial IV

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process terminal commissure I

Constrictor branchialis III

branchial process terminal commissure II

Constrictor branchialis IV

branchial process terminal commissure III

Subarcualis rectus I

two slips: lateral base of the posterior process of the


ceratohyal spicule I (dorsal slip), and ceratobranchial I
(ventral slip)

Subarcualis rectus II-IV

ventromedial surface of the ceratobranchial IV


branchial process

Subarcualis rectus II-IV


lateralis

distal part of the ceratobranchial IV branchial process

Subarcualis obliquus

urobranchial process branchial process

Diaphragmatobranchialis

peritoneum ceratobranchial III

Rectus cervicis

peritoneum branchial process

Rectus abdominis

peritoneum, approximately at half the abdomen level


pelvic griddle

110 Zootaxa 1600 2007 Magnolia Press

it is very thin, formed of a few


fibers

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FIGURE 63. Dermatonotus muelleri, stage 35. Musculature (A) Dorsal view,
superficial plane, (B) Dorsal view, deep plane, (C) Ventral view, (D) Lateral view,
superficial plane, (E) Detail of the insertions of mm. levatores arcuum branchialium,
lateral view, (F) Ventral view, whole. CB(II-IV) constrictor branchialis, DB
diaphragmatobranchialis, HA hyoangularis, IH interhyoideus, IM intermandibularis,
LB (I-IV) levator arcuum branchialium, LMA levator mandibulae articularis, LME
levator mandibulae externus, LMI levator mandibulae internus, LMLO levator
mandibulae longus, OH orbitohyoideus, RA rectus abdominis, SH
suspensoriohyoideus, SO subarcualis obliquus, SRI subarcualis rectus I, SRII-IV
subarcualis rectus II-IV, SRII-IVLAT subarcualis rectus II-IV lateralis. Scale lines =
1 mm.

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FIGURE 64. Dermatonotus muelleri, stage 35. Oral apparatus and buccopharyngeal cavity (A) Mouth, frontal view, (B) Buccal roof,
(C) Buccal floor. BFA buccal floor arena, BFAP buccal floor arena papilla, BP buccal pocket, C choana, DV dorsal velum, G glottis,
GZ glandular zone, MR median ridge, NLP narial lateral papillae, NWP narial wall papillae, P pustulation, PNA prenarial arena,
PNAP prenarial arena papilla, PPP prepocket papilla, TA tongue anlage, VV ventral velum. Scale lines = 1 mm.

Oral apparatus and buccopharyngeal cavity (N = 2, stages 34 and 35. Fig. 64). The mouth is terminal
with a wide oral slit devoid of papillae and keratinized structures. Gape width reaches 26% of the body length.
Two upper labial flaps hang covering the spatulate lower lip. In the buccal roof, the prenarial arena shows a
single small papilla and some pustules. The choanae are large, subcircular and unperforated. From the posterior margin of each choana, a large, flat and multifid narial wall papilla arises. Four tall, conical papillae
project medially from the choana lateral margin, accompanied by scarce smaller papillae and pustules. The
median ridge is nearly four times higher than wide, triangular, and with pustulate margin. Lateral ridge papillae are absent. The buccal roof arena is not defined, and numerous pustules distribute on the central zone and
posterior edge of the roof. Secretory pits appear in a broad array on the posterior margin of the buccal roof.
The dorsal velum is comparatively long and smooth. In the buccal floor, the posterior surface of Meckels cartilage shows 23 small pustules. The tongue anlage is small and devoid of lingual papillae. The buccal pockets are well-developed and have one bifid prepocket papilla projecting from the anterior margin, accompanied
by small pustules. The glottis is far anteriorly placed, on the posterior margin of the buccal floor arena. On
both sides, 911 tall, conical papillae are arranged approximately following a wide V-shape. Among them,
small pustules are scattered. The ventral velum is well-developed and posteriorly expanded; it has three marginal projections on the filter plates, and a small median notch.

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Gut content (N = 7, stages 3436. Tables 21 and 22). The digestive content was almost completely composed of small Volvocales (99.23%) with sizes below 1% of the tadpole body length. Figure 65 shows the distinctive food-strings obtained from the oesophagus and the most anterior part of the intestine.

FIGURE 65. Dermatonotus muelleri, stage 35. Mucus and food cords from the first portion of the gut. Scale line = 1 mm.

Elachistocleis bicolor. Previous literature for this species includes papers by Lavilla and Langone (1995), Lajmanovich (1998), Echeverra and Lavilla (2000), Haas (2001; 2003), and Ulloa Kreisel (2003). A revision on
internal morphology appeared in Vera Candioti (2006b).
Chondrocranium and hyobranchial skeleton (N = 5, stages 34 and 35. Fig. 66). The chondrocranium of
these larvae represents 31% of the body length. The maximum width is at the level of the processus lateralis
posterior of the palatoquadrate. The suprarostral cartilage has corpus and alae fused in a single structure with
a curved anterior margin and a posterior margin bearing a medial, slightly outlined projection. The suprarostral is fused to the anterior margin of trabecular horns, and only the lateral part remains free. The trabecular
horns correspond approximately to 21% of the total length of the chondrocranium and are flat and distally
wider. The cranial floor is lightly chondrified in the central area. The carotid and craniopalatine foramina are
visible, the latter elongate and larger than the former. In the posterior margin of the cranial floor, the notochordal canal extends 13% of the chondrocranium length. In the lateral walls of the chondrocranium, the
orbital cartilages are formed only marginally and the central region is occupied by a large foramen that joins
the optic, oculomotor, trochlear and prootic foramina. The chondrocranium is open dorsally, and the frontoparietal fenestra is lined by the taeniae tecti marginales. The otic capsules are quadrangular and occupy nearly
31% of the chondrocranium total length. The fenestra ovalis (26% of the capsule length) is located ventrolaterally on each otic capsule. The otic capsules are dorsally joined by the tectum synoticum. In the palatoquadrate, the articular process is short, wide, and has three small anterior processes. The muscular process is
scarcely developed and has a long ventrolateral process with a length similar to that of the subocular bar. The
subocular bar is uniformly wide and in the most posterior part presents a long, rectangular, flat processus lateralis posterior that bears a ventral, bifid subotic process. The palatoquadrate attaches to the braincase via
three points: the quadratocranial commissure, the ascending process, attached to the cranial floor, and the larval otic process. The lower jaw includes the Meckels and the infrarostral cartilages. Meckels cartilages are
bar-like with dorsal and retroarticular processes. The infrarostral cartilages are fused forming a ring-like structure with a laminar projection arising from the medial, posterior margin. In the hyobranchial skeleton, the ceratohyals are elongate and have a wide, rounded anterior process, a tall, thin, medially directed anterolateral
process, and a tall and thin posterior process, partially concealed by the ceratobranchial I; the lateral edge of
the ceratohyal has a wide laminar projection posteriorly directed; the articular condyle is outlined in the posterodorsal margin of the ceratohyal. The basihyal is a very thin, cartilaginous bar. The pars reuniens is continANATOMY OF ANURAN TADPOLES

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uous with the ceratohyals and the basibranchial. The basibranchial is small and bears a thin and very long
urobranchial process (about 2 times longer than the basibranchial). The basibranchial is posteriorly fused to
the hypobranchial plates, which are in turn fused to each other. The ceratobranchials are fused to the hypobranchial plates and constitute a large branchial basket. Between the ceratobranchials II and III there is a
closed branchial process. Dorsally, three large spicules are differentiated, and the most lateral, wider than the
others, apparently represents the complete fusion of spicules I and II.

FIGURE 66. Elachistocleis bicolor, stage 35. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B)
Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view. ALPC anterolateral process of ceratohyal, APC anterior process of ceratohyal, ARP articular process, ASP ascending process, BB basibranchial, BH basihyal,
CB(I-IV) ceratobranchial, CF carotid foramen, CH ceratohyal, CPF craniopalatine foramen, FF frontoparietal fenestra, FO fenestra
ovalis, HP hypobranchial plate, IC infrarostral cartilage, LOP larval otic process, LPC lateral process of ceratohyal, MC Meckels cartilage, MP muscular process, NC notochordal canal, OC otic capsule, PLP processus lateralis posterior, PPC posterior process of ceratohyal, PR pars reuniens, PS processus suboticus, QCC quadratocranial commissure, RP retroarticular process, SB subocular bar, SC
suprarostral cartilage, SF subocular fenestra, TC terminal commissure, TH trabecular horn, TS tectum synoticum, TTM taenia tecti
marginalis, UP urobranchial process, VP ventrolateral process. Scale line = 1 mm.

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Musculature (N = 5, stages 34 and 35. Table 19 and Fig. 67). Thirty muscles are present in this species.
TABLE 19. Elachistocleis bicolor, stages 34 and 35. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Mandibulolabialis

ventromedial region of Meckels cartilage ventrolateral


surface of the infrarostral

it is a cylindrical and compact


muscle

Intermandibularis

anterior surface of Meckels cartilage median


aponeurosis

the whole muscle has the shape of


an inverted triangle, and it attaches
to a median aponeurosis common
to the m. interhyoideus, adopting
the complete structure, a
distinctive X-shape

Levator mandibulae longus


superficialis

posterior margin of the muscular process posterior


surface of Meckels cartilage

Levator mandibulae longus


profundus

anterior, dorsal surface of the muscular process lateral


edge of the suprarostral

it is well-developed

Levator mandibulae internus

dorsal surface of the subocular bar, near the medial


margin lateral edge of Meckels cartilage

the insertion is via a long tendon

Levator mandibulae externus

articular process of the palatoquadrate lateral edge of


the suprarostral

the insertion is through a common


tendon with the m. l. m. l.
profundus; the mandibular branch
of the trigeminal nerve (V3) runs
ventrally to this muscle; there is no
division into mm. l. m. e.
superficialis and profundus

Levator mandibulae articularis

dorsal surface of the muscular process lateral edge of


Meckels cartilage

Suspensoriohyoideus

posterior part of the ventral surface of the processus


lateralis posterior and ventral surface of the otic capsule
dorsal surface of the lateral process of the ceratohyal

it is formed of a few fibers, loosely


disposed

Orbitohyoideus

anterior, dorsal margin of the muscular process lateral


edge of the ceratohyal

it is scarcely developed

Suspensorioangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

Quadratoangularis

ventral surface of the palatoquadrate retroarticular


process of Meckels cartilage

it is placed laterally to the former


muscle

Hyoangularis

dorsal surface of the ceratohyal retroarticular process of


Meckels cartilage

it is scarcely developed

Interhyoideus

ventral surface of the lateral process of the ceratohyal


median aponeurosis

it is formed of parallel, fibers,


transversally and obliquely
disposed

Interhyoideus posterior

it forms a continuous and extensive layer, ventral to the


peribranchial chamber

Geniohyoideus

posterior, ventral surface of the infrarostral diffuse near


the thyroid gland

Levator arcuum branchialium I

ventral surface of the processus lateralis posterior, near its


lateral margin lateral surface of the ceratobranchial I
...... continued

ANATOMY OF ANURAN TADPOLES

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TABLE 19 (continued)
Muscle

Insertions

Levator arcuum branchialium II

ventral surface of the otic capsule ceratobranchials I and


II

Levator arcuum branchialium


III

two slips: anterior and anterolateral points on the ventral


surface of the processus lateralis posterior terminal
commissure II and III

Levator arcuum branchialium


IV

ventral surface of the otic capsule medial margin of the


ceratobranchial IV

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

branchial process terminal commissure I

Constrictor branchialis III

branchial process terminal commissure II

Constrictor branchialis IV

branchial process terminal commissure III

Subarcualis rectus I

three slips: lateral base of the posterior process of the


ceratohyal spicule I (dorsal slip), ceratobranchial I
(ventral1 slip), and branchial process (ventral2 slip

Subarcualis rectus II-IV

ventromedial surface of the ceratobranchial IV


branchial process

Subarcualis rectus II-IV


lateralis

distal part of the ceratobranchial IV branchial process

Subarcualis obliquus

urobranchial process branchial process

Diaphragmatobranchialis

peritoneum ceratobranchial III

Rectus cervicis

peritoneum branchial process

Rectus abdominis

Comments

peritoneum, approximately at half the abdomen level


pelvic griddle

the ventral2 slip is very thin and


long, and originates laterally to the
base of the posterior process, on a
small process of the posterior
margin of the ceratohyal; the
insertion of the ventral1 on the
ceratobranchial I is medial
regarding that of the dorsal slip

FIGURE 67. Elachistocleis bicolor, stage 35. Musculature (A) Dorsal view, superficial plane, (B) Dorsal view, middle plane, (C) Dorsal view, deep plane, (D) Ventral view, (E) Lateral view, superficial plane, (F) Detail of the insertions of mm. levatores arcuum branchialium, lateral view, (G) Ventral view, whole. CB(IIIV) constrictor branchialis, DB diaphragmatobranchialis, GH geniohyoideus,
HA hyoangularis, IH interhyoideus, IM intermandibularis, LB(IIV) levator arcuum branchialium, LMA levator mandibulae articularis, LME levator mandibulae externus, LMI levator mandibulae internus, LMLP levator mandibulae longus profundus, LMLS levator mandibulae longus superficialis, ML mandibulolabialis, OH orbitohyoideus, QA+SA quadratoangularis + suspensorioangularis,
RA rectus abdominis, SH suspensoriohyoideus, SO subarcualis obliquus, SRI subarcualis rectus I, SRIIIV subarcualis rectus IIIV,
SRIIIVLAT subarcualis rectus IIIV lateralis. Scale lines = 1 mm.

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Oral apparatus and buccopharyngeal cavity (N = 2, stage 35. Fig. 68). The mouth is terminal with a wide
oral slit devoid of papillae and keratinized structures. Gape width reaches 29% of the body length. Two upper
labial flaps hang covering the spatulate lower lip. In the buccal roof, the prenarial arena shows a single small
papilla. The choanae are large, subcircular and unperforated. From the posterior margin of each choana, a
large, flat and multifid narial wall papilla arises. A single, flat, pustulate papilla projects medially from the
choana lateral margin, accompanied by scarce pustules. The median ridge is two times higher than wide, triangular, and with a pustulate margin. Lateral ridge papillae are absent. Posteriorly to the median ridge, the buccal roof arena is not defined; numerous pustules and small conical papillae distribute irregularly on the central
region of the roof. Secretory pits appear in a broad array on the posterior region of the buccal roof. The dorsal
velum is long and smooth. In the buccal floor, the posterior surface of Meckels cartilage shows small pustules. The tongue anlage is small and devoid of lingual papillae. The buccal pockets are well-developed and
have a large, wide, flat and multifid prepocket papilla projecting from the anterior margin. The glottis is far
anteriorly placed, on the posterior margin of the buccal floor arena. On both sides, 6 tall, bifid papillae are
arranged approximately following a wide V-shape. Among them, small pustules are scattered. The ventral
velum is well-developed and posteriorly expanded; it shows an undulate margin, and a small median notch.
Gut content (N =10, stages 34 and 35. Tables 21 and 22). The gut contents were mainly composed of
euglenoids and diatoms with sizes ranging from <11% of the tadpole body length. Like in the other microhylids, the food is organized in strings that coil when entering into the oesophagus (Fig. 65).

FIGURE 68. Elachistocleis bicolor, stage 35. Oral apparatus and buccopharyngeal cavity (A) Mouth, frontal view, (B) Buccal roof,
(C) Buccal floor. BFA buccal floor arena, BFAP buccal floor arena papilla, BP buccal pocket, C choana, DV dorsal velum, G glottis,
GZ glandular zone, MR median ridge, NLP narial lateral papillae, NWP narial wall papilla, P pustulation, PNA prenarial arena, PNAP
prenarial arena papilla, PPP prepocket papilla, TA tongue anlage, VV ventral velum. Scale lines = 1 mm.

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PIPIDAE
Xenopus laevis. This species has been long studied; previous literature includes papers by Ridewood (1897;
1898), Ramaswami (1941), Weisz (1945), Gradwell (1971), Seale and Wassersug (1979), Wassersug and Hoff
(1979; 1982), Satel and Wassersug (1981), Trueb and Hanken (1992), and Haas (2001; 2003), among other
researchers.

FIGURE 69. Xenopus laevis, stage 31. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B) Chondrocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view. ALPC anterolateral process of ceratohyal, APC anterior process of ceratohyal, ARP articular process, ASP ascending process, BB basibranchial, CB(I-IV)
ceratobranchial, CF carotid foramen, CH ceratohyal, CP crista parotica, CPF craniopalatine foramen, FF frontoparietal fenestra, HP
hypobranchial plate, IC infrarostral cartilage, LOP larval otic process, LPC lateral process of ceratohyal, MC Meckels cartilage, MP
muscular process, NC notochordal canal, OC otic capsule, OCH olfactory channel, PCQL processus cornu quadratus lateralis, PCQM
processus cornu quadratus medialis, PLP processus lateralis posterior, PPC posterior process of ceratohyal, PR pars reuniens, QCC
quadratocranial commissure, SB subocular bar, SF subocular fenestra, SP suprarostral plate, TA tectum anterius, TC terminal commissure, TCA tentacular cartilage, TS tectum synoticum, TTM taenia tecti marginalis. Scale line = 1 mm.

ANATOMY OF ANURAN TADPOLES

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Chondrocranium and hyobranchial skeleton (N = 5, stage 31. Fig. 69). The chondrocranium of these larvae represents 56% of the body length. The maximum width is at the plane of the muscular process of the
palatoquadrate and the processus lateralis posterior of the palatoquadrate. The ethmoid region is represented
by a broad plate, homologous to the suprarostral cartilage and the trabecular horns of other tadpoles (Sokol
1975; Swart & De S 1999). This plate attenuates laterally and joins with a thin anterior process of the palatoquadrate, the processus cornu quadratus lateralis, constituting the tentacular cartilage. The cranial floor is
completely cartilaginous and the carotid and craniopalatine foramina are visible and small. In the posterior
margin of the cranial floor, the notochordal canal extends 11% of the chondrocranium length. In the lateral
walls of the chondrocranium, the orbital cartilages are completely formed and show the optic, oculomotor, trochlear and prootic foramina. The chondrocranium is open dorsally through the frontoparietal fenestra, which
is lined by the taeniae tecti marginales and anteriorly by the tectum anterius. Two longitudinal channels, the
olfactory channels, diverge anterolaterally from the tectum anterius. The otic capsules are quadrangular and
large, occupying nearly 30% of the chondrocranium total length. The crista parotica is well-developed,
located anterolaterally to the otic capsule, and it is continuous with a flat flange of cartilage that borders the
lateral and posterolateral margin of the capsule. The fenestra ovalis (39% of the capsule length) is located ventrolaterally on each otic capsule. The otic capsules are dorsally joined by the tectum synoticum. In the palatoquadrate, the articular process is very short. Laterally, the thin processus cornu quadratus lateralis arises, and
medially, there appear a wide process, the processus cornu quadratus medialis. The muscular process is
weakly developed. The subocular bar is interrupted approximately at half its length: the anterior part encloses
the anterior portion of the subocular fenestra, and the posterior part arises from the long, flat, rectangular, posterolaterally directed processus lateralis posterior. The palatoquadrate attaches to the braincase via three
points: the broad quadratocranial commissure, the ascending process, with a high attachment to the neurocranium, and the larval otic process, which joins the processus lateralis posterior and the otic capsule. The lower
jaw includes the Meckels and infrarostral cartilages. Meckels cartilages are elongate, curved, without processes, and articulate with the fused, indistinct infrarostral cartilages. A remarkable feature of the hyobranchial skeleton of this species is the presence of craniobranchial commissures, which join the crista parotica of
the neurocranium with the lateral margins of the branchial basket. The ceratohyals are elongate and have a
thin, acuminate, medially directed anterior process, a low, wide and rounded anterolateral process, a robust
lateral process, and a long, thin posterior process, continuous with the basibranchial; the articular condyle is a
rounded protuberance visible from a dorsal view. The basihyal is absent and the pars reuniens and the basibranchial are fused forming a median element that lies in a passage formed by a groove of each ceratohyal
posterior process. The basibranchial is posteriorly fused to the hypobranchial plates. The urobranchial process
is absent. The ceratobranchials are fused to the hypobranchial plates and constitute a large, voluminous branchial basket. Proximal and terminal commissures I-III are present, joining all the ceratobranchials anterior and
distally. The ceratobranchials have numerous lateral projections, and dorsally, all the filter plates corresponding to each ceratobranchial are chondrified. Spicules are absent.
Musculature (N = 5, stage 31. Table 20 and Fig. 70). Twenty-four muscles are present in this species.
TABLE 20. Xenopus laevis, stage 31. Cranial, hyoid and hyobranchial musculature.
Muscle

Insertions

Comments

Intermandibularis

anterior margin of Meckels cartilage median


aponeurosis

it is very thin, formed of a single layer


of fibers; the whole muscle has the
shape of an inverted triangle, and it
attaches to a median aponeurosis
common to the m. interhyoideus

Levator mandibulae longus


superficialis

anterior, lateral region of the subocular bar dorsal,


lateral surface of Meckels cartilage

it is the most developed of the levator


muscles
...... continued

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TABLE 20 (continued)
...... continued
Levator mandibulae longus
profundus

anterior, lateral surface of the subocular bar ventral


surface of the tentacle cartilage, near the junction of
the tentacle and the distal tip of the suprarostral
cartilage

it is very thin, formed of a few fibers,


and it runs parallel to the m. l. m. l.
superficialis until it diverges toward its
insertion

Levator mandibulae internus

anterior, medial surface the subocular bar lateral


edge of Meckels cartilage

it is scarcely developed, formed of a


few fibers

Levator mandibulae externus

anterior, medial surface of the muscular process


dorsal, lateral region of the Meckels cartilage

the mandibular branch of the


trigeminal nerve (V3) runs dorsally to
this muscle; there is no division into
mm. l. m. e. superficialis and
profundus

Levator mandibulae articularis

anterior, dorsal surface of the palatoquadrate lateral


edge of Meckels cartilage

it is a short, oblique muscle

Orbitohyoideus

anterior, dorsal margin of the muscular process


lateral edge of the ceratohyal

Quadratoangularis

ventral surface of the palatoquadrate lateral edge of


Meckels, cartilage sharing the point of origin with
the m. hyoangularis

Hyoangularis

dorsal surface of the ceratohyal lateral edge of


Meckels cartilage

Interhyoideus

ventral surface of the lateral process of the ceratohyal


median aponeurosis

it is well-developed, formed of parallel


fibers, transversally disposed

Geniohyoideus

posterior, ventral surface of the infrarostral


proximal point of the ceratobranchial II

it is very thin, formed of 4-5 fibers

Levator arcuum branchialium IIII

ventral surface of the posterior region of the


subocular bar, ventral surface of the processus
lateralis posterior, and ventrolateral surface of the otic
capsule lateral surface of ceratobranchials I, III and
III

these three muscles are very close, and


it is impossible to tell them apart

Levator arcuum branchialium


IV

posterolateral surface of the otic capsule terminal


commissure III and medial, ventral surface of the
ceratobranchial IV

Dilatator laryngis

posterolateral surface of the otic capsule arytenoid


cartilage

Constrictor branchialis II

proximal point on the ceratobranchial II terminal


commissure I

Constrictor branchialis III

proximal point on the ceratobranchial III distal


point on the ceratobranchial III

it runs on the anterior margin of the


ceratobranchial III

Subarcualis rectus I

posterior, medial margin of the ceratohyal proximal


part of the ceratobranchial I

it is formed of a short, single slip of


fibers

Subarcualis rectus II-IV

proximal point on the ceratobranchial III, medial to


the former muscle terminal commissure III

this muscle resembles the mm.


constrictor branchiales in orientation,
due to its far lateral origin, without any
attachment on the medial
ceratobranchial IV

Subarcualis obliquus

ceratobranchial II median aponeurosis

Diaphragmatobranchialis

peritoneum distal edge of the ceratobranchial III

Rectus cervicis + Rectus


abdominis

ceratobranchial III pelvic griddle

in the literature about pipids, these two


muscles appear referred to as a single
muscle, the m. quadratohyoangularis

ANATOMY OF ANURAN TADPOLES

fibers of these two muscles are


continuous, and form two single layers
on each side of the abdomen

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FIGURE 70. Xenopus laevis, stage 31. Musculature (A) Dorsal view, superficial plane, (B) Dorsal view, deep plane, (C) Ventral view,
(D) Lateral view, superficial plane, (E) Lateral view, deep plane, (F) Ventral view, whole. CB(IIIII) constrictor branchialis, GH geniohyoideus, HA hyoangularis, IH interhyoideus, IM intermandibularis, LB(I-IV) levator arcuum branchialium, LMA levator mandibulae
articularis, LME levator mandibulae externus, LMI levator mandibulae internus, LMLP levator mandibulae longus profundus, LMLS
levator mandibulae longus superficialis, OH orbitohyoideus, QA quadratoangularis, RA rectus abdominis, RC rectus cervicis, SO subarcualis obliquus, SRI subarcualis rectus I, SRIIIV subarcualis rectus IIIV. Scale lines = 1 mm.

Oral apparatus and buccopharyngeal cavity (N = 2, stage 31. Fig. 71). The mouth is terminal with a wide
oral slit devoid of papillae and keratinized structures. Gape width reaches 32% of the body length. Two thin
tentacles arise from the buccal commissures. The buccal roof is not pigmented and devoid of any papillae or
pustulation. The choanae are large, subcircular, and anteriorly located. On both sides of the roof, there appear
three paired pad-like structures, supposed to be homologous to the dorsal velum of other species. Conspicuous
secretory pits appear in the dorsal vela, and the tissue surrounding them. The buccal floor is also short and
smooth, with only a small pair of short papillae on the anterior margin of the ceratohyals. A free valve-like
flap is absent and the secretory ridges, that in other tadpoles are characteristic of the ventral velum, develop in
a structure named pharyngobranchial tract by Weisz (1945). This structure includes a thick central band
along the dorsal edge of the hypobranchial plate, and triangular projections out along the crest of each filter
plate. The secretory ridges run parallel to the contour of the pharyngobranchial tract. Secretory pits appear on
the anterior, central region of the pharyngobranchial tract.

FIGURE 71. Xenopus laevis, stage 31. Oral apparatus and buccopharyngeal cavity (A) Mouth, frontal view, (B) Buccal roof, (C) Buccal floor. C choana, DV(I-III) dorsal vela, FP filter plate, PBT pharyngobranchial tract. Scale lines = 1 mm.

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Gut content (N = 7, stages 3031. Tables 21 and 22). As in microhylids, distinctive mucous cords appear
inside the digestive tract. These cords are, however, far thinner, with a diameter 0.3 mm (Fig. 72). Entangled
in these mucous strings, there appear unicellular chlorophytes as small as 0.005 mm (which represents <1% of
the tadpole size, accumulating almost 2% of the total food volume) and large cladocerans (3%6% of the tadpole size; 97.6% of the total volume).

FIGURE 72. Xenopus laevis, stage 31 (A) Mucus and food cords from the gut. Small chlorophytes (<1% tadpole body length) and
cladocerans (arrow; 36% tadpole body length) appear entangled in the mucus, (B) Xenopus laevis tadpole found dead after trying to
ingest a whole dead conspecific larvae. Scale lines = 1 mm.

Morphological variation. Geometric morphometrics. Relative warp analysis


Chondrocranium. Four clusters were detected by the relative warp analysis, and they are shown in the scatterplot of the first two relative warps (axes RW1 and RW2; Fig. 73). The first relative warp (RW1) captures
52.94% of the total chondrocranium shape variation, and together with RW2 accumulates 71.51% (the
remaining percentages appear in Table 23). The first axis clearly separates Lepidobatrachus llanensis, with
the highest score. Tadpoles of Dendropsophus microcephalus group show the lowest scores on this axis. The
second axis separates microhylids and Xenopus laevis, with low scores, from Dendropsophus species, with the
highest values. The remaining species form a group with intermediate scores on both axes. The deformation
grids describe positive and negative deviations from the mean configuration along the relative warp axes. Figure 73 shows that high scores on RW1 are mainly associated with a widening of the anterior part of the chondrocranium caused by the lateral translation of landmarks 27, and by relatively smaller otic capsules,
described by landmarks 912. On RW2, species with highest scores show a conspicuous narrowing of the
anterior part of the chondrocranium as a result of the medial translation of landmark 2, and a large, medially
curved muscular process of the palatoquadrate, described by landmarks 47. Species with the lowest scores
show a wider anterior part of the chondrocranium, and the muscular process is almost parallel to the dorsoventral plane. Species with intermediate scores have a generalized, quadrangular chondrocranium.
TABLE 23. Relative warp analysis (RWA) of chondrocrania of tadpoles of 19 species (N = 19). Singular values and percentages explained by each deformation.
N

Eigenvalue

Acumm. %

Eigenvalue

Acumm. %

0.55498

52.94

52.94

10

0.05738

0.57

98.67

0.32876

18.58

71.51

11

0.05368

0.50

99.16

0.25751

11.40

82.91

12

0.04389

0.33

99.49

0.17952

5.54

88.45

13

0.03560

0.22

99.71

0.14345

3.54

91.99

14

0.02425

0.10

99.81

0.12361

2.63

94.61

15

0.02033

0.07

99.88

0.08673

1.29

95.90

16

0.01904

0.06

99.94

0.08570

1.26

97.17

17

0.01658

0.05

99.99

0.07370

0.93

98.10

18

0.00671

0.01

100

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FIGURE 73. Chondrocranium. Relative warp analysis (RWA). Scores of tadpoles of 19 species on two first axes. CA Chaunus
arenarum, CC Ceratophrys cranwelli, CP Chiasmocleis panamensis, CS Chaunus spinulosus, DM Dendropsophus microcephalus,
DN Dendropsophus nanus, DRM Dermatonotus muelleri, EB Elachistocleis bicolor, HR Hypsiboas rosenbergi, LL Lysapsus limellum, LLL Lepidobatrachus llanensis, PH Phyllomedusa hypochondrialis, PHS Phyllomedusa sauvagii, PP Pseudis paradoxus, PS
Physalaemus santafecinus, SB Scinax boulengeri, SN Scinax nasicus, TA Telmatobius cf. atacamensis, XL Xenopus laevis. Grids
describe shape variation at positive and negative values of axes. The arrows show the chondrocranial regions whit pronounced shape
changes.

Hyobranchial skeleton. Four clusters were detected by the RWA of hyobranchial skeleton; they are shown in
the scatterplot on the first two relative warps (Fig. 74). The first relative warp (RW1) captures a high percentage of the total shape variation, 53.76%, and accounts for 72.89 % together with RW2 (the remaining values
appear in Table 24). Dendropsophus species and Ceratophrys cranwelli score high on RW1, whereas suspension-feeding microhylids and Xenopus have the lowest values. Suspension-rasper, benthic and nektonic tadpoles score with intermediate values on RW1. All these three groups share high values on RW2. Finally,
Lepidobatrachus llanensis tadpoles constitute a separate cluster, with intermediate and low values on RW1
and RW2 respectively. The deformation grids added to Figure 74 show that on RW1, shape variation is mainly
associated with the position of landmarks 58 relative to 9 and 1416, which reflect the size of the branchial
basket. From the consensus shape, species with high scores on RW1 have reduced branchial baskets, whereas
species with low scores have enlarged branchial baskets. Landmarks 9 and 1416 also vary in their location
relative to landmarks 1013, indicating a change in the size of the hypobranchial plate from high to low scoring species. On RW2, main shape variation is due to landmarks 14, which indicate a lateral expansion of the
ceratohyals in low scoring specimens.

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FIGURE 74. Hyobranchial skeleton. Relative warp analysis (RWA). Scores of tadpoles of 19 species on two first axes. CA Chaunus
arenarum, CC Ceratophrys cranwelli, CP Chiasmocleis panamensis, CS Chaunus spinulosus, DM Dendropsophus microcephalus,
DN Dendropsophus nanus, DRM Dermatonotus muelleri, EB Elachistocleis bicolor, HR Hypsiboas rosenbergi, LL Lysapsus limellum, LLL Lepidobatrachus llanensis, PH Phyllomedusa hypochondrialis, PHS Phyllomedusa sauvagii, PP Pseudis paradoxus, PS
Physalaemus santafecinus, SB Scinax boulengeri, SN Scinax nasicus, TA Telmatobius cf. atacamensis, XL Xenopus laevis. Grids
describe shape variation at positive and negative values of axis. The arrows show the hyobranchial regions whit pronounced shape
changes.

A MANOVA on measurements of the hyobranchial skeletons was performed on the four groups obtained
after the RW analysis (Fig. 2; Table 25). Four groups differ significantly (Wilks = 0.006; p < 0.0001); in

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post hoc test, there is no significant difference on in-lever arm proportion of Lepidobatrachus llanensis and
microhylids + Xenopus laevis groups (p = 0.986).

TABLE 24. Relative warp analysis (RWA) of hyobranchial skeletons of tadpoles of 19 species (N = 58). Singular values
and percentages explained by each deformation.
N

Eigenvalue

% Acumm.

Eigenvalue

% Acumm.

1.29491

53.76

53.76

15

0.09518

0.29

98.73

0.77264

19.14

72.89

16

0.08814

0.25

98.97

0.53983

9.34

82.24

17

0.07766

0.19

99.17

0.38816

4.83

87.07

18

0.07072

0.16

99.33

0.30716

3.02

90.09

19

0.06541

0.14

99.47

0.24305

1.89

91.99

20

0.05839

0.11

99.57

0.23079

1.71

93.69

21

0.05643

0.10

99.68

0.20128

1.30

94.99

22

0.05241

0.09

99.77

0.16399

0.86

95.85

23

0.04450

0.06

99.83

10

0.14761

0.70

96.55

24

0.03855

0.05

99.88

11

0.13472

0.58

97.13

25

0.03695

0.04

99.92

12

0.12417

0.49

97.63

26

0.03379

0.04

99.96

13

0.11829

0.45

98.08

27

0.02908

0.03

99.98

14

0.10561

0.36

98.44

28

0.02251

0.02

100

TABLE 25. In-lever arm proportion and relative areas of the hyobranchial skeleton of tadpoles of 19 species. CB area of
ceratobranchial, CH area of ceratohyal, HC area of hypobranchial plate, ILAP in-lever arm proportion. Species list has
been reorganized in order to highlight the uniformity of values within RWA groups.
ILAP

%CH

%HB

%CB

Chiasmocleis panamensis

0.23

0.16

0.08

0.76

Dermatonotus muelleri

0.15

0.17

0.05

0.77

Elachistocleis bicolor

0.22

0.16

0.07

0.77

Xenopus laevis

0.20

0.20

0.07

0.73

Chaunus arenarum

0.33

0.27

0.20

0.53

Chaunus spinulosus

0.32

0.26

0.20

0.54

Hypsiboas rosenbergi

0.37

0.26

0.20

0.54

Lysapsus limellum

0.32

0.29

0.19

0.53

Phyllomedusa hypochondrialis

0.29

0.27

0.17

0.56

Phyllomedusa sauvagii

0.24

0.25

0.14

0.61

Physalaemus santafecinus

0.34

0.26

0.19

0.54

Pseudis paradoxus

0.25

0.27

0.19

0.54

Scinax boulengeri

0.23

0.28

0.18

0.54

Scinax nasicus

0.42

0.25

0.20

0.56

Telmatobius cf. atacamensis

0.39

0.26

0.25

0.50

Ceratophrys cranwelli

0.51

0.39

0.32

0.29

Dendropsophus microcephalus

0.53

0.46

0.33

0.21

Dendropsophus nanus

0.49

0.46

0.32

0.22

Lepidobatrachus llanensis

0.21

0.35

0.24

0.41

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Gut content variation. Correspondence analysis


This analysis excludes Chiasmocleis panamensis because food items could not be quantified. The results of
the CA performed on food matrices with the remaining 18 species are summarized in Tables 2627 and the
biplots of Figures 75 and 76. In the CA of the food type matrix, the two first axes explain 32.4% of the variance in the dataset, and variables that most contribute to the axes are the proportions of filamentous chlorophytes, oliqochaetes and tadpoles consumed (Figure 75). The first axis separates Scinax boulengeri, whose
gut content was almost totally composed of fragments of filamentous chlorophytes. On the second axis, Dendropsophus species score with high values, in association with ingestion of whole oligochaetes. Lepidobatrachus llanensis has the lowest scores and consumed mainly whole tadpoles. All the remaining species ingested
various types of food items, including microalgae, protozoans, small invertebrates and macrophytes. In the
CA of the food size matrix (Fig. 76), the two first axes explain 36.24% of the variance in the dataset, and variables that most contribute to the construction of the first axis are the percentages of large food items (i.e.,
those that represent more than 60% of the tadpole size). The first axis separates Lepidobatrachus llanensis,
Dendropsophus nanus and D. microcephalus from the remaining species with lower scores. Variables that
most contribute to axis 2 are the percentages of food items with sizes <1% and 10% of the tadpole size. On
this axis, Dermatonotus muelleri and Phyllomedusa sauvagii separate from the other species because of a
marked association with food items of size <1% of the body length. Elachistocleis bicolor and Chaunus
arenarum consume mainly food particles between <11% of their length. Chaunus spinulosus, Phyllomedusa
hypochondrialis, Lysapsus limellum, Scinax nasicus, Physalaemus santafecinus, Hypsiboas rosenbergi, Ceratophrys cranwelli, and Xenopus laevis appear associated with a food item size between 19% of the tadpole
length. Telmatobius cf. atacamensis, S. boulengeri and Pseudis paradoxus consume frequently food particles
of sizes between 1030% of their body length.

TABLE 26. Correspondence analysis (CA) of gut contents of tadpoles of 18 species (N = 18). Food types matrix. Singular values and percentages explained by each extracted axis. Chiasmocleis panamensis is excluded because gut content
data could not be recorded.
N

Eigenvalue

% Acumm.

Eigenvalue

% Acumm.

0.986

16.82

16.82

0.171

2.91

95.77

0.914

15.58

32.40

10

0.113

1.92

97.69

0.874

14.91

47.31

11

0.088

1.51

99.19

0.735

12.53

59.84

12

0.036

0.61

99.80

0.659

11.24

71.08

13

0.009

0.16

99.96

0.579

9.87

80.95

14

0.002

0.04

99.99

0.433

7.38

88.33

15

0.01

100

0.266

4.53

92.86

16

100

TABLE 27. Correspondence analysis (CA) of gut contents of tadpoles of 18 species (N = 18). Food sizes matrix. Singular values and
percentages explained by each extracted axis. Chiasmocleis panamensis is excluded because gut content data could not be recorded.
N

Eigenvalue

% Acumm.

Eigenvalue

% Acumm.

0.931

21.18

21.18

12

0.062

1.42

97.86

0.662

15.06

36.24

13

0.055

1.25

99.13

0.554

12.61

48.85

14

0.022

0.50

99.62
..... continued

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TABLE 27 (continued)
N

Eigenvalue

% Acumm.

Eigenvalue

% Acumm.

0.429

9.77

58.61

15

0.013

0.29

99.91

0.413

9.40

68.02

16

0.004

0.09

100

0.353

8.03

76.05

17

100

0.268

6.09

82.14

18

100

0.231

5.27

87.40

19

100

0.192

4.38

91.78

20

100

10

0.123

2.79

94.57

21

100

11

0.083

1.89

96.46

FIGURE 75. Biplot of the correspondence analysis (CA) on diet of tadpoles of 18 species. Food type matrix. Shaded: CA Chaunus
arenarum, CC Ceratophrys cranwelli, CS Chaunus spinulosus, DM Dendropsophus microcephalus, DN Dendropsophus nanus, DRM
Dermatonotus muelleri, EB Elachistocleis bicolor, HR Hypsiboas rosenbergi, LL Lysapsus limellum, LLL Lepidobatrachus llanensis,
PH Phyllomedusa hypochondrialis, PHS Phyllomedusa sauvagii, PP Pseudis paradoxus, PS Physalaemus santafecinus, SB Scinax
boulengeri, SN Scinax nasicus, TA Telmatobius cf. atacamensis, XL Xenopus laevis. Vectors: diet variables, qualitative type of food.

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FIGURE 76. Biplot of the correspondence analysis (CA) on diet of tadpoles of 18 species. Food size matrix. Shaded: CA Chaunus
arenarum, CC Ceratophrys cranwelli, CS Chaunus spinulosus, DM Dendropsophus microcephalus, DN Dendropsophus nanus, DRM
Dermatonotus muelleri, EB Elachistocleis bicolor, HR Hypsiboas rosenbergi, LL Lysapsus limellum, LLL Lepidobatrachus llanensis,
PH Phyllomedusa hypochondrialis, PHS Phyllomedusa sauvagii, PP Pseudis paradoxus, PS Physalaemus santafecinus, SB Scinax
boulengeri, SN Scinax nasicus, TA Telmatobius cf. atacamensis, XL Xenopus laevis. Vectors: diet variables, food items size <1%
150% of tadpole body length.

Gut content-morphology relationship. Partial canonical phylogenetic ordination


This analysis excludes Chiasmocleis panamensis because of the lack of data for the food matrix. CCA and
partial CPO were performed on food size, morphology, and phylogenetic matrices of the remaining 18 species. After a Monte Carlo permutations test, morphological and phylogenetic matrices were reduced because
some of the variables had no significant variance, and the analysis excluded them automatically. In the morphological matrix, the variables that were retained are the first partial warp of the hyobranchial skeleton, the
ih/oh ratio and mouth gape width; together they explain almost 33% of the total inertia in the food size matrix
(p < 0.05). In the phylogenetic matrix, only the genus Dendropsophus was significant by accounting for
14.74% of the total food size-variation (p = 0.006). Tables 28 and 29 show individual significances of variables in both matrices. After the partial CPO, considering morphological and phylogenetic matrices, variance
in prey size was partitioned into variances unique to morphological variables (24% of the food size matrix),

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unique to phylogeny (the genus Dendropsophus; 12%; p = 0.002), and the shared variance (3%). The morphological matrix was reduced again; only mouth gape width remained significant for the gut content ordination
by explaining a 12% of the total inertia (p = 0.041), whereas the phylogenetically independent hyobranchial
apparatus effect (skeleton and ih/oh ratio) was small and nonsignificant (6%; p = 0.179 and p = 0.285, respectively). The triplot in Figure 77 shows the ordination of tadpole species, food sizes proportions and morphological variables on the first two canonical axes (46.7% of the variation). Four clusters were defined.
Elachistocleis bicolor and Dermatonotus muelleri score low on the first ordination axis and high on the second. These species possess the lowest values on the first relative warp of the hyobranchial skeleton (i.e., a
well-developed branchial basket), high values of the ih/oh ratio, an intermediate value of mouth gape width,
and frequently consume food items smaller than 1% of their body length. Ceratophrys cranwelli, Dendropsophus nanus and D. microcephalus have high scores on axis 1 and the lowest on axis 2, the highest values of
the hyobranchial skeleton first relative warp (i.e., a reduced branchial basket), the lowest ih/oh ratio, a low or
intermediate value of gape width, and a strong association with food sizes between 5060% and 90% of the
body length. Lepidobatrachus llanensis separates from the other species, with high scores on axes 1 and 2, a
slightly reduced branchial basket, a low ih/oh ratio, a very large mouth gape, and a food item size that exceeds
80% of the body length. Finally, a large group of species has intermediate scores on canonical axes 1 and 2.
Most of them show intermediate values of the first relative warp (i.e., branchial baskets occupying 4050% of
the total hyobranchial surface), intermediate values on ih/oh ratio and mouth gape, and food item sizes frequently between 130% of the body length.
TABLE 28. Partial canonical phylogenetic ordination (pCPO) of food size, morphology and phylogeny of tadpoles of 18 species. Individual significance of morphological variables ( = 0.05). Percentages of explained variation, F and p values after 9999 Monte Carlo
irrestrict permutations.
Variable

F-ratio

Var. %

Acumm. Var. %

ih/oh

2.44

0.002*

10.99

hRW1

2.02

0.012*

11.5

22.49

mouth

2.04

0.050*

10.76

33.25

h2

0.75

0.653

h3

1.24

0.239

h4

0.95

0.494

h5

1.14

0.349

h6

1.52

0.095

filt

1.10

0.374

TABLE 29. Partial canonical phylogenetic ordination (pCPO) of food size, morphology and phylogeny of tadpoles of 18 species. Individual significance of taxonomic groups ( = 0.01). Percentages of explained variation, F and p values after 9999 Monte Carlo
irrestrict permutations. Groups composition appears in Fig. 3.
Group

F-ratio

Var. %

H (Dendropsophus)

2.78

0.006*

14.74

0.10

0.986

1.19

0.300

0.67

0.711

1.33

0.200

1.14

0.329

1.48

0.125

1.07

0.369

0.75

0.669

1.17

0.341

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FIGURE 77. Triplot of the canonical correspondence analysis (CCA) on diet and morphology of tadpoles of 18 species. Shaded: CA
Chaunus arenarum, CC Ceratophrys cranwelli, CS Chaunus spinulosus, DM Dendropsophus microcephalus, DN Dendropsophus
nanus, DRM Dermatonotus muelleri, EB Elachistocleis bicolor, HR Hypsiboas rosenbergi, LL Lysapsus limellum, LLL Lepidobatrachus llanensis, PH Phyllomedusa hypochondrialis, PHS Phyllomedusa sauvagii, PP Pseudis paradoxus, PS Physalaemus santafecinus, SB Scinax boulengeri, SN Scinax nasicus, TA Telmatobius cf. atacamensis, XL Xenopus laevis. Percentages: prey sizes relative to
tadpole body length. Arrows: significant morphological variables: HRW1 first relative warp of the hyobranchial skeleton, MOUTH
mouth gape width, IH/OH mm interhyoideus and orbitohyoideus ratio.

Discussion
Interspecific variation. Morphology
Skeleton. Morphological variation among cartilaginous skeletons of anuran larvae is well documented. Since
the synthesis presented by Cannatella (1999), the number of descriptions of chondrocrania have increased,

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and studies involving quantitative aspects have been recently added to qualitative approaches (e.g., Larson
2002; 2005; Vera Candioti 2006a). Skeletal features, as well as muscular, oral, and other larval characters, are
proving useful in the reconstruction of phylogenetic relationships (e.g., Larson & De S 1998; Maglia et al.
2001; Haas 2003; Pgener et al. 2003)
Most of the species in this study have cartilaginous skeletons which generally coincides with what Cannatella (1999) described as a generalized tadpole skeleton. This is evident in the ordination plots of the chondrocrania and hyobranchial skeletons, where, from a central cluster of numerous species, unusual morphologies
diverge in the morphospace (Figs. 73 and 74). The group of species with generalized morphology includes
Chaunus arenarum, C. spinulosus, Hypsiboas rosenbergi, Lysapsus limellum, Phyllomedusa hypochondrialis,
P. sauvagii, Physalaemus santafecinus, Pseudis paradoxus, Scinax boulengeri, S. nasicus and Telmatobius cf.
atacamensis. These species differ in several traits, mainly relative to phylogeny, and the character states are
frequently maintained within genera.
Chaunus arenarum and C. spinulosus show skeletal features similar to C. marinus and C. schneideri, e.g.,
suprarostral with single corpus and differentiated, dorsally fused alae, quadratoorbital commissure, quadratoethmoid process and lateral process of the trabecular horn present, and larval otic process absent (Fabrezi &
Vera 1997; Haas 2003). In the hyobranchial skeleton, the basihyal is absent in C. schneideri (Fabrezi & Vera
1997; Haas 2003). The gastromyzophorous tadpoles of Atelophryniscus chrysophorus, now included in Chaunus (Frost et al. 2006 and references therein) have a highly modified skeletal morphology associated with
their life in fast flowing waters (Lavilla & De S 2001). The genus Chaunus was recently separated from Bufo
by Frost et al. (2006), in a study which, mainly on the basis of molecular characters, divides the large, paraphyletic genus Bufo into several monophyletic genera with new nominations (Pramuk 2006 presented similar results based on adult morphology and molecular data of South American Bufo). Most of the larval
features in Chaunus are shared with other genera, and the presence of the quadratoorbital commissure has
been proposed as a synapomorphy of bufonids excluding Melanophryniscus (Frost et al. 2006).
Physalaemus santafecinus has a skeleton similar to those of Chaunus tadpoles. The alae and corpus of the
suprarostral are dorsally fused, with two deep notches in the distal margin of the cartilage. The quadratoorbital
commissure and quadratoethmoid and anterolateralis of the otic capsule processes are present, and the larval
otic process and basihyal are absent. Physalaemus biligonigerus and P. cuqui share several of the cited features, except for the suprarostral of P. cuqui, where alae and corpus are not fused, but syndesmotically articulated (Fabrezi & Vera 1997). Haas (2003) mentioned the presence of the larval otic process and basihyal in P.
biligonigerus, whereas Fabrezi and Vera (1997) did not find such structures in the same species.
Morphological variation within the genus Telmatobius is low. Five species described, T. cf. atacamensis,
T. espadai (formerly, T. bolivianus), T. pisanoi, T. ceiorum and T. laticeps, agree in numerous traits such as the
configuration of the suprarostral cartilage, adrostral cartilages, well-developed quadratoethmoid and pseudopterygoid processes, larval otic process absent, and presence of the anterolateral process of the otic capsule (in
T. espadai, the crista parotica is also very well-developed) (Fabrezi & Lavilla 1993; Lavilla & De la Riva
1993, as T. bolivianus; this study). Some intertaxic differences include the relationship between the elements
forming the suprarostral (fused in T. ceiorum and T. espadai), the shape and size of adrostral cartilages, the
attachment of the ascending process relative to the oculomotor foramen (intermediate in T. pisanoi and T.
espadai), among others, and in the hyobranchial skeleton, the junction among ceratobranchials, spicules and
hypobranchial plates, the shape of the urobranchial process, and the presence of basihyal (only in T. espadai)
also contribute.
Previous studies on hylid larvae indicate a wide variation in the chondrocrania and visceral skeletons,
mainly at inter-generic levels. Among hylines, the skeletons of Hypsiboas and Scinax spp. have very different
features. The chondrocranium of H. rosenbergi has a three-elements suprarostral, with alae dorsally articulated to the corpus, quadratoethmoid process, pseudopterygoid process absent, and a very long anterolateral
process of the otic capsule that almost reaches the otic process (Haas 1996a, mentions a larval otic process); in

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the hyobranchial skeleton, the branchial basket is well-developed with numerous lateral projections and the
basihyal is absent. Other species of Hypsiboas belonging to different species groups have similar traits. The
suprarostral cartilage is comparable to that of H. andinus, H. cordobae, H. geographicus, H. lanciformis, H.
pulchellus, H. raniceps and H. semilineatus. The genus Hypsiboas has been recently separated from Hyla on
the basis of molecular characters (Faivovich et al. 2005). Both genera differ in several chondrocranial features, yet some traits are shared by species across genera. Hyla arborea, H. annectans and H. cinerea have a
suprarostral cartilage different from that of Hypsiboas spp., with alae and corpus almost completely fused by
their lateral margins, resulting in a distal border with slightly pronounced notches (<50% of the suprarostral
proximodistal length Haas 2003). Besides in Hypsiboas rosenbergi, the larval otic process is absent in other
Hypsiboas, such as H. andinus, H. lanciformis, H. geographicus, H. raniceps and H. semilineatus; conversely,
it is present in H. cordobae, H. pulchellus, and two Hyla species (H. annectans and H. cinerea). Finally, the
basihyal is present in Hysiboas andinus, H. geographicus, H. pulchellus, H. raniceps and H. semilineatus
(Lavilla & Fabrezi 1987; De S 1988; Haas 1996a; 2003; DHeursel & De S 1999; Alcalde et al. 2000; Vera
Candioti 2000; Alcalde 2001; Alcalde & Rosset 2003).
In Scinax species, alae and corpus of suprarostral cartilage are fused to various extents, resulting in distal
notches of various depths. In S. boulengeri, S. acuminatus, and S. uruguayus (Fabrezi & Lavilla 1992; Alcalde
et al. 2006; this study), notches are slightly insinuated, and the distal margin is almost smooth, whereas in S.
nasicus, S. fuscovarius, S. ruber and S. granulatus, notches are deeper (Fabrezi & Vera 1997; Haas 1996a;
2003; Alcalde & Rosset 2003; this study). Scinax squalirostris has a similar suprarostral cartilage, although a
cartilaginous bridge connecting alae and corpus ventrally has been reported in one specimen (Alcalde & Rosset 2003). Tadpoles of S. boulengeri and S. uruguayus also share the massive configuration of the infrarostral
and Meckels cartilage, the narrow muscular process, and the uniformly wide trabecular horns (Alcalde et al.
2006). There is a close resemblance across Scinax studied species concerning the remaining skeleton features,
such as the small otic capsules, larval otic process, pseudopterygoid process absent, ceratobranchials with lateral projections, and a small or absent basihyal (Fabrezi & Lavilla 1992; Haas 1996a; 2003; Fabrezi & Vera
1997; Alcalde & Rosset 2003).
Recently incorporated to Hylinae (Frost 2007 and citations therein), the genera Lysapsus and Pseudis are
very similar to each other. They possess a distinctive combination of traits, such as a single suprarostral cartilage, with a deep dorsomedial notch, a thickened articulation zone of the trabecular horns, weak development
of the orbital cartilages, ultralow attachment of the ascending process, laterally expanded middle and caudal
palatoquadrate; quadratoethmoid, pseudopterygoid, and larval otic processes present, a reticulating cartilaginous connection between spicules III and IV of the hyobranchial skeleton, and basihyal absent (Lavilla & De
S 1999; Haas 2003; this study). Recently, Alcalde and Barg (2006) addressed a more complete study on these
two genera, and pointed out some variable features, e.g. the length of the pseudopterygoid process, the larval
crista parotica, the processus basicapsularis, the configuration of the ascending process, and the proximal
commissures in the hyobranchial skeleton.
Finally among hylids, and within the large group of tadpoles with a generalized morphology, the Phyllomedusinae have a morphological uniformity as well (with the exception of Phasmahyla guttata Fabrezi &
Lavilla 1992). All features mentioned in the previously described species are found in the species I studied:
suprarostral cartilage with deep distal notches, quadratoethmoid process, subocular bar with three triangular
processes in the lateral margin, larval otic process, ascending process incorporated into the cranial floor, and
well-developed branchial baskets with lateral projections and basihyal present, among other characters (Fabrezi & Lavilla 1992; Haas 1996a; 2003; Fabrezi & Vera 1997; Sheil & Alamillo 2005). Other species, Phyllomedusa distincta, P. trinitatis, P. vaillanti and Agalychnis callidryas also have a pseudopterygoid process. In
Phyllomedusa trinitatis and P. vaillanti, the elements forming the suprarostral cartilage are medially detached
(Haas 1996a; Sheil & Alamillo 2005); some specimens of P. sauvagii in the present study show the same condition.

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A group of species diverges from the generalized pattern. Dendropsophus nanus, D. microcephalus, Chiasmocleis panamensis, Dermatonotus muelleri, Elachistocleis bicolor, Ceratophrys cranwelli, Lepidobatrachus llanensis and Xenopus laevis separate from the remaining species in the ordination plots of the
chondrocrania and hyobranchial skeletons.
Tadpoles of the Dendropsophus microcephalus group seem to have a very uniform morphology (Fabrezi
& Lavilla 1992; Haas 1996a; Vera Candioti & Haas 2004; Vera Candioti et al. 2004); indeed, D. nanus and D.
microcephalus skeletons are qualitatively nearly indistinguishable; one difference is the posterior fusion of the
infrarostral cartilages in D. microcephalus (however, Fabrezi & Lavilla 1992 found fused infrarostrals in a
sample of D. nanus tadpoles). Both species possess rostrocaudally long chondrocrania with short, narrow trabecular horns, single suprarostrals, and straight palatoquadrates with a convex, quadrangular muscular process. Furthermore, the hyobranchial skeletons of these species are very similar to each other, and yet very
different from other hylids, with thick, rostrocaudally long ceratohyals, reduced branchial baskets with barlike ceratobranchials devoid of lateral projections and spicules. Further descriptions of skeletons of other species from this and related groups (former 30-chromosomes Hyla spp., e.g., D. labialis, D. columbianus, D.
minutus, D. marmoratus, D. parviceps, D. leucophyllatus groups) are still pending; such data will contribute
to understanding if these similar traits constitute apomorphic characters capable of defining these groups of
species. To date, the only related species described is D. ebraccatus (D. leucophyllatus group Haas 2003),
and in characters of both the skeleton and musculature, it more closely resembles Hypsiboas rosenbergi and
similar species.
Ceratophrys cranwelli tadpoles diverge slightly from the remaining species in the chondrocrania ordination, and noticeably in the hyobranchial skeletons ordination (Vera Candioti 2006a; this study). These larvae
share a number of character states with congeneric species; the chondrocranium is similar to that of C. cornuta, C. ornata, C. calcarata and C. aurita, with robust construction, very short trabecular horns, strong jaw
cartilages, and a closed cranial roof (Lavilla & Fabrezi 1992; Wild 1997a,b; Haas 2003; Vera Candioti 2005).
Likewise, the hyobranchial skeletons have a uniform morphology, with short, robust ceratohyals, basibranchial continuous with the pars reuniens, and scarcely developed branchial basket with lateral projections
reduced or absent, and spicules absent. The development of the ceratohyals and the reduction of the branchial
basket cause this species to cluster with the Dendropsophus microcephalus group tadpoles in the hyobranchial
skeleton ordination (Vera Candioti 2006a; this study).
Tadpoles of Lepidobatrachus invariably separate from the other species in ordination analyses (Vera Candioti 2006a; this study); they are referred to as aberrant larvae, and there are more differences between them
(Ortons type IV larvae, Orton 1953) and other type IV tadpoles than between type IV and the remaining types
of larvae (M. Fabrezi pers. comm.). The cartilaginous skeleton of Lepidobatrachus tadpoles is characterized
by a noticeable lateral expansion of the anterior part, including the suprarostral cartilage, lower jaw and anterior part of the palatoquadrate, such that the longitudinal axis of the palatoquadrate, which is nearly parallel to
the neurocranium axis in the generalized chondrocrania, it reaches an angle 50 in these larvae. The quadratocranial commissure appears as a bar almost perpendicular to the chondrocranium axis and longer than the
subocular bar (Ruibal & Thomas 1988; Lavilla & Fabrezi 1992; Wild 1997b; this study). Despite the visible
shape differences revealed by ordination techniques, some skeletal and muscular characters support the clade
composed of Ceratophrys, Chacophrys and Lepidobatrachus, such as the absence of spicules and the complete fusion of infrarostrals and suprarostrals (Lavilla & Fabrezi 1992; Wild 1997b; 1999; Haas 2003). Fabrezi
(2004) and Wild (1999) analyzed these ceratophryine genera in a context of heterochronical processes and
stressed characters that, although intergenerically variable, develop before, or faster than in remaining
anurans. Additionally, Fabrezi (2006) presented a geometric morphometrics analysis of adult skulls and lower
jaws of ceratophryines compared to numerous anuran species. In the ordination plots, ceratophryine species
diverge from most of the other species (Chacophrys, less evidently), with shape changes associated with
developmental patterns of peramorphosis. The placement of Ceratophrys near the generalized morphology

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species, in the chondrocranium ordination of the present study (Fig. 73), supports the idea presented by Fabrezi (2006), according to which, the set of cranial distinctive features of ceratophryines appears after metamorphosis.
Finally, one last group that diverges includes the analyzed microhylids and pipids. As regards microhylids, most of the exotrophic species described (with the exception of Scaphiophryne, Otophryne, and
Hoplophryne Noble 1929; Wassersug 1984; Wassersug & Pyburn 1987) have only minor differences in their
skeletons, and the list of common characters is profuse. A very distinctive feature is the presence of the posterolateral and subotic processes of the palatoquadrate (Wassersug 1989; Haas 2003). Among species in the
present study, the main difference is the presence of a ventrolateral process of the palatoquadrate, well-developed and long in Elachistocleis bicolor, unlike Chiasmocleis panamensis and Dermatonotus muelleri where it
is scarcely visible or absent (see also Lavilla 1992; Lavilla & Langone 1995; Vera Candioti 2006b). Haas
(2003) considered this process, also present in Gastrophryne carolinensis and Hamptophryne boliviana
(Wassersug & Hoff, 1982; De S & Trueb 1991; Haas 2003), to be a synapomorphy of South American microhylids; however, Chiasmocleis and Dermatonotus are not included in the species analyzed by this author. The
presence of a well-developed crista parotica, as an irregular, partially fenestrated cartilaginous plate extending
between the otic capsule and the posterior palatoquadrate, is also variable. Among species described, it is
present in D. muelleri, G. carolinensis, H. boliviana, Hypopachus barberi, Kaloula pulchra, and O. pyburni
(Sokol 1975; 1981; Wassersug & Pyburn 1987; De S & Trueb 1991; Lavilla 1992; Haas 2003; this study) and
absent in E. bicolor, C. panamensis, Microhyla ornata, Uperodon systoma, and apparently in Hy. variolosus
(Ramaswami 1940; Starrett 1968; Wassersug & Hoff 1982; Lavilla & Langone 1995; Haas 2003; this study).
Regarding the hyobranchial skeleton, there are no marked intertaxic differences (Gradwell 1974; Sokol 1975;
1981; Wassersug & Pyburn 1987; De S & Trueb 1991; Lavilla 1992; Lavilla & Langone 1995; Haas 1995;
2003). All forms have very voluminous branchial baskets occupying more than 70% of the total hyobranchial
area, with ceratobranchials with numerous, anastomosed lateral projections, lateral processes ventrally
expanded, and a long, thin urobranchial process (excepting in O. pyburni, S. madagascariensis and Dyscophus antongilii Wassersug 1984; Haas 2003). De S and Trueb (1991) mentioned differences in basihyal
shape, the presence and relation of the pars reuniens with ceratohyals, and the presence of hypobranchial
plates and spicules.
Regarding pipids, the chondrocranium and hyobranchial skeleton of filter feeding species are very similar,
with some minor differences. Pipa carvalhoi and P. parva differ from Xenopus laevis and Silurana tropicalis
in the absence of the basibranchial and of the expansive flat chondrification of the crista parotica, and the
presence of a continuous subocular bar (Sokol 1977; Haas 2003). Additionally, in P. carvalhoi, there is no differentiation into Meckels and infrarostral cartilages in the lower jaw (Haas 2003). Hymenochirus and
Pseudhymenochirus skeletons are very different from those of the other pipid larvae, particularly in the hyobranchial apparatus configuration. Some features, such as the huge ceratohyals and basibranchial and the
reduced branchial basket, have been related to their predaceous habits (Sokol 1962; 1977); this issue will be
further discussed in a following section. Tadpoles of Rhinophrynus, which along with Pipidae integrate the
extant Pipoidea, share several skeletal features with pipids, such as the fusion of the suprarostral cartilages
and trabecular horns, the extended crista parotica, and the processus lateralis posterior in the subocular bar.
Some differences are the basibranchial, indistinguishable from hypobranchial plates, the presence of a long
and thin urobranchial process, and the absence of craniobranchial commissures (Swart & De S 1999; Haas
2003). The continuity of cartilage between the suprarostrals and the trabecular horns in basal anurans, and the
homology between infrarostral plus Meckels cartilages of anuran and Meckels cartilage of salamanders and
caecilians, together with the expression of the gene zax (related to bapx1-gene, which regulates jaw joint
development) in a region corresponding to the infrarostral cartilage in X. laevis, has led Svensson and Haas
(2005) to hypothesize that supra- and infrarostral cartilages (exclusive to anuran tadpoles) stem from the evolution of new articulations within preexisting cartilages, rather than novel cartilage condensations.

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Musculature. Compared to the skeletons, information about anuran tadpole musculature is very scarce. Even
then, it is possible to observe that interspecific variation is not so marked as in the cartilaginous skeleton, and
several differences among species are due to relative muscle development, and less frequently to presenceabsence of muscles or changes in their origin and insertion sites.
The species of Chaunus, Phyllomedusa and Scinax, Hypsiboas rosenbergi, Physalaemus santafecinus,
and Telmatobius cf. atacamensis have a similar muscular configuration, with some differences in mm. l. m.
lateralis, l. m. externus, mandibulolabialis, subarcuales recti, subarcualis obliquus, interhyoideus posterior,
and diaphragmatopraecordialis. The general arrangement of muscles is, furthermore, frequently constant
within genera.
Chaunus tadpoles in this study share a m. mandibulolabialis composed of a single slip, both of mm. l. m.
externus superficialis and profundus, and m. l. m. lateralis present, m. subarcualis rectus I constituted by three
slips, mm. levator arcuum branchialium IV and tympanopharyngeus almost non- distinguishable, mm. interhyoideus posterior and diaphragmatopraecordialis absent, and a peculiar disposition of m. subarcualis rectus
II-IV, where some lateral fibers insert caudally into the distal region of the ceratobranchial IV. Chaunus marinus have the same muscular configuration (Haas 2003). Most characters are also maintained at family level
(Sedra 1951; Starrett 1968; Carr & Altig 1991; Haas 2001; 2003), and the absence of the m diaphragmatopraecordialis and the configuration of the m. subarcualis rectus II-IV have been proposed as a synapomorphy
of Bufonidae by Frost et al. (2006).
Physalaemus santafecinus tadpoles show some differences regarding Chaunus spp.: the mm. interhyoideus posterior and diaphragmatopraecordialis are present, and the mm. subarcuales recti and tympanopharyngeus have a different configuration. In P. santafecinus, even though m. subarcualis rectus I has three slips, the
ventral2 slip does not reach the branchial process III, but inserts near the ventral1 slip, on the branchial process
II. Haas (2003) coded P. biligonigerus in his matrix, assigning it the two slips state. Unlike Chaunus spp., m.
subarcualis rectus II-IV shows a rather typical disposition, and the fiber slip identified as the m. tympanopharyngeus is clearly distinguishable from the m. levator arcuum branchialium IV.
Among hylids, Scinax spp. and Hypsiboas rosenbergi possess a m. mandibulolabialis composed of two
slips, mm. l. m. externus superficialis and profundus, interhyoideus posterior, and diaphragmatopraecordialis
present, m. subarcualis rectus I formed of two slips, m. subarcualis obliquus with insertions in branchial processes II and III, and fibers of the m. tympanopharyngeus inserted anteriorly to the glottis, near the opposite
muscle. Scinax boulengeri and H. rosenbergi share in addition the presence of m. l. m. lateralis. Compared to
other taxa described, most hylids have these features. The m. mandibulolabialis with two slips is found in all
hylid species studied (Carr & Altig 1991; Haas 2003), except for Dendropsophus ebraccatus, which in that
single trait bears a closer resemblance to the D. microcephalus group tadpoles. The mm. l. m. externus superficialis and profundus are present as well in all species revised. The mm. interhyoideus posterior and diaphragmatopraecordialis are also present in most hylids (Haas 2003; Alcalde 2005), and the impossibility of
finding them in Dendropsophus species I studied might be due to an overall poor development of branchial
muscles in these small tadpoles, which would make necessary an histological analysis. The configuration of
the m. subarcualis rectus I is variable among hylines, and there also appears to be some intraspecific variation.
In some species, the muscle is composed of three slips, inserted on ceratobranchials I, II and III, respectively
(e.g., Hyla cinerea, Smilisca baudinii Haas 2003); in some cases, two slips converge in their insertion on the
same ceratobranchial (e.g., Hypsiboas pulchellus, H. andinus, H. raniceps, Scinax nasicus, S. squalirostris
Alcalde 2005). Finally, some species have only two slips, inserted on the ceratobranchials I and II, or I and III
(e.g., Aplastodiscus perviridis, Hypsiboas rosenbergi, Scinax boulengeri, S. ruber, Trachycephalus resinifictrix Haas 2003). The m. subarcualis obliquus inserting on ceratobranchials II and III, with a clearly bifurcated shape, is common among hylines, and some species have both this and the alternative state of a single
insertion, e.g., S. nasicus, Hyla annectans, Smilisca baudinii (Haas 2003; this study). Finally, the m. l. m. lateralis appears in larval stages of hyline studied by Alcalde (2005) and Haas (1996a; 2001; 2003), and its

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absence in S. nasicus can be consequence of a later appearance. Unlike the remaining hylines studied, Hypsiboas rosenbergi shows a m. rectus cervicis with two insertions, on ceratobranchials III and IV. This condition
is shared with H. raniceps, belonging to the H. albopunctatus species group (Alcalde 2005). In Phyllomedusa
species, the m. mandibulolabialis invades the upper lip, but the division into slips is not as clear as in Scinax
spp. and Hypsiboas rosenbergi (in H. pulchellus, the division is evident as well; pers. obs.). As in hylines,
mm. l. m. externus superficialis and profundus, l. m. lateralis, and mm. interhyoideus posterior and diaphragmatopraecordialis are present, and the m. subarcualis rectus I is constituted by two slips. The m. subarcualis
obliquus is different, however, with a single insertion on the ceratobranchial II. Finally, the m. tympanopharyngeus, although clearly distinguishable from the m. l. a. b. IV, does not reach the region anterior to the glottis, as in Scinax and Hypsiboas. The species of Phyllomedusinae studied by Starrett (1968), Carr and Altig
(1991), Haas (1996a; 2003), and Alcalde (2005), coincide in all these characters.
Lastly, Telmatobius larvae apparently differ from the former species due the distinctive pattern of muscles
inserting on the diaphragm. As already mentioned, I could not detect mm. interhyoideus posterior and diaphragmatopraecordialis in T. cf. atacamensis, but there are two very conspicuous muscles in T. ceiorum specimens (fixed with Bouins solution, instead of formaline). The lateral slip corresponds to the m. interhyoideus
posterior; the medial slip could be interpreted as a second slip of the m. interhyoideus posterior, or as the m.
diaphragmatopraecordialis, which, instead of running caudally and inserting on the wall of the abdominal cavity, it runs anteriorly to insert near the articular process of the palatoquadrate; a third option would be consider
this slip as a whole different, unknown muscle. Haas (2003) described two morphological patterns for mm.
interhyoideus posterior and diaphragmatopraecordialis. In most species, muscles meet in a smooth arch that
encircles the peribranchial chamber. In most ranids, hyperoliids, rhacophorids, Megophrys, Pelobates, and
Odontophrynus, the muscles are adjoined in connective tissue anterior to the heart, in an angled orientation.
Telmatobius ceiorum tadpoles appear to have a third pattern, characterized by a muscle running anteriorly to
insert in connective tissue near the articular process of the palatoquadrate. Histological sections and development studies would be needed to assess the identity and homologies of this muscle, as well as its presence in
other Telmatobius species. As regards the remaining muscular features, preliminary personal examination of
T. ceiorum, T. laticeps, T. oxycephalus, T. pinguiculus, T. pisanoi, T. scrocchii, T. stephani, and T. sp. from La
Rioja (Argentina) revealed similar traits, such as mm. levator mandibulae lateralis, externus superficialis and
profundus present, and m. subarcualis rectus I formed of two slips. Additionally, some specimens of most species (excepting T. atacamensis and T. pinguiculus, but maybe because a few individuals were analyzed) show
a configuration of the m. subarcualis rectus IIIV similar to that typical of bufonid tadpoles, i.e., a thin slip
that diverges laterally invading the fourth branchial septum. Published information about musculature of this
genus is very scarce. There are no significant differences regarding the description of Telmatobius sp. by Palavecino (1999), and Carr and Altig (1991) reported the absence of m. mandibulolabialis in Telmatobius sp.
Other species have peculiar muscular configurations. For example, Dendropsophus tadpoles and Lysapsus
and Pseudis species show a unique disposition of the m. l. m. lateralis, between the articular process and nasal
sac, and an also divergent arrangement of the m. subarcualis rectus II-IV, with anterior and posterior slips
(Haas 1996a; 2003; Vera Candioti 2004; Vera Candioti & Haas 2004; Vera Candioti et al. 2004; Alcalde &
Barg 2006). Dendropsophus tadpoles, identical to each other, differ from Lysapsus and Pseudis spp. in the
mm. mandibulolabialis (1 vs. 2 slips; excepting P. cardosoi Alcalde & Barg 2006), subarcualis rectus I (2 vs.
3 slips), and subarcualis obliquus (2 vs. 1 insertion; excepting P. minutus Alcalde & Barg 2006). The m.
tympanopharyngeus of L. limellum was misidentified in Vera Candioti (2004), confused with an internal slip
of the m. levator arcuum branchialium IV (Alcalde & Barg 2006). However, this muscle (defined according to
Haas 2003) is present in Lysapsus tadpoles in this study, so its absence, reported by Alcalde and Barg (2006),
renders this character variable within the species.
Ceratophryine tadpoles also have unusual muscular configurations. Ceratophrys cranwelli larvae from
this study lack mm. quadratoangularis and suspensoriohyoideus (unlike Palavecino 1999 tadpoles), and have

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single mm. mandibulolabialis and subarcualis rectus I. This condition is shared by C. ornata (Haas 2003),
excepting the two slips of the m. subarcualis rectus I in this latter species. Haas (2001; 2003) also mentioned
for C. ornata the presence of the m. l. m. lateralis; since this muscle can appear late in development, the situation could be explained by ontogenetic variation among the tadpoles studied. On the other hand, Lepidobatrachus llanensis larvae resemble those of L. laevis, given the presence of m. submentalis and the absence of
mm. mandibulolabialis, suspensoriohyoideus and quadratoangularis. The presence of m. l. m. lateralis
reported by Haas (2003) in L. laevis may result from ontogenetic differences among analyzed larvae. Both of
ceratophryine genera share the absence of mm. suspensoriohyoideus, quadratoangularis, interhyoideus posterior, and diaphragmatopraecordialis, all of which characters are proposed as synapomorphies for the group by
Haas (2003).
Microhylids species studied show similar muscular features, yet they differ from other anuran tadpoles.
Haas (2001; 2003) revised an eight species sample, and he found a number of constant characters (most of
them, excepting Scaphiophryne tadpoles): m. mandibulolabialis inserting in the infrarostral cartilage; mm. l.
m. longus and internus originated anterior to subocular fenestra; single m. l. m. externus; m. l. m. lateralis
absent; mm. intermandibularis and interhyoideus attached to a central zone of connective tissue, in a distinctive X-shape manner; m. interhyoideus posterior well-developed and extensive; m. geniohyoideus with a diffuse origin near the thyroid gland; compact and hard to differentiate muscles of the angular complex (not in O.
pyburni Wassersug & Pyburn 1987); m. suspensoriohyoideus posteriorly originated; m. subarcualis rectus
II-IV lateralis present; and mm. tympanopharyngeus and diaphragmatopraecordialis absent. All these features
appear in microhylids analyzed in this study. As regards m. subarcualis rectus I, the microhylids revised by
Haas (Elachistocleis bicolor included) possess 1 or 2 slips (1 in Paradoxophyla palmata and Phrynomantis
bifasciatus). In this study, E. bicolor and Chiasmocleis panamensis have a third slip, very long and thin, that
reaches the branchial process. The m. suspensoriohyoideus, as mentioned, has a very posterior origin in
microhylids, and in some of them (E. bicolor, Kaloula pulchra, Gastrophryne carolinensis, and Hamptophryne boliviana Haas 2003), it reaches the ventral region of the otic capsule. In C. panamensis, Dermatonotus muelleri and the remaining species studied by Haas (Dyscopus antongilii, Ph. bifasciatus, S.
madagascariensis, Pa. palmata), the m. suspensoriohyoideus originates on the posterior part of the ventral
side of the posterolateral process. The m. levator arcuum branchialium III has an unusual disposition in the
three species analyzed. It is formed of two portions that cross in a distinctive manner, the medial portion lying
on the lateral portion, and then inserting laterally, below the posterolateral process. Haas (2003) described the
same for G. carolinensis and H. boliviana, and suggests that this crossing is synapomorphic for neotropical
microhylids. Finally, D. muelleri, like some species mentioned by Starrett (1968), has a single m. l. m. longus,
without division into superficialis and profundus slips.
Finally, pipids tadpoles show a peculiar combination of muscular characters, and distinctive features are
the absence of m. constrictor branchialis IV, and the disposition of the m. subarcualis rectus II-IV. According
to Sokol (1975), this latter muscle, along with the mm. constrictor branchiales, forms a sphincter around the
second and third branchial slits. Tadpoles of Silurana tropicalis, Pipa carvalhoi and P. parva show almost
identical characteristics to those of Xenopus, the only difference being the single m. levator mandibulae longus in Pipa (Sokol 1977; Haas 2003). The musculature of Hymenochirus tadpoles is also similar, except for
the branchial muscles; some of these muscles are absent (two mm. levatores arcuum branchialium, two mm.
constrictores branchiales, m. subarcualis rectus II-IV), apparently in correlation with the reduction of the ceratobranchials (Sokol 1962; 1977). Like in pipids, Rhinophrynus dorsalis shows a medial insertion of the m.
levator arcuum branchialium IV, and an anterior position of the jaw levator muscles. This species, however,
lacks the m. geniohyoideus, shows a plesiomorphic configuration of the m. subarcualis rectus II-IV, and has a
m. levator mandibulae externus superficialis (Haas 2003).
Regarding the relative development of mm. interhyoideus and orbitohyoideus, Table 30 shows the ratios
of the nineteen species considered in this study. These results bear an overall similarity to those found by Satel

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and Wassersug (1981) for related species. The three microhylids and Xenopus laevis show the highest values,
as in Satel and Wassersug (1981), and the lowest values are those of Dendropsophus microcephalus, D. nanus
and Lepidobatrachus llanensis. Among generalized tadpoles, the highest values are those of Phyllomedusa
spp. and Scinax boulengeri, whereas the lowest belong to Telmatobius cf. atacamensis and Pseudis paradoxus.
TABLE 30. Ih/oh values (mm. interhyoideus and orbitohyoideus) in tadpoles of 19 species. Species list has been reorganized in order to highlight the uniformity of values within RWA groups.
ih/oh
Chiasmocleis panamensis

1.81

Dermatonotus muelleri

1.24

Elachistocleis bicolor

1.40

Xenopus laevis

1.64

Chaunus arenarum

0.35

Chaunus spinulosus

0.43

Hypsiboas rosenbergi

0.35

Lysapsus limellum

0.44

Phyllomedusa hypochondrialis

0.50

Phyllomedusa sauvagii

0.61

Physalaemus santafecinus

0.38

Pseudis paradoxus

0.26

Scinax boulengeri

0.56

Scinax nasicus

0.45

Telmatobius cf. atacamensis

0.21

Ceratophrys cranwelli

0.25

Dendropsophus microcephalus

0.06

Dendropsophus nanus

0.15

Lepidobatrachus llanensis

0.13

Oral apparatus and buccopharyngeal cavity. The literature describing the oral apparatus and
buccopharyngeal cavity of tadpoles is profuse, allowing intra- and interspecific comparisons. The results of
this study show the existence of a group of similar species, and some taxa that diverge from this generalized
morphology.
Oral apparatuses and buccal cavities are alike in Chaunus spp., Hypsiboas rosenbergi, Lysapsus limellum,
Phyllomedusa spp., Physalaemus spp., Scinax spp. and Telmatobius cf. atacamensis. All of these species show
an oral disc with keratinized, serrated rostrodonts, rows of keratodonts arranged in a 2/2 2/4 disposition, and
a continuous or interrupted papillar margin. Buccal roofs and floors have a variety of structures, papillae,
ridges, pustules in varied numbers and extent of development, choanae, buccal pockets, and dorsal and ventral
vela of varied configurations. Differences and similarities among species are commented below.
Chaunus species have in common an oral disc lined by large marginal papillae, interrupted by dorsal and
ventral gaps, with scarce submarginal papillae, and keratodonts arranged according the LTRF 2(2)/3. Buccal
roofs in both species studied show a conspicuous prenarial ridge, accompanied by prenarial arena papillae,
well-developed lateral ridge papillae, and buccal roof arena papillae bilaterally arranged. The buccal floor
shows the distinctive presence of a pair of non-keratinized, anteromedially directed spurs, not reported in previous descriptions (Fiorito de Lpez & Echeverra 1989; Fabrezi & Vera 1997; Ulloa Kreisel 2003). Spurs are

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frequent in several families, and to date, they have been mentioned in hylids, leptodactylids, ranids, and dendrobatids (Wassersug 1980; Wassersug & Heyer 1988; Faivovich 2002; Vera Candioti et al. 2004). Both
Chaunus species studied also coincide in the number of infralabial and lingual papillae, 2 and 4 respectively.
Finally, the ventral velum is well-developed, with marginal projections regularly placed. Chaunus schneideri
tadpoles have similar characters (Fabrezi & Vera 1997; Ulloa Kreisel 2003). Chaunus dorbignyi, C. fernandezae, and C. pygmaeus tadpoles (from the C. granulosus group) show a different oral disc, with a LTRF 2(2)/
2 (Echeverra 1998; Borteiro et al. 2006). Keratodont morphology in C. spinulosus coincides with that
described for C. arenarum (Fiorito de Lpez & Echeverra 1984; 1989), and Echeverra (1998) reported more
cusps and more dense keratodonts in C. fernandezae. It is to be noted that some species formerly placed in
Bufo (like Chaunus as well), show some differences with other bufonids. For instance, Bufo scitulus (now
Rhinella) lacks a ventral gap, and Bufo divergens (now Ingerophrynus) possesses only two lingual papillae
(Inger 1985; Caramaschi & Niemeyer 2003).
Physalaemus santafecinus have a combination of features usual in other species within the genus, and
descriptions in this study agree with those by Perotti and Cspedez (1999). The oral disc, with dorsal gap and
2 lower labial ridges is similar to that of P. biligonigerus (Perotti & Cspedez 1999). A third tooth ridge and a
ventral gap appear in P. albonotatus, P. cuqui, P. cuvieri, P. fernandezae, and P. henselii tadpoles (Vizzoto
1967; Cei 1980; Fabrezi & Vera 1997; Kolenc et al. 2006). As regards the buccopharyngeal cavity, some features are homogeneous within the genus, e.g., the prenarial ridge and large postnarial papillae. Variable characters are the number of lingual papillae, 1 in P. santafecinus and P. biligonigerus, 3 in P. cuqui, and 4 in P.
petersi and P. pustulosus (recently assigned to the revalidated genus Engystomops by Nascimento et al. 2005),
the number of buccal floor arena papillae, and the shape of the median ridge (Wassersug & Heyer 1988; Fabrezi & Vera 1997; Perotti & Cspedez 1999; Ulloa Kreisel 2003).
Among the species analyzed, Telmatobius cf. atacamensis have more numerous and denser filtering structures in the sample analyzed. Lavilla (1983b) studied Telmatobiinae species, and found that the oral discs of
Telmatobius spp. lack constrictions in the lateral margins, a frequent condition in the subfamily. In most of the
cases, Telmatobius species from the highlands of Argentina differ from the northern taxa in having ventral
submarginal (intramarginal) papillae. Regarding the buccal cavity, T. cf. atacamensis share with other Argentinean (T. ceiorum, T. laticeps, T. oxycephalus, T. pinguiculus, T. pisanoi, T. scrocchii, T. stephani, and T. sp.
from La Rioja), and Peruvian species (T. arequipensis, T. breviceps, T. carrillae, T. culeus, T. marmoratus, and
T. rimac) the barely naked prenarial arena, two lingual papillae, 4 infralabial papillae, 34 main pairs of postnarial papillae, prepocket papillae, buccal arenas with large and dense papillae, groups of papillae lateral to
the buccal roof arena, and the general configuration of the ventral velum (Wassersug & Heyer 1988; Ulloa
Kreisel 2003; Aguilar & Pacheco 2005; pers. obs.). Telmatobius jelskii differs in having a third lingual papillae (Wassersug & Heyer 1988), but this could be just an anomaly. Additionally, Telmatobius species have a
couple of small, bicuspidate keratinized spurs, located posteriorly to the infrarostrodont (Wassersug & Heyer
1988; pers. obs.).
Lastly, most of studied hylids share a generalized oral morphology. Hypsiboas rosenbergi differs from
remaining taxa, firstly in having 4 lower labial ridges in its oral disc. This deviation from the typical 3-row
pattern has been reported for other Hypsiboas from the same and different groups, e.g., H. boans, H. crepitans, and H. rufitelus (4 rowsDuellman 1970; Wassersug 1980), H. geographicus and H. semilineatus (56
rowsDHeursel & De S 1999), among others. Regarding the buccal cavity, there is a broad variation. Some
variable characters are the number of infralabial papillae (1 pair in H. pulchellus; 2 in H. geographicus and H.
semilineatus; 3 in H. rosenbergi; 8 in H. rufitelus), and the prenarial arena configuration, either naked or with
ridges or papillae (small pustules in H. pulchellus and H. andinus; ridges and papillae in H. rosenbergi, H.
geographicus, and H. semilineatus; a small ridge in H. rufitelus Wassersug 1980; DHeursel & De S 1999;
Vera Candioti 2000; Ulloa Kreisel 2003). Most of species have 1 pair of lingual papillae, postnarial papillae,
and very ornamented choanae, with a narial valve and pustules or papillae in their margins. In H. rosenbergi,

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as in H. rufitelus, the anterior wall of choanae forms large vacuities with high, thick, pustulate walls (Wassersug 1980). Suctorial tadpoles formerly known as Hyla mixe present numerous differences with remaining species, such as numerous keratodonts rows (7/10, 7/11), an enormous proliferation of distinctively arranged
buccal floor papillae, and a conspicuous massive cone-like structure in the prenarial arena (Wassersug 1980).
These tadpoles are currently assigned to a new genus, Megastomatohyla (Faivovich et al. 2005). Finally, at
microanatomical level, Hypsiboas pulchellus keratodonts, studied by Echeverra (1992) and Vera Candioti
(2000) also have a scarcely marked body, a slightly convex head, and fewer cusps (1012 vs. 1214) than in
H. rosenbergi. Other species formerly named Hyla have very different configurations, and they will be discussed later, together with Dendropsophus microcephalus and D. nanus.
Scinax species analyzed show some differences in their oral discs. Scinax nasicus possesses the typical
oral apparatus, similar to that described for S. eringiophilus, S. fuscovarius, S. squalirostris, among others
(Echeverra & Montanelli 1992; Echeverra 1997a; Faivovich 2002). Scinax boulengeri, like other related tadpoles (S. garbei, S. rostratus, S. pedromedinae, S. sugillatus Duellman 1970; 1978; Duellman & Wiens
1993; Hero & Mijares-Urrutia 1995) has a structure named labial arm by McDiarmid & Altig (1990), i.e., a
modification of the last keratodonts row. In the cladistic analysis of the genus, recently presented by Faivovich
(2002), this group of species consolidates with several synapomorphies besides the presence of labial arm,
e.g., ventral gap present and spurs absent (spurs absent also in species of the S. catharinae clade Kolenc et
al. 2007). Scinax acuminatus is the closets related species, and also shares with S. boulengeri the keratodont
morphology, infrequent within the genus: unicuspidate, spike-like vs. rounded, convex head, with numerous
marginal cusps, characteristic of other species (S. eringiophilus, S. fuscovarius, S. nasicus Echeverra &
Montanelli 1992; Echeverra 1997a; Sandoval 2000; Vera Candioti 2000; Vera Candioti et al. 2004; this
study). Regarding the buccal cavity, features appear to be relatively constant within the genus, with 1 pair of
lateral ridge papillae, postnarial papillae, scarce or absent papillation on the buccal roof, 1 pair of infralabial
papilla, and absence of lingual papillae, among others (Echeverra & Montanelli 1992; Echeverra 1997a;
Sandoval 2000; Vera Candioti 2000; Ulloa Kreisel 2003; Vera Candioti et al. 2004).
Buccal features in Lysapsus and Pseudis tadpoles are very similar to each other and regarding previously
described species; however, some differences are evident. The oral disc is alike in all of the forms, excepting
P. paradoxus tadpoles described by Bokermann (1967), which present a third upper keratodonts row. In general terms, buccal papillation is scarcer in Lysapsus than in Pseudis species (Rada & Bello 1988; De S &
Lavilla 1997; Ulloa Kreisel 2003; Vera Candioti 2004). The number of infralabial papillae varies among 0, 2
and 4 (P. paradoxus, L. limellum, and P. minutus, respectively); lingual papillae are generally 2 (excepting P.
minutus, with 3); buccal roof papillae are scarce in L. limellum and P. minutus, and very numerous in P. paradoxus, which also has the highest number of buccal floor papillae.
Phyllomedusinae species have oral discs with a well-developed papillar margin, and keratodonts arranged
in a LTRF 2(2)/3(1). These traits are shared by Pachymedusa dacnicolor, Agalychnis callidryas, A. annae, and
Hylomantis lemur, studied by Duellman (1970). Distinctive features of the buccal cavity are the prenarial
arena ridge, postnarial papillae, 1 pair of lateral ridge and lingual papillae, and well-developed, secretory dorsal and ventral vela. Such features are also found in P. boliviana, P. trinitatis and A. callidryas (Kenny 1969;
Wassersug 1980; Ulloa Kreisel 2003). Agalychnis callidryas tadpoles have in addition, one pair of small keratinized spurs, placed caudally to the infrarostrodont (Wassersug 1980).
Microhylids tadpoles have highly variable configurations of oral apparatus and buccopharyngeal cavity.
The oral apparatus is defined by the absence of keratinized structures, excepting Scaphiophryne species and
Otophryne pyburni (Wassersug 1984; Wassersug & Pyburn 1987; Haas 2003; Glos et al. 2005). Donnelly et
al. (1990) revised morphological variation among microhylid free-living tadpoles: in the upper lip there may
be a couple of flaps, supported by the suprarostral cartilage, pending and concealing the lower lip, or such
flaps may be absent (e.g., in Nelsonophryne aterrima, Dasypops schirchi, Kaloula borealis); the lower lip
may have varied shapes, and even be accompanied by papillae (e.g., in N. aterrima, Microhyla zeylanica, M.

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okinavensis); finally, the lower lip may be well-developed and upturned, constituting an umbelliform structure
(in M. achatina and M. heymonsi). The buccopharyngeal cavity has a uniform morphology in numerous species, with a papilla or ridge within the prenarial arena, unperforated choanae with a large papillar projection
emerging from the posterior margin, prepocket papillae, lingual and lateral ridge papillae absent, buccal roof
and floor almost naked, with tall papillae bilaterally disposed on both sides of the glottis, and exposed glottis,
located between the two halves of the well-developed ventral velum (Savage 1955; Gradwell 1974; Inger
1985; Wassersug 1980; Chou & Lin 1997). The three species analyzed in this study have upper labial flaps
and a naked, spatulate lower lip. Inside the buccal cavity, some differences are the number of papillae posterolateral to the choanae (4 in Dermatonotus muelleri, and 2 in Elachistocleis bicolor and Chiasmocleis panamensis), and in Dermatonotus, more buccal floor arena papillae. Results in this study coincide with former
descriptions in Echeverra and Lavilla (2000) and Ulloa Kreisel (2003). There are some nomenclature discrepancies in the literature regarding prenarial, postnarial, and lateral ridge papillae in microhylids. Wassersug
(1976) referred to small, posteriorly directed projections at the anterolateral corner of the choanae as prenarial
papillae; thus, papillae of microhylids are not prenarial papillae (as in Echeverra & Lavilla 2000) but prenarial arena papillae. Postnarial papillae are located within postnarial arena, and even when they are not associated with the narial walls, Wassersug (1976) maintained the equivalent name; thus, large structures projecting
from the posterior margin of the unperforated choanae in microhylids are not postnarial papillae (as in Echeverra & Lavilla 2000 and Vera Candioti 2006b) but a structure probably homologous to the narial valve projections of other tadpoles (Wassersug 1980). Finally, papillae projecting from the posterolateral edge of the
choanae are not lateral ridge papillae (as in Echeverra & Lavilla 2000 and Vera Candioti 2006b) but structures related to the internal nares (Wassersug 1980). Some tadpoles of Microhyla described by Wassersug
(1980) and Chou and Lin (1997) show, at first glance, very different configurations; however, some common
features are still recognizable, e.g., lingual and lateral ridge papillae absent, prepocket papillae, tall papillae
on both sides of the glottis, unperforated choanae with a large projection (in the case of M. heymonsi and M.
berdmorei, a tongue-like flap), and a glottis anteriorly located. Otophryne pyburni and S. calcarata also have
some of these traits, such as lingual papillae absent, anterior glottis, a palp-like structure projecting from the
posterior margin of the unperforated choana (Wassersug 1984; Wassersug & Pyburn 1987).
All pipid tadpoles are devoid of keratinized structures in their oral apparatuses. Pipa, Xenopus and Silurana have a simple, transverse slit-like opening, and the two latter species share the presence of long barbels
in the commissures. The oral apparatuses of Hymenochirus and Pseudhymenochirus are protrusible, funnellike, with a rounded, dorsal opening. Xenopus laevis and Silurana tropicalis show a very similar configuration
of their buccopharyngeal cavity. Pipa tadpoles differ by having dorsal vela with thick tentacles having numerous gland cells, and by lacking ventral velum. Hymenochirus lacks any filtering structure inside the buccopharyngeal cavity (Sokol 1962; 1977; Wassersug & Rosenberg 1979).
A group of taxonomically related and unrelated tadpoles possesses oral apparatuses and buccopharyngeal
cavities different from the generalized pattern. Among studied larvae, Ceratophrys cranwelli is characterized
by a very conspicuous oral disc, with scarce marginal papillae, well-developed, strong infrarostrodont, and
numerous keratodonts rows. As regards the buccopharyngeal cavity there are 3 pairs of infralabial papillae, 1
pair of lingual papillae, and overall sparse papillation on the buccal roof and floor (Ulloa Kreisel 2003; this
study). All these characteristics are shared by C. aurita (Wassersug & Heyer 1988). Lepidobatrachus llanensis tadpoles have some similar features, such as oral papillae, infralabial papillae (only 1 pair in L. llanensis)
and overall reduced papillation, absent on the buccal roof (Ulloa Kreisel 2003; this study). Lepidobatrachus
laevis has comparable traits, excepting the presence of 3 lingual papillae and 1 pair of papillae in the region of
buccal pocket (Wassersug & Heyer 1988). Regarding the unusual rostrodonts of Lepidobatrachus spp., Altig
(2006) suggested that the spike-like structures may be hypertrophied serrations with the sheath lacking or
minimally developed and thus may be further evidence of a developmental relationship between rostrodonts,
papillae, tooth ridges and labial teeth.

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Finally, Dendropsophus nanus and D. microcephalus lack keratodonts and oral papillae, and the oral
apparatus is defined by a protrusible U-shaped oral tube. The buccal cavity is characterized by the scarcity of
papillae and ridges, more pronounced in D. nanus, in which the sole structures to be found are a couple of globose infralabial papillae (Vera Candioti et al. 2004). This condition has also been verified in other tadpoles of
the same and closely related groups, such as D. phlebodes, D. ebraccatus, D. saracuayensis (Wassersug
1980), and to a lesser extent, D. minutus (Echeverra 1997b).
Interspecific variation. Diet
Analyses of tadpole diet are scarce in the literature (a review appeared in Alford 1999 and Hoff et al.
1999). This kind of analysis implies some methodological difficulties which render the results and further
conclusions hard to generalize. Firstly, quantification is bound to be biased in favor of those identifiable,
intact, and large enough items. A case in point was the analysis of Chiasmocleis panamensis larvae, in the
course of which it was impossible to identify and quantify food items in the digestive tract. Secondly, variation in food availability, plus the wide distribution of several species, determines that a tadpole sample, significant at a statistical level, may not be so at species level. In this study and in the literature in general, tadpoles
of each species come from the same pond, and it is arguable how constant the results in other water bodies and
locations may be. Thirdly, as widely acknowledged by several researchers, gut content analysis is only an
approximation to diet, since it does not provide per se an idea about what of the material that is captured actually constitutes the diet, i.e., what part of what is ingested is digested and assimilated (Altig et al. 2007; R.
Altig, pers. comm.). It is necessary then, to keep in mind that this report is circumstantial, and by no means a
comprehensive record of what tadpoles can effectively do. On the other hand, qualitative composition of diet
(with taxonomic identification of food items) may be generally not very informative, being subject to environmental and temporal variations. This has consequences for the interspecific variation analysis. If the species
studied were collected in different water bodies or dates, a low overlap in diets may be due to such sampling
variation. Conversely, if the species have been collected in the same place and date, it is probable that the
overlap will be high, because of high resource availability in the environment. Additionally, as Inger (1986)
pointed out, an accurate or loose taxonomic identification of quantified food items can result in overlapping
values lower or higher, respectively. Several studies report that there exists no differentiation in trophic niche,
but only in space and time (e.g., Heyer 1976; Lajmanovich 1998). However, some authors find low overlapping values among some species, and differential selection of certain food types (Steinwascher & Travis 1983;
Taylor et al. 1995; Rossa-Feres et al. 2004).
Diet studies generally coincide in that, except for some specialized forms (e.g., Crump 1983; Lanoo et al.
1987; Deban & Olson 2002; Vera Candioti et al. 2004), tadpoles are mainly phytophagous, consumers of
microalgae, debris, and vegetal remnants, whereas zooplankton and animal matter in general, are less frequent
in gut contents (e.g., Daz-Paniagua 1985; 1989; Lajmanovich 1994; 1997; 1998; Lajmanovich & Fernndez
1995; Vera Candioti & Lajmanovich 1998; Vera Candioti 2000; Arias et al. 2002; Rossa-Feres et al. 2004;
Dutra & Callisto 2005). However, this may be a consequence of the quantitative methodology employed in
the cited studies. Quantification of food items is usually made through numeric frequencies, or frequencybased importance indexes, which tend to overestimate the contribution of small food particles appearing in
high amounts, in detriment of larger items that despite of their low numeric frequency, may more strongly
contribute to feeding (Hyslop 1980). Thus, zooplankton components, which are often larger and in lower frequencies in freshwater environments when compared to microalgae (in a more general frame, the ecological
size scaling factor; e.g., Margalef 1980; Dickie et al. 1987; Rodrguez 2005), may result underestimated, thus
leading to erroneous conclusions. Petranka and Kennedy (1999) provided two more explanations about why
invertebrate contribution to diet may be higher than suggested, regarding the collective effect of dense tadpoles assemblages, diluted in a per capita analysis, and to rapid gut clearance rates in anuran tadpoles in general.

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Table 21 shows the contribution of each food-category in the species considered in this study. Rather than
infrequent, animal food-categories often accumulated higher percentages than the vegetal fraction. This interpretation renders the carnivorous-herbivorous dichotomy artificial and dependent on a strict definition of
terms. If the zooplankton ingestion makes a diet carnivorous (as it does, even when one would tend to consider carnivory something more spectacular), then most of the species in this study are as carnivorous as herbivorous. The species where the vegetal material was highly significant are Chaunus spinulosus,
Dermatonotus muelleri, Elachistocleis bicolor, Phyllomedusa spp., and Scinax boulengeri. However, far from
indicating a preference for such a regime, these cases can be explained simply in terms of environmental
availability and tadpole opportunism. For instance, in the case of C. spinulosus, the gut content almost completely composed of diatoms is surely due to oligotrophy in the water body where the tadpoles were collected
(a Prepuna lotic environment). In P. sauvagii, D. muelleri, and S. boulengeri, the abundance of vegetal material is linked to algae blooms at the collection site (Volvocales, euglenoids, filamentous chlorophytes, respectively; pers. obs.). On the other hand, in microhylids and phyllomedusines, the preponderance of vegetal
material can also be linked to the size of food particles, which are in general terms, smaller than that of animal
material. When the said tadpoles ingest a large proportion of very small food items, the distribution of sizes
biases toward the smallest sizes, and secondarily, toward vegetal material. On the other hand, in tadpoles of
Ceratophrys cranwelli, frequently referred to as carnivores, approximately half the volume of their gut contents is represented by colonial algae. These results, where animal matter is significant in diets, agree with
Savage (1952), Nathan and James (1972), Steinwascher and Travis (1983), Kupferberg (1997), and more
recently Schiesari (2004 cited in Altig et al. 2007), Hunte-Brown (2006), and Whiles et al. (2006) studies,
who also pointed out that the ingestion of animal food items would have a positive effect on growing rates in
anuran larvae.
TABLE 21. Proportions of food types in tadpoles of 18 species. Matrix appears transposed. nq, non-quantifiable. Species
as in Fig. 1.
Ca
Cyanophytes

Cs

Cc

Lll

Ta

Dm

Dn

Hr

Ll

Ph

Phs

Pp

Sb

Desmids

0.56

0.01

0.21

0.20

3.23

6.73

0.07

0.10

0.80

Diatoms

41.39 99.33

0.03

0.01

9.36

0.35

0.01

2.60

26.7

49.57

0.51

1.26

Sn

Ps

Drm

0.20

Eb

Xl

3.96

0.52 15.12 0.17

21.1

15.63 9.66

0.01

21.9

0.04

10.41 2.01

0.11

26.3

0.54

Euglenoids

0.01

0.01

1.42

0.67

86.07

Filamentous
chlorophytes

nq

nq

98.51

nq

Unicellular
chlorophytes

1.61

Macrophytes

0.35

1.23

0.21

22.51

3.04

28.76

2.07

5.61

0.3

Volvocales

45.56

10.5

5.04

99.23 0.73

0.01

10.59

0.78

0.01

TOTAL
VEGETAL
FRACTION

41.95 99.33 46.17

Ciliates

37.28

Crustaceans

0.63

Insects

Nematods
Oligochaetes
Rotifers
Tadpoles

25.11 41.88 65.04 86.65 30.13 99.31 28.63 32.60 99.52 74.26

15.69

2.6

24.51 12.29

7.69

0.02

49.52

26.9

27.58

81.57

4.20

0.06

0.03

0.04

0.57

16.96

1.22

3.56

0.03

0.44

0.04

2.34

0.89

87.70

Tecamebians

0.19

0.05

0.11

0.08

0.01

4.55

TOTAL
ANIMAL
FRACTION

58.05

0.67

96.81 99.96

0.07

0.67

68.90

0.14

0.01

4.54

15.93

0.13

0.08

0.02

23.5

7.05

0.14

0.77

11.84 13.07

53.83 99.99 89.41 99.23 99.99 74.89 58.12 34.96 13.35 69.84

ANATOMY OF ANURAN TADPOLES

0.47

2.19

8.43

97.6

34.38 12.30 0.01


0

46.47

0.12

0.49

0.69

19.60 2.52
0

17.38 6.00

9.61

0.18

7.21

71.36 67.40 0.48 25.74 97.81

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The application of a different methodology renders these results barely comparable with most of the previous literature. Quammen and Durtsche (2003) studied the diets of Chaunus americanus, Pseudacris crucifer
and Rana sylvatica tadpoles, through volume-based quantification, and find that in the three species, diets are
mainly composed of debris and diatoms, and in the case of R. sylvatica, a significantly different proportion of
invertebrates.
As regards prey-sizes, Heyer (1973) and Inger (1986) suggested that there does exist a partitioning among
species. Conversely, among taxa analyzed by Rossa-Feres et al. (2004), there was no significant difference
among sizes of particles ingested. In species analyzed in this study, food items sizes are within a highly variable range. Table 22 shows that a group of species consume mainly ( 50%) food particles representing <1
5% of the body size (Chaunus spp., Dermatonotus muelleri, Elachistocleis bicolor, Hypsiboas rosenbergi,
Lysapsus limellum, Xenopus laevis, and Phyllomedusa spp.). In Physalaemus santafecinus, Pseudis paradoxus, Scinax spp. and Telmatobius cf. atacamensis, higher percentages are between 720% of the body size.
Ceratophrys cranwelli shows two modes on sizes <4% and 20% of the body. Finally, in Dendropsophus
nanus, D. microcephalus, and Lepidobatrachus llanensis the more frequently consumed food size exceeds
90% of the tadpole body. These groups are also inferred, in general terms, from ordination analysis of Figure
76.
TABLE 22. Proportions of food sizes in tadpoles of 18 species. Matrix appears transposed. Species as in Fig. 1.
Ca

Cs

Cc

Lll

Ta

Dm

Dn

Hr

Ll

Ph

Phs

Pp

Sb

<1%

22.89

0.01

0.18

0.01

8.55

0.13

3.92

4.30

86.62

1.56

Sn

Ps

Drm

Eb

12.08 13.99 98.14 35.15

Xl
1.61

1%

48.65 24.83

2.68

0.01

1.04

1.00

0.01

25.46 38.02 56.43

0.33

1.46

27.11 19.17

1.50

46.62

0.16

2%

9.85

74.04

5.86

0.01

6.10

0.15

2.63

0.43

13.88

2.41

0.22

8.08

0.60

3%

0.50

12.13

0.02

2.09

1.98

0.01

7.85

10.21

0.20

3.40

11.97

0.05

0.65

15.74

4%

0.02

21.38

1.13

0.01

48.34

6.32

3.19

0.69

17.28

0.26

0.54

0.29

24.89

5%

0.01

14.84

5.88

0.89

9.34

0.61

2.07

3.90

7.51

0.82

10.88

7.87

43.83

6%

0.43

0.04

0.79

8.61

11.20

0.13

6.45

0.47

6.29

1.98

4.32

1.23

13.18

7%

11.53

25.32

2.62

3.96

0.45

3.49

31.89

3.74

0.11

8%

0.60

4.06

0.12

0.72

21.16

21.71

9%

18.03

7.03

3.15

19.61

19.82 22.83

10%

2.92

20%

15.73

52.29 29.00

30%

4.48

50%

6.67

0.50

60%

0.24

70%

2.74

80%

9.07

4.17

90%

14.01

68.02 28.08

1.12

44.51

0.31

0.26

27.65 31.41

3.16

0.57

0.54

0.42

26.64

120%

12.64

130%

33.65

66.09

150%

27.82

Inger (1986) considered three categories of tadpoles from the Bornean rainforest, on the basis of absolute
sizes of food particles consumed: microphagous ( x = 0.0260.05 mm), mesophagous ( x = 0.0690.08
mm), and macrophagous tadpoles ( x > 0.12 mm). However, when creating categories, it is necessary to take
into account predator size, mainly in those cases with a varied sample of species. If Ingers data are reanalyzed, by relativizing food particle sizes to tadpole lengths (tabulated in the paper), it is observed that even in
those tadpoles considered as macrophagous (Leptolalax gracilis and L. montanum), food sizes only reach 1%
of the tadpole body length. Given that food item sizes range is much wider in the present study, a definition of
microphagy vs. macrophagy including the whole spectrum is necessary. This subject will be further discussed
in the next section.

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Finally, as regards the mechanism of food intake, Deban et al. (2001) summarized the modes in amphibians, in a study that includes anurans, urodeles and caecilians. Among tadpoles, these authors recognize three
mechanisms: jaw prehension (biting), which implies grasping of prey between the jaws; suction feeding,
which occurs when a relatively large prey is drawn into the mouth by a single expansion of the buccal cavity;
and finally, filter feeding, which consists of the removal of numerous, small food particles from the water
either by rhythmically repeated buccal expansions that draw water into the mouth, or by moving forward over
the particles. The employed mechanism relates to the size of the food particles to be consumed. In this way,
predators far larger than their prey are usually filter feeders, and the boundary between collecting individual
items (hunting) and filter feeding would be set by benefit-cost considerations (Schoener 1969; 1971; Hespenheide 1973). On the other extreme, some predators accede to prey larger than themselves, by social hunting.
Among the species considered in this study, even when direct observations were not made (excepting Ceratophrys cranwelli), the implicit mechanisms may be inferred from the digestive contents. Tadpoles of Lepidobatrachus and Dendropsophus ingest large, whole prey, and are examples of suction feeding. In the
remaining species, the main mechanism seems to be filter feeding, supplemented by jaw prehension (for
example, when grazing on filamentous algae). Ceratophrys tadpoles show the three mechanisms mentioned
by Deban et al. (2001); they can ingest whole prey, tear them apart if they are too large, and, apparently, given
the large amount of small particles within the digestive contents, these tadpoles are also capable of filter feeding.
Ecomorphological considerations
Generalities. Ecomorphology is the study of relationships of form and environmental factors as an attempt to
isolate the contribution of one to the other (Motta et al. 1995a); it attempts to understand the interrelationships between morphological variation among individuals, populations, species and higher taxa, and communities and the corresponding variation in their ecology (Leisler & Winkler 1985, in Chan 2001). The concept
of ecomorphology refers to any aspect of the phenotype related to bioroles, these understood as biological
roles caused (or mediated) by selection (Szalay 2000). One of the principles of ecomorphology is that morphology restricts resource use, or in other words, morphological design limits the ability of organisms to perform tasks. Thus, an ecomorphological approach has a certain prediction capacity in one sense or the other
(i.e., form from function, and function from form). Bock and Von Wahlert (1965) set up the theoretical basis
for ecological morphology (later, ecomorphology), and defined terms such as form, function, biological role,
and adaptation (Winkler 2002).
In anuran larvae, several studies have contributed to interpret the correlation among external and internal
morphology and developmental modes, diet, and microhabitat (e.g., Noble 1929; Wassersug & Hoff 1979;
Wassersug 1980; Satel & Wassersug 1981; Altig & Johnston 1989; Haas & Richards 1998; Hall et al. 2002;
Van Buskirk 2002; Alcalde & Rosset 2003; Vera Candioti & Haas 2004; Vera Candioti et al. 2004; Dayton et
al. 2005; Vera Candioti 2005). The concept of ecomorphology is closely related to phenotypic plasticity and
character displacement concepts, according to which, some morphological characters are susceptible to
change in certain environmental conditions, hypothetically in response to several pressures. In tadpoles, this
subject is now being explored, particularly in relation to predation, competence, physical-chemical conditions,
and diet, and those phenomena are proposed as mediators of species divergence (e.g., Pfennig & Murphy
2000; 2002; Vences et al. 2002; Storz 2004).
Some issues need to be clarified prior to carrying out an analysis of the correspondence between tadpole
trophic ecology and morphology. To begin with, how are micro- and macrophagy to be defined? In literature
reviewed, although two different feeding processes (microphagy and macrophagy) are referred to, definitions
are only implicit. One of the usages refers to the absolute size of food particles, for instance, in the already
commented paper by Inger (1986), where a Bornean tadpole assemblage is studied and classified into three
categories, corresponding to three food size ranges. As mentioned, the problem with this definition is that it is

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not applicable to samples with very heterogeneous predator sizes, because a certain food particle can render a
small tadpole a macrophagous form, yet constitute a tiny item to a larger larva. A second alternative is to consider as part of a microphagous diet all of those particles whose trajectory inside the tadpole includes an obligatory way through branchial filters, and those particles going directly to oesophagus as part of a
macrophagous diet. In this case, the boundary between food item sizes in both processes depends on the spacing of filtering and trapping structures, which can vary ontogenetically and interspecifically (Kenny 1969;
Wassersug 1980). This definition appears to be the most accurate, but it requires detailed observations of the
destination of each particle in each case, and this is not regularly carried out in studies, including the one presented here. A third definition, implicit in some works and related to the second, refers to food intake, and it
contrasts suspension-feeding to macrophagy (e.g., Wassersug 1975; 1980; Petranka & Kennedy 1999). When
applying this definition, it is necessary to register the mechanism involved in the intake of each particle, and
this mechanism also depends on the relative size of the food item (i.e., how large a food item should be as to
the predator can detect it and individually pursuit it); again, predator size needs to be taken into account. A
possible solution, as implemented in the present work, is to gain operativeness at the expense of losing the
accuracy of a functional definition: first, to relativize food size to certain measurements indicative of tadpole
size (e.g., chondrocranium length, body length, ratios between them). This was already employed by Emerson
(1985), in analyzing the relation between cranial morphology and diet in adult anurans. Once the range of
food sizes is obtained, categories can be defined, by some manner independent from morphological characters; otherwise, the circularity is obvious and further investigations on diet-morphology relationship lack any
sense. In this study, a possible categorization that makes compatible the resulting sizes range (Table 22) and
the ordination of species according to gut content (Fig. 76) would be: microphagous species, those ingesting
food particles below 1% of the tadpole body size; macrophagous species, those ingesting food particles larger
than 50% of the body size. The term mesophagous is reserved for the species ingesting sizes between the
mentioned extremes, since the more commonly used term generalists would refer to an ability to consume
particles of both of the extremes. Among tadpoles studied, there seems to be an incipient segregation between
those species consuming food particles within 19% of the body size, and within 1030% (Fig. 76). It would
be worth noting that a conclusive assignation of species to each category must be done after an adequate ontogenetic variation study; such study was not carried out in this work, thus the discussion derived is applied in
principle to the stages analyzed. Additionally, although categories are, by definition, uninterchangeable, i.e.,
non-overlapping, the placement of tadpoles is not so, rather, it is based on the food sizes they more frequently
eat, and this does not prevent other sizes from appearing in their diet. In fact, Table 22 shows that those species with the narrowest ranges are Dermatonotus muelleri (<12% of the body), followed by Phyllomedusa
spp., Elachistocleis bicolor, Xenopus laevis, Hypsiboas rosenbergi, Scinax nasicus, and Chaunus spp. (<1
10% of the body), whereas Ceratophrys cranwelli, S. boulengeri, Telmatobius cf. atacamensis, Pseudis paradoxus, Physalaemus santafecinus, and Lysapsus limellum have wider ranges (<130, and up to 50% of the
body). In Dendropsophus microcephalus, D. nanus and Lepidobatrachus llanensis, percentages of small food
items are very low (less than 2%).
Another aspect to be considered when trying to link feeding habits with morphological characters is a
consistent definition of generalized morphology, including its level of application (e.g., oral, skeletal, muscular levels, all of them). If generalized implies frequent, then one would be led to imagine a tadpole with
an oral disc, serrated rostrodonts, LTRF 2/3 (according to Altig & Johnston 1989 present in 51% of the
species they studied), buccopharyngeal cavity with varied filtering and trapping structures, hyobranchial skeleton with a ceratobranchial area occupying 50% of the total area, and hypobranchial area smaller that the ceratohyal, and buccal floor raising musculature less developed than the depressor musculature, in a proportion
1:2, such as several species of Chaunus, Leptodactylus, Hyla, Scinax, etc. This is an accurate and somewhat
strict definition, but it is its strictness that allows detection of differences among species. In the paper by
Petranka and Kennedy (1999), where generalized tadpoles are suggested to be capable of macrophagy, some

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of the species included are notably divergent from the general features mentioned, and the authors do not provide the definition on which they have ground their study. For instance, Dendropsophus minutus tadpoles
have an oral apparatus ad buccopharyngeal cavity different from other hylines, with reduced or absent structures (Echeverra 1997b). Hoplobatrachus occipitalis tadpoles show an oral disc with well-developed rostrodonts, with dentiform projections, and noncusped keratodonts comparable to those of Ceratophrys cranwelli,
Leptobrachium spp. and Spea bombifrons (Inger 1986; Altig & McDiarmid 1999a; Grosjean et al. 2004; Vera
Candioti 2005). The hyobranchial skeleton of congeneric tadpoles of Hoplobatrachus tigerinus was studied
by Khan (2003), and shows large ceratohyals and a reduced branchial basket, like several macrophagous species. On the other hand, items such as rotifers, included in the paper, may hardly be considered to be part of a
macrophagous diet, particularly for large tadpoles. All these comments by no means invalidate Petranka and
Kennedys conclusions; most of the cases they present, do support the argument of macrophagy coupled with
generalized morphology, and the authors experimentally prove the ability of Rana spp. tadpoles for attacking
and consuming large items relative to their sizes. The purpose here is only to insist on the lack of precise definitions, and a clear context for addressing the discussion on tadpoles feeding mechanisms.
Diet-morphology relationship. From all the aforementioned in the section about interspecific variation, most
chondrocranial characters, musculature configuration (in terms of presence-absence and trajectory of muscles), and the amount of filtering structures inside the buccal cavity appear not to have an unequivocal relation
to food sizes. Muscular characters, related to presence-absence and trajectories of muscles, are maintained
within genera, and even at a suprageneric level. The lack of relation with trophic ecology can be seen, for
example, in that species phylogenetically linked and having different feeding habits, such as the Dendropsophus microcephalus group species and the former pseudines, show a similar muscular configuration. Regarding buccal filtering structures, the observed patterns seem to be in most cases a product of common historical
processes as well. As several authors have suggested, in some cases anatomy reflects mainly inherited characters, and morphological designs are flexible enough so as not to require modifications linked to specific ecological habits (e.g., Gans et al. 1985; Gans & De Vee 1987; Abdala & Moro 1996). In Dendropsophus spp.
and ceratophryines, a convergent pattern of reduction and absence of filtering structures is observed, in this
case, linked to the ingestion of large food particles.
Results of the CCA indicate that the size of the branchial basket, the ih/oh ratio and mouth gape width are
the morphological variables most related to food size distribution. When phylogeny is taken into account
(pCPO), mouth gape width explains a significant, phylogenetically independent percentage of the prey-size
variation. The hyobranchial apparatus configuration (branchial basket size and ih/oh ratio) is correlated with
phylogeny, since the phylogenetically independent percentages they explain are small and nonsignificant.
Regarding phylogeny, only the genus Dendropsophus is significant in prey-size ordination, and it explains a
percentage of variation that is not correlated with the morphological variables considered. The variance
shared by phylogeny and morphology indicates that the variation attributable to historical processes contains
an ecomorphological component (Giannini 2003), related, in this case, to hyobranchial apparatus configuration. According to Figure 77, four groups of tadpoles in the food size-morphology relationship space would
appear:
Elachistocleis bicolor + Dermatonotus muelleri. These species share the lowest values in the first relative
warp of the hyobranchial skeleton, i.e., a highly developed branchial basket and reduced hypobranchial area,
along with the highest ih/oh values and large mouth gape width. They ingest mainly items that represent <1%
of the body size. They are microphagous feeders with a microphagous-like morphology.
Chaunus spp. + Phyllomedusa spp. + Scinax spp. + Hypsiboas rosenbergi + Lysapsus limellum + Physalaemus santafecinus + Pseudis paradoxus + Telmatobius cf. atacamensis + Xenopus laevis. These species share
intermediate values on the first relative warp of the hyobranchial skeleton, and high on the second, i.e., a branchial basket occupying 4050% of the total, and ceratohyals not laterally expanded, with similar distances
among their processes. The in/oh ratios and mouth gape width also have intermediate values. Food item sizes
vary within 130% of the body length. They are microphagous and mesophagous feeders with a generalized
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morphology. Xenopus tadpoles location in this group is explained by the small amount of prey-sizes <2% of
the tadpole length.
Dendropsophus nanus + D. microcephalus + Ceratophrys cranwelli. These species share the highest values
on the first relative warp of the hyobranchial skeleton, i.e., a highly reduced branchial basket, robust ceratohyals and hypobranchial plates, low ih/oh values, and a small (Dendropsophus) or intermediate (Ceratophrys)
mouth gape width. They ingest mainly food particles of 50% the body size. They are macrophagous feeders
with macrophagous-like morphology.
Lepidobatrachus llanensis. This species shows intermediate values on the first relative warp of the hyobranchial skeleton, and the lowest on the second, i.e., a branchial basket occupying 4050% of the total area,
and laterally expanded ceratohyals, with a long distance between anterior and anterolateral processes. The ih/
oh ratio is low, as in the former group. Mouth gape width is the largest in the sample, approximately 65% of
the tadpole body length. Food sizes associated to this morphology exceed 70% of the tadpole body length.
This species is a macrophagous feeder whose morphology differs from the other three groups; i.e., a megalophagous-like morphology.
Groups formed in the ordination of hyobranchial skeletons generally remain unchanged after the inclusion
of more species in the analysis (Vera Candioti 2006a). Figure 78 shows the ordination resulting from the RW
analysis of the species in the present study, and a set of 42 species obtained from literature, representative of
several guilds proposed by McDiarmid and Altig (1999). The guilds included, and the species representing
them are as follows: arboreal tadpoles: Anotheca spinosa and Hoplophryne rogersi; benthic tadpoles: Chacophrys pierotii, Dendrobates tinctorius, Leptodactylus chaquensis, L. gracilis, L. labyrinthicus, L. podicipinus, Melanophryniscus orejasmirandai, and Scaphiopus intermontanus; carnivorous tadpoles: Ceratophrys
cornuta, Hoplobatrachus tigerinus, Hymenochirus boettgeri, Lepidobatrachus laevis, Leptodactylus pentadactylus and Spea bombifrons; clasping tadpoles: Boophis sp. and Leptobrachium hasselti; exoviviparous tadpoles: Rhinoderma darwinii; gastromyzophorous tadpoles; Chaunus chrysophorus and Atelopus tricolor;
nektonic tadpoles: Pseudis minutus, Scinax acuminatus and Trachycephalus venulosus; neustonic tadpoles:
Phasmahyla guttata; nidicolous tadpoles: Cycloramphus stejnegeri, Eupsophus calcaratus and Flectonotus
goeldii; paraviviparous tadpoles: Gastrotheca christiani; fossorial tadpoles: Leptobrachella mjobergi, macrophagous tadpoles: Occidozyga laevis; psammonic tadpoles: Otophryne pyburni; suctorial tadpoles: Ascaphus truei, Heleophryne natalensis, Litoria nannotis and Nyctimystes dayi; suspension feeding tadpoles:
Gastrophryne carolinensis, Kaloula pulchra, Microhyla ornata, and Rhinophrynus dorsalis; suspensionrasper tadpoles: Phyllomedusa boliviana (Ridewood 1898; Noble 1929; Wassersug & Hoff 1979; Lavilla
1987; 1991; Wassersug & Pyburn 1987; Ruibal & Thomas 1988; Fabrezi & Lavilla 1992; Haas 1995;
1996a,b; 2003; Fabrezi & Vera 1997; Lavilla & Vaira 1997; Wild 1997a; 1999; Haas & Richards 1998; Hall &
Larsen 1998; Larson & De S 1998; Lavilla & De S 1999; 2001; Swart & De S 1999; Khan 2003; Larson et
al. 2003; Vera Candioti et al. 2005; Haas et al. 2006). A second RWA with only 10 landmarks in the hyobranchial skeleton was performed, in order to include the four species with reduction in ceratobranchials (Atelopus
tricolor, Chaunus chrysophorus, Hoplophryne rogersi and Hymenochirus boettgeri). The results are very similar to those of the previous analysis, and the four species have been added to the 16-landmarks-based RW
plot, showing their putative location. A discriminant analysis on the shape variables of the 61 species resulted
in four significantly different groups, in both 16 landmarks and 10 landmarks-analyses (Wilks < 0.02; p <
0.0001 in both cases; Fig. 79). Rhinophrynus dorsalis was misclassified, and then included within microhylids
and Xenopus group (p = 0.99). A redundancy analysis (RDA) was performed on the discriminant scores and a
phylogenetic matrix (Giannini 2003), to explore the significance of taxonomic groups in the pattern of hyobranchial morphology discriminant analysis. Microhylids excluding Otophryne, and Ceratophrys + Chacophrys are the only two significant groups for the discriminant ordination, and account for about 29% and
8% of the total variance (p 0.001 in both 16 and 10 landmarks-based analyses; Figure 80). Rhinophrynus +
Xenopus clade is significant in the 16 landmarks analysis (p < 0.001), but not in the 10 landmarks analysis,
where Hymenochirus is included.

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FIGURE 78. RWA of the hyobranchial skeletons of tadpoles of 19 species from this study (SET1, N = 58), plus 38 species from literature (SET2, N = 38). The four underlined species have reduction in number of ceratobranchials, and were added after a 10-landmarks-based RWA (SET1, N = 58; SET2, N = 42). SET1: CA Chaunus arenarum, CC Ceratophrys cranwelli, CP Chiasmocleis
panamensis, CS Chaunus spinulosus, DM Dendropsophus microcephalus, DN Dendropsophus nanus, DRM Dermatonotus muelleri,
EB Elachistocleis bicolor, HR Hypsiboas rosenbergi, LL Lysapsus limellum, LLL Lepidobatrachus llanensis, PH Phyllomedusa hypochondrialis, PHS Phyllomedusa sauvagii, PP Pseudis paradoxus, PS Physalaemus santafecinus, SB Scinax boulengeri, SN Scinax
nasicus, TA Telmatobius cf. atacamensis, XL Xenopus laevis. SET 2: AS Anotheca spinosa, AT Ascaphus truei, ATT Atelopus tricolor, BX Boophis sp., CCO Ceratophrys cornuta, CHC Chaunus chrysophorus, CHP Chacophrys pierotii, CYS Cycloramphus stejnegeri, DT Dendrobates tinctorius, EC Eupsophus calcaratus, FG Flectonotus goeldii, GC Gastrophryne carolinensis, GH
Gastrotheca christiani, HN Heleophryne natalensis, HOR Hoplophryne rogersi, HT Hoplobatrachus tigerinus, HYB Hymenochirus
boettgeri, KP Kaloula pulchra, LC Leptodactylus chaquensis, LG Leptodactylus gracilis, LH Leptobrachium hasselti, LLB Leptodactylus labyrinthicus, LLV Lepidobatrachus laevis, LM Leptobrachella mjobergi, LN Litoria nannotis, LP Leptodactylus pentadactylus,
LPO Leptodactylus podicipinus, MO Microhyla ornata, MOJ Melanophryniscus orejasmirandai, ND Nyctimystes dayi, OL Occidozyga laevis, OP Otophryne pyburni, PG Phasmahyla guttata, PHB Phyllomedusa boliviana, PM Pseudis minutus, RD Rhinoderma
darwinii, RDO Rhinophrynus dorsalis, SA Scinax acuminatus, SCI Scaphiopus intermontanus, SPF Spea bombifrons, TV Trachycephalus venulosus, XL Xenopus laevis.

FIGURE 79. Discriminant analysis on the scores of RW from 16-landmarks-based (A, N = 96), and 10-landmarks-based (B, N = 100)
analyses of hyobranchial skeletons of anuran tadpoles (four groups significantly different: Wilks 0.001, p < 0.001; Wilks
0.008, p < 0.001, respectively). According to probabilities of group membership, Rhinophrynus dorsalis (arrow) was misclassified,
and then assigned to group 3 (p = 0.99).

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FIGURE 80. Phylogenetic hypothesis for Anura based in Frost et al. (2006) and Donnelly et al. (1990), employed for phylogenetic
canonical ordination method (Giannini 2003). Significant monophyletic groups are shaded (p < 0.001 in all cases).

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As observed, Occidozyga laevis, Ceratophrys cornuta, Leptobrachella mjobergi, and Anotheca spinosa
tadpoles are placed near Dendropsophus nanus, D. microcephalus and C. cranwelli. Gastrophryne carolinensis, Kaloula pulchra, Microhyla ornata, and Xenopus laevis place with Elachistocleis bicolor, Chiasmocleis
panamensis, and Dermatonotus muelleri. Lepidobatrachus laevis integrates itself with L. llanensis. A large
group of species distributes among and marginally in the generalized species group. Hoplobatrachus tigerinus, Hoplophryne rogersi, Hymenochirus boettgeri, Boophis sp., Eupsophus calcaratus and Nyctimystes dayi
are located in the extreme near the macrophagous group. Otophryne pyburni and Rhinophrynus dorsalis are
placed between Xenopus and the generalized morphology group. The location of Atelopus tricolor and Chaunus chrysophorus, near Lepidobatrachus spp., can be associated to the expanded ceratohyals of both species,
related to the belly sucker. The four groups thus formed are considered, nominated as follows:
macrophagous morphology tadpoles: Anotheca spinosa, Ceratophrys cranwelli, C. cornuta, Dendropsophus microcephalus, D. nanus, Leptobrachella mjobergi and Occidozyga laevis.
megalophagous morphology tadpoles: Lepidobatrachus laevis and L. llanensis.
generalized morphology tadpoles: Ascaphus truei, Atelopus tricolor, Boophis sp., Chaunus arenarum, C.
chrysophorus, C. spinulosus, Chacophrys pierotii, Cycloramphus stejnegeri, Dendrobates tinctorium, Eupsophus calcaratus, Flectonotus goeldii, Gastrotheca christiani, Heleophryne natalensis, Hoplobatrachus tigerinus, Hoplophryne rogersi, Hymenochirus boettgeri, Hypsiboas rosenbergi, Leptobrachium hasselti,
Leptodactylus chaquensis, L. gracilis, L. labyrinthicus, L. pentadactylus, L. podicipinus, Litoria nannotis,
Lysapsus limellum, Melanophryniscus orejasmirandai, Nyctimystes dayi, Otophryne pyburni, Phasmahyla
guttata, Phyllomedusa boliviana, P. hypochondrialis, P. sauvagii, Physalaemus santafecinus, Pseudis minutus, P. paradoxus, Rhinoderma darwinii, Scaphiopus intermontanus, Scinax acuminatus, S. boulengeri, S.
nasicus, Spea bombifrons, Telmatobius cf. atacamensis, and Trachycephalus venulosus.
microphagous morphology tadpoles: Chiasmocleis panamensis, Elachistocleis bicolor, Dermatonotus
muelleri, Gastrophryne carolinensis, Kaloula pulchra, Microhyla ornata, Rhinophrynus dorsalis and Xenopus
laevis.
Considering this morphological patterns, and taking into account qualitative information on trophic ecology of the species taken from literature, a general characterization of the mentioned groups is discussed.
Species conforming macrophagous group are characterized mainly by the reduced size of the branchial
basket, accompanied by developed ceratohyals and hypobranchial plates. Additionally, in-lever arm proportion values are the highest among the tadpoles studied (Table 25; Wassersug & Hoff 1979). The in-lever arm
(ceratohyal lateral portion) is the insertion surface of the m. orbitohyoideus, and in general, the longer it is, the
more developed the muscle (Wassersug & Hoff 1979). Thus, in these species ih/oh values are the lowest
(Table 30; Satel & Wassersug 1981). It is interesting to note that the relation between macrophagy and ih/oh
ratio is not symmetric, i.e., a macrophagous or carnivorous diet cannot be a priori inferred from a developed
m. orbitohyoideus. Storz (2004) pointed out that a change from soft food (such as detritus and algae, in typically omnivorous diets) to harder and active food can affect development of mandibular musculature; this
author cited Pomeroy (1981), who showed that Spea multiplicata tadpoles fed a diet of lettuce have larger m.
orbitohyoideus than tadpoles reared on trout food gelatine cubes. Larson and Reilly (2003) studied the functional aspects of another muscle group, in relation to gill irrigation and feeding in anuran larvae. These
authors (supporting previous observations by Gradwell 1972) mentioned that the mm. levatores mandibulae
(l. m. longus, internus, and externus) and the mm. angularis (hyoangularis and suspensorioangularis) are
active during feeding. Levator muscles are responsible for the adduction of the lower jaw, contributing to a
forceful closing of the mouth. The mm. angularis cause the Meckels cartilage and the infrarostrals to rotate
backward, pulling open the lower jaw and producing a wide mouth opening. I made a preliminary calculation
of levator and angular muscle development for the species considered, by estimating volumes from linear
dimensions, and finding the ratio between them. Results show that in this macrophagous morphology tadpoles, mm. angularis are proportionately more developed (levator/angular ratio: C. cranwelli = 1.35; D.
microcephalus = 0.06; D. nanus = 0.09). The larger value in C. cranwelli is due to the fact that mm. levatores
mandibulae longus are also massive.
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Ingestion of large-sized items requires either a large mouth opening and buccal cavity, or a jaw apparatus
capable of tearing the prey apart before engulfing them. The species in the macrophagous group share the fact
that they have achieved a large buccal cavity volume by the enlargement of the buccal floor (Wassersug &
Hoff 1979; Vera Candioti 2005; 2006a). All these tadpoles possess very robust ceratohyals, with a rostrocaudal length greater than that of the hypobranchial plates. Regarding the oral apparatus, configurations are
diverse. Dendropsophus nanus and D. microcephalus have an oral tube, devoid of keratodonts and papillae.
The mouth gape is very small, which coupled with the great development of the buccal floor lowering musculature, allows for the generation of an important suction force at an oral level. The great development of the
jaw abductor muscles indicates that the small oral gape could be increased by a significant lowering of the
lower jaw. In fact, mouth gape width is a rather conservative measurement of mouth opening; Wassersug and
Yamashita (2001) have shown that, at maximum mouth opening, Rana catesbeiana tadpoles can reach a gape
140% the width of the suprarostrodont, which implies an angle of 180 between upper and lower jaws. Occidozyga laevis possesses a narrow upper lip, a protrusible U-shaped lower lip, and although rostrodonts are
present, keratodonts and papillae are absent (Inger 1985; Inthara et al. 2005). Anotheca spinosa has welldeveloped rostrodonts and reduced keratodont rows. Ceratophrys species have an oral disc with developed
rostrodonts and numerous rows of spike-like keratodonts. Buccopharyngeal cavities present an overall reduction or absence of filtering structures (Duellman 1970; Wassersug 1980; Inger 1985; Duellman & Trueb 1986;
Wassersug & Heyer 1988; Vera Candioti 2005; this study). Regarding diet, all of these species are able to
ingest large items relative to their body size, including filamentous macrophytes, oligochaetes, arthropods,
and other tadpoles (Wassersug 1980; Jungfer 1996; McDiarmid & Altig 1999; Vera Candioti 2005). Particles
can be ingested whole, as in the case of oligochaetes consumed by Dendropsophus species. In Ceratophrys,
when certain limit of prey size relative to tadpole size is reached (in my observations, 60% of the tadpole
length), the well-developed keratinized structures in the oral apparatus, along with the strong jaw levator muscles allow for a previous tearing apart of items. The fossorial tadpole of Leptobrachella mjobergi shows some
features similar to that of macrophagous tadpoles, such as the relatively enlarged ceratohyal area, (42% of the
total hyobranchial area), the relatively reduced ceratobranchial area (40%), the absence of filter plates, and a
particular insertion pattern of the m. rectus cervicis, which suggests that this muscle might act synergistically
with the m. orbitohyoideus, to generate a large suction force; features such as the numerous papillae on the
buccal floor and buccal roof arenas, with secretory cells, however, point to a microphagous diet (Haas et al.
2006). Data on diet are not conclusive, and Haas and collaborators recommended larger specimen samples
and evaluation of their gut contents to reveal resource use in this species.
The hyobranchial skeleton of Lepidobatrachus species is defined by its great lateral expansion. The branchial basket, although with bar-like ceratobranchials devoid of lateral projections and spicules as in macrophagous tadpoles, is only slightly reduced in area (Table 25). Unlike macrophagous larvae, the large buccal
cavity volume is achieved by widening the whole body. The large lateral extension of the ceratohyals is, in
fact, part of a lateral extension of the anterior and middle chondrocranium. The wide suprarostral and the
lower jaw, both laterally expanded, create a very large mouth opening. The lateral extension of palatoquadrates and ceratohyals, in turn, yield a large buccal volume. This implies that prey can be not only exceptionally large (nearly equal to the predator size), but also engulfed intact. The ceratohyal lateral portion is short,
unlike that of macrophagous tadpoles (Table 25). However, the m. orbitohyoideus is well-developed, and its
insertion site extends to the anterior margin of the quadratocranial commissure. This results in a low ih/oh
ratio, similar to that of macrophagous larvae. The lower jaw abductor muscles are well developed (levator/
angular ratio: 0.14), which allow for a wide mouth opening, enormous per se. Conversely, the jaw adductor
muscles are scarcely developed, and this, along with the weak keratinized oral structures, would limit the possibility of tearing the prey apart before ingestion. Regarding the oral apparatus and buccal cavity, traits are like
those in most macrophagous tadpoles, with reduced oral papillation and keratinized structures, and barely
present filtering structures in the buccal roof and floor. Additionally, Lepidobatrachus tadpoles, like macroph-

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agous Dendropsophus nanus, have short intestines, a frequent trait in carnivores ( 3.5 times the body length
Ulloa Kreisel 2003; Vera Candioti et al. 2004). As shown, Lepidobatrachus species diverge from other
macrophagous feeders in relation to some different morphological features, and even when at first glance food
item size seems insubstantial, an explanation is in order. Table 22 shows that Dendropsophus nanus may consume oligochaetes that represent 130% of its own size, whereas for L. llanensis size is slightly larger, being
150% of tadpole size. This difference is in fact minimized as a result of having worked with prey lengths
instead of volumes; an oligochaete may be longer than the body of D. nanus, but its diameter is minute,
whereas a tadpole, besides being longer than the body of L. llanensis, it is proportionately wide and high.
Once corrections are made, it becomes apparent that an oligochaete represents 3.5% of D. nanus body volume, and a tadpole at least 15% of Lepidobatrachus body volume. The prey volume consumed by D. nanus
and D. microcephalus is constrained by their small buccal gaps, whereas in L. llanensis, the notable mouth
gape width allows for ingestion of prey of significantly greater volume (Ruibal & Thomas, 1988; this study).
This justifies keeping the term megalophagy (as coined by Ruibal & Thomas 1988) for Lepidobatrachus tadpoles feeding.
Most of species integrate the generalized morphology group, characterized by hyobranchial skeletons
with branchial baskets occupying approximately 50% of the total area (Table 25), and a hypobranchial area
smaller than the ceratohyal area. The in-lever arm proportion among studied species is x = 0.32, agreeing
with reports in Wassersug and Hoff (1979). The ih/oh ratio has also intermediate values ( x = 0.41), as commented by Satel and Wassersug (1981). Most of species, moreover, have a generalized oral apparatus, with
marginal papillae, rostrodonts, and keratodonts arranged in 2 upper and 3 lower rows. Wassersug and Yamashita (2001) provided an interesting explanation on what this type of oral disc allows and restricts during rasping
feeding: keratinized structures, together with cartilaginous pieces and underlying ligaments, supply a kinetic
flexibility that determines rapid and efficient responses to shape and resistance irregularities of the substrate
surfaces; such flexibility, however, restricts the kind of food to be consumed, hindering the generation of
strong suction pressure at jaw level. Prey sizes that appear associated with all of these features are frequently
in the range of 130% of tadpole size.
Within this group of generalized morphology, it is possible to detect a general trend toward a greater
development of the branchial basket, from the extreme near macrophagous group, to the extreme near
microphagous group. This tendency can be associated with a decreasing gradient of food particle size and
water flow speed. The macrophagous extreme gathers some non-feeding, fast water, and carnivorous species (e.g., Eupsophus calcaratus, Boophis sp., Hoplobatrachus tigerinus). The resemblance between hyobranchial skeletons of suctorial and macrophagous tadpoles has already been reported, and it is explained by the
fact that both larvae types generate strong negative pressures inside their buccal cavities, either to adhere to
the substrate, or to capture and retain large prey (Wassersug & Hoff 1979; Haas & Richards 1998; Vera Candioti et al. 2004). On the other hand, like macrophagous tadpoles, endotrophic larvae do not depend on an efficient filtering mechanism to obtain their food, and some of them have relatively reduced branchial baskets as
well (Lavilla 1991; Haas 1996b; Vera Candioti et al. 2005). Excluding the endotrophs, species in this extreme
have macrophagous diets. Hoplophryne rogersi feeds mainly on arthropods, vegetal remnants, and anuran
eggs (Noble 1929). Hymenochirus boettgeri pursuits and ingests prey such as microcrustaceans, mosquito larvae, and small tadpoles (Sokol 1962; Deban & Olson 2002). Haas and Richards (1998) reported the presence
of intact ephemeropterans in the gut contents of Boophis sp. Finally, Hoplobatrachus spp. tadpoles regularly
prey upon other anuran larvae (Grosjean et al. 2004), and Khan (1997; 2003) remarked that the smallest particle which is filtered on the filter ruffle of H. tigerinus, is the size of small cladocerans and copepods (Daphnia
and Cyclops). The neustonic larvae of Microhyla heymonsi, M. achatina, Colostethus nubicola and Xenophrys
minor, characterized by their umbelliform mouth, could not be included in the analysis of Figure 77, due to
absence of illustrations of their hyobranchial skeletons in literature. Wassersug (1980) mentioned the reduction of the branchial basket of these species, but according to the drawings of the buccal floors, such reduction

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appear not to be as marked as in macrophagous-like morphology. It seems probable that, in an ordination analysis, the mentioned species will locate within the generalized morphology group, in the extreme near macrophagous morphology tadpoles. Regarding diets, Smith (1916) and Heyer (1973) have mentioned the ability
of Microhyla species to ingest large food particles.
In the opposite extreme of the generalized morphology group, near the microphagous group, are species
with low mobility, inhabitants of lentic environments, or slow water microhabitats in lotic environments.
Otophryne pyburni and Phyllomedusa spp. have more developed branchial baskets that those of remaining
species (60% of the total hyobranchial area). Furthermore, Phyllomedusa species possess the highest ih/oh
ratios in this group. Regarding the buccopharyngeal cavity, the Phyllomedusinae have well-developed and
dense filtering structures (Wassersug 1980; this study). The mentioned forms feed on very small food particles, the smallest within the group in the Phyllomedusa studied (Wassersug & Pyburn 1987; this study). Leptobrachium hasselti (and presumably, other Leptobrachium species as wellInger 1986; Grosjean 2001) is a
mosaic of features, with branchial basket whose development is comparable to that of Phyllomedusinae, and
relatively low ih/oh ratio and oral apparatus with rostrodonts and noncusped keratodonts comparable to those
of some macrophagous tadpoles. The remaining species of the group are nektonic, benthic and neustonic
forms, that feed on small particles (among studied species, sizes 130% of the tadpole size), obtained in varied ways from varied microhabitats.
Finally, microphagous tadpoles possess hyobranchial skeletons with a well-developed branchial basket,
occupying 70% of the total area, and reduced hypobranchial area. The low in-lever arm proportion values
obtained for the species in this study agree with those mentioned by Wassersug and Hoff (1979). These
authors calculated a wide angle of rotation of the ceratohyal during lowering of the buccal floor. This allows
these tadpoles to ingest large water volumes into the buccal cavity, without having to generate a high negative
pressure; this explains, besides, the high ih/oh ratio determined by the poor development of the m. orbitohyoideus. As regards oral apparatus, these species generally lack keratinized structures and oral papillae. The filtering structures inside the buccal cavity are not as abundant and dense as in other tadpoles, and may be even
absent, but this would be balanced by the development and complexity of the food traps. Wassersug and
Rosenberg (1979) studied the morphology of branchial food traps in tadpoles of several species. In microhylids, the food traps form separate plates in the anterior region of the filter cavity, and collecting surfaces are
secretory ridges with secretory zones 12 cells wide. In Xenopus, the ridges are located on the pharyngobranchial tract, and the secretory zone is a single row of secretory cells. Thus, even when at gross anatomical level
food traps of these species are very different, the configuration of ridges is similar, with narrow secretory
zones and shallow troughs between ridges. Agalychnis callidryas shows also a pattern of food traps unusual
for a hylid, with long ridges with secretory zones 13 cells. Most generalized Neobatrachia tadpoles, instead,
show branchial food traps with secretory pits and ridges with secretory zones 46 cells wide. All these observations led Wassersug and Rosenberg to conclude that highly efficient suspension-feeders have branchial food
traps with long, parallel secretory ridges with a narrow secretory zone and shallow troughs between the
ridges.
On the other hand, I could find conspicuous mucus cords only in the digestive tract of microhylids and
Xenopus. In microhylids, the characteristic array of cords, in a double helix, coincides with observations and
explanations by Kenny (1969), for Phyllomedusa trinitatis. According to this author, secretory tissues of ventral and dorsal vela (secretory ridges and secretory pits) produce mucus which agglutinates food particles.
Four mucus cords are formed: three ventral cords, which enter either branchial cavity entangling particles filtered therein, and a dorsal mucus cord, coming from the dorsal velum. All these cords become intertwined in
the oesophagus, forming a main cord on either side, and these, in turn, become mutually twisted about each
other as they pass down to the gut. Wassersug (1972) studied the filtering and entrapping process in Rana tadpoles, and he proposed a mechanism according to which the collecting surface of the ventral velum functions
primarily in causing single small particles to coalesce into larger units. This mechanism involves textural dif-

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ferences in the food trap epithelium, local eddies, and formation of mucus webs and clumps of food particles
that reach the oesophagus. Taking all this information into account, it would seem that in most tadpoles,
mucus entrapment occurs through the mechanism Wassersug (1972) proposed, with formation of clumps of
entangled cells. In Xenopus, microhylids, and to a lesser extent, in phyllomedusines, the peculiar morphology
of the food traps would be related to the formation and transport of conspicuous mucus cords. Furthermore,
some structural differences in secretory ridges in microhylids and Xenopus (e.g., the troughs being far narrower in the latter Wassersug & Rosenberg 1979), could probably account for the differences in their mucus
cords. The main cords in microhylids are two, and the double helix they form is as wide as the oesophagous
lumen. Conversely, Xenopus cords are remarkably thin, although they also appear in intertwined pairs; additionally, the mucus seems to be very dense, since cords remain intact even after the removal and homogenization of the digestive content.
Finally, Wassersug (1972) explored the efficiency of several tadpoles in removing solid particles from a
suspension. Xenopus laevis and Rhinophrynus dorsalis are able to retain the smallest particles (0.126 ), in
comparison to generalized morphology tadpoles (Ascaphus truei and Rana pipiens, 0.557 ). As the author
commented, both the structural differences in secretory ridges, and the chemistry of the mucus, presumably
determine the lower size of the particles which various tadpoles can effectively entrap.
The above commented groups, as already mentioned, are based on what tadpoles usually eat, i.e., the food
size percentages more frequent in gut contents. Although accurate conclusions are only achieved through
experimental studies, an approach to what species are effectively capable of doing, is through the analysis of
ranges of food size consumed and average particle-size, where minimum and maximum values also intervene.
Table 31 shows the percentages of food item sizes, indicating those species with non-generalized morphologies, and minimum and maximum food sizes recorded in each one of them. The categorization into morphological types is effected on the basis of hyobranchial skeleton ordination, which often coincides with what is
indicated by ih/oh ratio, oral apparatus configuration, and to a lesser extent, buccopharyngeal cavity. As
regards large food particles, among the species of generalized and microphagous type studied, neither one
exceeds a prey-size of 30% of the body length. Reviewing the literature, though, several authors mention species with similar hyobranchial skeletons as capable of macrophagy. For instance, Rhinophrynus dorsalis
shows a hyobranchial skeleton with a well-developed branchial basket, and a high ih/oh ratio, as in microhylids (Satel & Wassersug 1981; Swart & De S 1999), and it is either a proficient suspension-feeder or a
zooplankton and tadpoles predator (Starrett 1960; Wassersug 1972; Swart & De S 1999). Orton (1943) and
Swart and De S (1999) attributed the macrophagy of this species to an early formation of the lower jaw cartilages. Likewise, microhylids of the genus Scaphiophryne are reported as bottom-feeders and carnivorous
(Blommer-Schlsser 1975; Wassersug 1984; 1989; Altig & McDiarmid 1999b). As regards generalized morphology tadpoles, Petranka and Kennedy (1999) provided a list of generalized morphology species where
macrophagous diets have been recorded. Most of these species have presumably complete generalized morphology, at skeletal, muscular, buccal and buccopharyngeal levels (e.g., Chaunus spp., Engystomops pustulosus, Pleurodema nebulosa, some Scaphiopus spp., etc.). Other species show some generalized traits coupled
with certain macrophagous-like features. For instance, as already mentioned, Hoplobatrachus spp. and Dendropsophus minutus possess very divergent, macrophagous-like oral apparatuses and buccopharyngeal cavities (Chou & Lin 1997; Echeverra 1997b; Grosjean et al. 2004). Spea spp. carnivorous morphs appear among
generalized morphology tadpoles in the hyobranchial skeletons ordination, but they possess macrophagouslike oral apparatuses and very low ih/oh ratio (e.g., Satel & Wassersug 1981; Pfennig & Murphy 2000; 2002;
Storz 2004). As already mentioned, Petranka and Kennedys paper does not take into account the predator size
to define macrophagy. It remains an open question whether the items tabulated as preys represent a percentage
of the predator length contained in a range similar to 130%, or whether the mechanism of ingestion involves
a previous tearing apart of prey, yielding eatable fragments within the said range. What is clear, from previous
studies and the results of this work, that rather than continuing to consider generalized tadpoles as mainly her-

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bivores and suspension feeders, it would be necessary to rethink the food resources they are able to take in.
This implies a wide variety of behaviors, food types and feeding mechanisms, such as predation on zooplankton, macroinvertebrates, and co- and heterospecific eggs, embryos, tadpoles and metamorphs, among others.
Finally, in macrophagous and megalophagous morphologies, the size of prey ingested whole can increase to
150% of the body length.
TABLE 31. Proportions of food sizes in tadpoles of 18 species. Matrix appears transposed, and species have been rearranged according their morphology. Frequencies = 0 of the extreme of each range have been removed, in order to highlight minimum and maximum food sizes in each species. MIM microphagous morphology, MAM macrophagous
morphology, MEM megalophagous morphology, X average food size, relative to tadpole body length. Species as in Fig.
1.
Mim.

Generalized morphology

Drm Eb

Xl

Ca

Cs

Mam.

Hr

Ll

Ph

Phs

Ps

Pp

0.13

3.92

4.30

86.62 13.99 1.56

Sb

Sn

Ta

Mem.

Cc

Dm

Dn

Lll

12.08 8.55

0.18

0.01

<1% 98.14 35.15 1.61

22.89 0.01

1%

1.50

46.62 0.16

48.65 24.83 25.46 38.02 56.43 0.33

19.17 1.46

27.11 1.04

2.68

1.00

0.01

0.01

2%

0.22

8.08

0.60

9.85

3%

0.65

4%

5%

74.04 6.10

19.82 22.83 0.15

2.41

2.63

0.43

13.88 0.00

5.86

0.00

0.01

0.00

15.74 0.00

0.50

7.85

0.00

10.21 0.20

0.05

0.00

3.40

11.97 2.09

12.13 1.98

0.01

0.02

0.29

24.89 0.00

0.02

48.34 6.32

3.19

0.69

0.54

17.28 0.00

0.26

1.13

21.38 0.00

0.01

0.00

7.87

43.83 0.00

0.01

0.89

9.34

0.61

2.07

10.88 3.90

7.51

0.82

5.88

14.84 0.00

0.00

0.00

6%

1.23

13.18 0.00

0.00

8.61

11.20 0.13

6.45

4.32

0.47

6.29

1.98

0.79

0.43

0.00

0.00

0.04

7%

0.11

0.00

0.00

2.62

3.96

0.45

3.49

3.74

0.00

0.00

31.89 25.32 11.53 0.00

0.00

0.00

8%

0.00

0.60

0.12

0.72

21.71 0.00

21.16 .

0.00

4.06

0.00

0.00

0.00

9%

18.03 .

7.03

0.00

19.61 0.00

3.15

0.00

0.00

0.00

0.00

0.00

10% .

0.00

1.12

0.00

44.51 0.00

2.92

0.00

0.00

0.00

0.00

20% .

0.26

3.16

27.65 31.41 .

52.29 15.73 29.00 0.31

0.00

30% .

0.42

0.54

26.64 .

4.48

0.00

0.57

0.00

50% .

6.67

0.00

0.50

0.00

60% .

0.00

0.24

0.00

70% .

0.00

0.00

2.74

80% .

0.00

4.17

9.07

90% .

68.02 28.08 14.01

120% .

0.00

130% .

66.09 33.65

150% .

12.64

27.82

0.5% 1.3% 4.4% 2.4% 1.8% 3.3% 3.1% 1.7% 1.2% 5.5% 11.3% 16.7% 3.4% 13.0% 11.1% 67.5% 118% 123%

In the extreme of the smaller food sizes there appears to be no distinction between minimum food sizes in
microphagous and generalized tadpoles. This is surely due to the fact that particles that mark the difference
between those species able to retain them and those which are not, are much smaller. The experimental studies
by Wassersug (1972) showed that the three species he studied, Ascaphus truei, Rana pipiens and Xenopus laevis, are capable to clear a solution with particles of 0.557 , i.e., almost 10 times smaller that the smallest food
item I measured in the digestive contents. Xenopus laevis and Rhinophrynus dorsalis are able to retain minute
particles of 0.126 . This could explain also the observations in Chiasmocleis panamensis, where, as aforementioned, I was unable to identify and quantify the digestive content in two sets of tadpoles, which could

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indicate that these larvae feed on minute particles, hard to be detected with microscope on usual magnifications. As regards macrophagous and megalophagous morphologies, in Dendropsophus nanus, D. microcephalus and Lepidobatrachus llanensis small particle frequencies are very low, suggesting poor efficiency in
retention, associated with a reduction of filtering and entrapment structures in buccopharyngeal cavity and
branchial basket. Ceratophrys cranwelli shows a more generalist diet, with a considerable contribution of
food particles below 10% of the body size. Among macrophagous morphology tadpoles, this species have the
least reduced branchial basket, the highest ih/oh ratio, the largest number of filtering structures within the buccopharyngeal cavity, and also a relatively large digestive tract (6.73 times longer than the body Ulloa Kreisel
2003).
To sum up, combining the observations in this work and the information available in literature, it can be
synthesized:
microphagous morphology tadpoles are able to retain the smallest food particles, compared to the remaining species. According to my observations, however, items that are effectively ingested are in an intermediate
range, not significantly different from that of the generalized morphology tadpoles. As regards larger food
items, the reports of macrophagous diets in microphagous morphology species indicates that the features considered in the hyobranchial apparatus are not a limitation in this case.
generalized morphology tadpoles ingest frequently food particles within an intermediate size range,
obtained through a variety of feeding modes (suspension feeding, surface rasping, browsing, predation).
According to experimental works, they are not able to retain food items as small as those of microphagous
morphology tadpoles. In the opposite extreme, several studies record the occurrence of macrophagy coupled
with generalized morphologies. Even when considering a strict definition of macrophagy (referring to ingestion of large, whole prey and taking into account predator size), and disregarding those cases involving previous tearing apart of prey, it would still be possible to assume that generalized tadpoles are able to consume
large items in relation to their body size.
macrophagous and megalophagous morphology tadpoles ingest whole, large particles with relation to their
length, with a greater volumetric prey-predator relation in megalophagous forms. The proportion of small
food items in the analyzed samples is very small, indicating poor efficiency in retaining those particles.
Intermediate species (i.e., species diverging in morphological features and prey size from those representative of the group) could be included in this general characterization. Examples among studied species are
Ceratophrys cranwelli, with the said attenuated morphological macrophagous-like traits, and a noticeable
contribution of small food items in their diets, and Phyllomedusa spp., with the more developed branchial baskets, the higher ih/oh ratio, numerous buccal filtering structures, and an average food size value smaller than
the remaining generalized tadpoles. In several species, morphology indicate an assignation to a certain group,
but prey size range overlaps with that of other groups (e.g., microphagous and generalized morphology tadpoles capable of macrophagy); experimental studies and further observations could reveal whether these are
exceptions, or frequent examples that soften the interspecific variation in diets, yet blurring the relation with
morphological variables.
To conclude, it would seem that macrophagous feeding is possible across a broad array of morphological
designs. First, it occurs on macrophagous morphology, associated with robust and long ceratohyals, a marked
reduction of the branchial basket, a diverging oral apparatus, and an overall scarcity of filtering structures in
the buccal cavity, or at least with some of these characters. Second, it occurs in megalophagous morphology,
where the large buccal cavity volume results from the widening of the hyobranchial skeleton and neurocranium, and where the branchial basket area is only slightly reduced, the mouth has a wide opening and lacks
keratodonts, and the buccal cavity is devoid of filtering structures. Third, it occurs among tadpoles with generalized hyobranchial skeletons, oral apparatuses and buccopharyngeal cavities. And finally, it is also possible
in some forms with typically microphagous-like hyobranchial skeletons, mouths and buccal cavities. Macrophagy seems to have a closer relation with some muscle development. Most of the species that feed on large

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prey have an extensive development of the buccal floor depressor musculature, regardless of the hyobranchial
skeleton configuration. For instance, Spea bombifrons tadpoles have a low ih/oh ratio in carnivorous morphs,
but similar to generalized tadpoles in omnivorous morphs (Wassersug & Hoff 1981). Conversely, an efficient
microphagy (retention of minute particles, 0.1 ) seems to occur only linked to a remarkable development of
the branchial basket, which supports very complex filtering and trapping structures. This kind of microphagy
would be exclusive to microhylids, pipids, and rhinophrynids (Wassersug 1972).
The morphological variables of the hyobranchial apparatus and food size (variables which yield to the
general groups of macrophagous, microphagous, mesophagous and megalophagous morphology and diet, in
this study), may be incorporated to those considered by other authors in the discussion of ecomorphological
guilds. A brief comment is noteworthy necessary prior to the integration mentioned. The grouping of species
according to certain morphological and ecological variables, and the subsequent generation of categories, or
ecomorphological guilds is a complicate task. The overall idea is to identify general patterns where variables
of different kinds converge. However, one tends to discretize the morphological and ecological spaces, which
results in an adjusted classification of the diversity, and one would expect to find the predicted correlation
every time new data are added to the analysis. The conceptualization of the groups so formed, as real entities,
is consolidated with their naming, and this makes the panorama more rigid. Thus, one would expect to find a
biunivocal relation between categories and their constitutive elements, i.e., only microphagous tadpoles in a
guild named Microphagous tadpoles, and only there; only carnivores in a guild named Carnivores, and not in
alternative guilds, etc. The expectations one brings to such classification into ecomorphological guilds, immediately collides with the proposed classifications, which are in several cases, ambiguous and confusing. Some
terms often used as denominations for categories contribute to this confusion, since they have intuitive,
assumed, non-formalized definitions, v.g, the above mentioned terms microphagy and macrophagy, carnivore
and herbivore, suspension feeder and predator. These terms refer to different variables, such as food item size,
qualitative kind of food, ingestion mechanism, respectively, and even then, they are usually employed as
denominations for categories, which, in theory, are mutually exclusive. Additionally, they are presented as
binomials, without making explicit the boundary between them. In order to homogenize the use and sense of
these terms, it is necessary to arrive at definitions which are precise and yet comprehensive and referential
enough so as to avoid misinterpretations. And even then, once the concepts have been rigorously defined, the
categories generating and naming with them are not universal, but contingent and redefinable when the
empiric content they are based on changes.
Taking up the integration with other schemes of ecomorphological guilds, some of the groups proposed by
McDiarmid and Altig (1999) (created on the basis of external morphology, developmental mode, and habitat)
are recovered when considering the hyobranchial apparatus structure (Fig. 77). Some carnivores and macrophagous tadpoles (sensu McDiarmid & Altig 1999) form discrete clusters in the hyobranchial skeletons
ordination, with distinctive features already commented (macrophagous and megalophagous morphology
groups). In the same manner, suspension feeding tadpoles (sensu McDiarmid & Altig 1999) in general correspond to the microphagous morphology group. The large cluster of hyobranchial generalized morphology
joins the remaining guilds added to the analysis, with an apparent segregation between some endotrophic and
purely lotic forms (clasping, suctorial, gastromyzophorous tadpoles) and some purely lentic or slow-water
forms (suspension-rasper, psammonic, fossorial tadpoles). The fact that numerous groups based on external
morphology, developmental modes, and microhabitat can be consolidated into a few general patterns of hyobranchial apparatus structure, indicates a more conservative internal morphology, in comparison with external
and behavioral characters. It would appear that, if selection processes occur, these characters are more malleable than some internal morphological characters, where the developmental constraints appear to be stronger.
Ulloa Kreisel (2003) has recently studied morphological structures related to feeding, in a set of anuran
larvae of northern Argentine, and she supported a classification based on morphology and morphometrics of
the buccal cavity and digestive tract, in relation to feeding habits (inferred from literature). Results show some

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general patterns compatible with the groups that appear in the present study. The tadpoles of Lepidobatrachus
and Ceratophrys have short digestive tracts, and the gastric region occupies a large percentage of the total
tract, in comparison to other larvae. Additionally, the midgut is the shortest among the analyzed taxa, and the
posterior intestine has a conspicuous dilatation in the most anterior portion. Dendropsophus nanus tadpoles
share these features (Vera Candioti et al. 2004; pers. obs.). The gastric region is a manicotto glandulare in
Dendropsophus, and a larval stomach in Ceratophrys and Lepidobatrachus, being distinguishable in the latter,
by the mucous cells of the glandular neck. In the remaining forms, definite patterns are not verified, and there
is a high overlapping of morphological features assigned to different guilds. The length of the digestive tract,
in relation with qualitative diet composition (herbivore, carnivore) is object of study in several researches
(e.g., Altig & Kelly 1974; Horiuchi & Koshida 1989, in Alford 1999). Additionally, Relyea and Auld (2004)
investigated digestive tract length variation in tadpoles, in relation to competence and predation phenomena.
Their results showed a remarkable phenotypic plasticity in response to diet and interactions, which obscures
any generalization to be made from interspecific comparisons.
Finally, the results obtained in the presented study can be analyzed within a theoretical ecological frame,
including general issues such as resource utilization, niche, form-function, etc. Ferry-Graham et al. (2002)
presented a very interesting paper about the specialization phenomenon, inquiring, among other subjects, into
the varied concepts and uses of the term specialist. A species that utilizes a few food items among a broad
range of available prey is considered to be a specialist. This is not always accompanied by apomorphic morphological characteristics, as the predator may merely possess a narrow niche. In general, the mechanism that
determines which preys are taken from the environment is behavioral (behavioral specialists), morphological
(functional specialists linked to predator morphology), or ecological (ecological specialists linked to competence or other interactions). Among the species in this study, varied situations occur. On one hand, macrophagous tadpoles such as Dendropsophus nanus, D. microcephalus, Ceratophrys cranwelli and
Lepidobatrachus llanensis have a morphology linked to a preference of large food items. Several features tend
specifically to the capture and handling of large prey, e.g., the development of buccal floor depressor muscles,
a wide mouth gape width in Lepidobatrachus, a narrow oral gape that allows generation of strong negative
pressure at mouth level in Dendropsophus species, or yet a well-developed oral apparatus, with numerous
spike-like keratodonts rows in Ceratophrys. Some other features reduce the possibility of extending the range
toward the smallest food sizes, e.g., the reduction or absence of buccal filtering structures, reduction of branchial basket and with it, of branchial filters. Such reductions are less pronounced in C. cranwelli, as evidenced
by the high proportion of small food particles in its diet. According to the terminology employed by FerryGraham et al. (2002), the species just mentioned would be considered to be functional specialists. It is interesting that these species, belonging to different families, have converged in more than one morphological
character, reflecting one of the multidimensional aspects of the convergence phenomenon, where multiple
traits of organisms can converge in a coordinate answer to a single environment aspect, in this case, prey size
(Harmon et al. 2005). On the other hand, microphagous species have a set of morphological traits tending to
increase effectiveness in consuming minute items, e.g., the great development of branchial baskets, branchial
filters and secretory tissues. This, however, does not set a limit to the large-size items which can be ingested,
as shown by macrophagous microhylids and Rhinophrynus dorsalis, with typically microphagous hyobranchial skeletons. The same occurs with several generalized morphology species, which, though frequently consumers of intermediate-size food items, may occasionally have macrophagous diets. In such cases, efficiency
in a given activity is not coupled with a reduced ability to perform alternative activities. Thus, either the specialization is at a different, non-analyzed morphological level, or, as Ferry-Graham et al. (2002) pointed out, it
could occur at a behavioral level, i.e., for some reason (availability, maximization in energy intake, etc.), predators consume more frequently a few food items out of a broad range of food items.
As regards morphology-ecology interaction, Koehl (1996) carried out a comprehensive analysis, arguing
that the quantitative relationship between a measure of performance and a measure of morphology is nonlin-

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ear. This implies that there are ranges of the morphological parameter where modifications of structure make
little difference, and other ranges where small morphological changes can have significant consequences.
When morphology of a structure does not affect performance of some function, there is allowance for diversity of form (functional equivalency) and for assumption of other functions. This could be the case with the
occurrence of macrophagy in such variety of arrays of hyobranchial skeletons. In other words, in this case,
morphological structures are flexible enough to allow a broad range of possibilities in food resources utilization, which results in species that frequently consume certain types of food, notwithstanding how effective
they may be in consuming others. For instance, microhylids and Xenopus laevis consume food items similar
in size to those eaten by generalized tadpoles eat, even when they can ingest much smaller items; some generalized tadpoles, although frequently consuming intermediate-sized particles, are capable of ingesting much
larger items; finally, some macrophagous morphology tadpoles, such as Ceratophrys cranwelli, though frequent predators of large prey, can supplement their diets with small particles such as microalgae.
Finally, Koehl (1996) stressed that descriptive studies relating form-function (like the present study) are
an effective way to reveal patterns that can guide further research about mechanisms determining such a relationship. This author also detailed some of the reasons why the prediction capacity of these studies may result
non-reliable. First, the analysis may not reveal a connection between structure and function in cases for which
the effects of morphology on performance is nonlinear, or for which different mechanisms can play similar
roles. They can also fail to reveal a mechanistic relationship between a structural feature and performance if
the feature studied is only one of several that affect the performance. They can find correlations between morphological features and performance that are not causally related when other correlated but unmeasured morphological variables are responsible for the performance differences assessed. This can be related with the
scale-effect in the form-function relationship, mentioned by Lauder (1996), according to which, function and
structure appear to be reasonably predicted at very specific or general levels (e.g., histological, ecological,
behavioral levels), whereas at an intermediate level (such as musculoskeletal function), the relationship
between structure and function becomes more obscure. For all of these reasons, predictions of guild membership, based on correlations between morphological and ecological patterns must be considered tentative, in so
far the mechanisms underlying in varied processes associated to biological diversity are understood.

Conclusions and Perspectives


As summary and conclusion for this work, a few final comments are listed, regarding the results obtained and
the discussion addressed.
1.The analysis of the species studied, and the comparison with previous information about other taxa, support the idea that morphological diversity can be summarized into some general patterns.
On one hand, chondrocranium, musculature, oral apparatus and buccal cavity characters are relatively
constant intragenerically, although several taxa show some variation, even intraspecifically.
1.a.In the cartilaginous skeleton, the most variable characters are the configuration of the suprarostral
cartilage, the presence of quadratoorbital commissure and larval otic, anterolateral of the otic capsule, lateral
trabecular, quadratoethmoid, and pseudopterygoid processes, the attachment of the ascending process to the
braincase, and the general configuration of the hyobranchial skeleton. According to these qualitative characters, Chaunus and Physalaemus chondrocrania are very similar to each other, with suprarostrals with single
corpus and differentiated alae, quadratoorbital commissure present, and larval otic process absent. Telmatobius tadpoles have some similar traits, and are the only ones in the sample species with adrostral cartilages.
The Hylidae family shows a great intergeneric variation, mainly in the configuration of suprarostrals and palatoquadrates, the presence of quadratoethmoid, pseudopterygoid, anterolateral of the otic capsule, and larval

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otic processes, the attachment of the ascending process to the braincase, and the development of the branchial
basket. These features appear in different combinations in the five groups of hylids studied: phyllomedusines,
Lysapsus + Pseudis, Hypsiboas, Scinax, and Dendropsophus; additionally, the two species of Scinax differ in
some characters, showing their assignation to different species groups. Although at first glance they appear
very different, the ceratophryine Ceratophrys, Chacophrys, and Lepidobatrachus share some qualitative skeletal characters, such as the complete fusion of the infrarostrals and suprarostrals, and the absence of spicules
in the hyobranchial skeleton. With a few exceptions, microhylids are a very homogeneous group, and the list
of synapomorphies is profuse; some variable characters are the presence of the ventrolateral of the palatoquadrate, and the crista parotica. Finally, notwithstanding several differences (mainly in the hyobranchial
skeleton), some of them possibly due to different feeding habits, the skeletons of pipid larvae are very similar,
with common features such as the fusion of suprarostrals and trabecular horns, high suspensorium, and larval
otic process present.
1.b.Interspecific variation in musculature is not as marked as in the skeleton. Some variable characters
are the configuration of the mm. mandibulolabialis, l. m. lateralis, l. m. externus, interhyoideus posterior, diaphragmatopraecordialis, subarcuales recti, subarcualis obliquus, and tympanopharyngeus. Chaunus tadpoles
show a single m. mandibulolabialis, a peculiar disposition of the m. subarcualis rectus II-IV, and lack mm.
interhyoideus posterior and diaphragmatopraecordialis. Physalaemus larvae possess mm. interhyoideus posterior and diaphragmatopraecordialis, and the mm. subarcuales recti and tympanopharyngeus have a different
configuration from that of Chaunus. Scinax, Hypsiboas and Phyllomedusa possess a m. mandibulolabialis
with two slips, a m. subarcualis rectus I with two or three slips, and a m. tympanopharyngeus clearly differentiated from the m. levator arcuum branchialium IV. Phyllomedusines differ from most of the hylines, in the
configuration of the m. subarcualis obliquus, with a single insertion on the hyobranchial skeleton, and the
insertion of the m. tympanopharyngeus, not reaching the region anterior to the glottis. Dendropsophus, Lysapsus and Pseudis share the unusual disposition of the m. l. m. lateralis, inserted on the nasal sac, and the m. subarcualis rectus II-IV divided into anterior and posterior parts. Telmatobius larvae apparently differ by having a
distinctive pattern of muscles inserting on the diaphragm, with a muscle slip running anteriorly toward the
articular process of the palatoquadrate. Ceratophrys and Lepidobatrachus share the absence of the mm.
quadratoangularis, suspensoriohyoideus, interhyoideus posterior, and diaphragmatopraecordialis, and Lepidobatrachus also lacks the m. mandibulolabialis. Microhylids musculature is very conservative within the
group, yet different from the remaining species; variable characters are the number of slips of the m. subarcualis rectus I and the configuration of the m. l. m. longus. The Microhylidae species in this study support the
idea that Neotropical forms show a distinctive crossing of the fibers of the m. levator arcuum branchialium III.
Lastly, some remarkable features in the muscular configuration of pipid larvae are the absence of m. constrictor branchialis IV, the insertion on a median raphe of the m. subarcualis obliquus, and the unusual disposition
of the m. subarcualis rectus II-IV, without any attachment on the medial ceratobranchial IV.
1.c.The characters of the oral apparatus and buccal cavity are highly variable across the species studied,
but, with some exceptions, they are generally maintained within the genera. The oral apparatus of Chaunus,
Hypsiboas, Lysapsus, Phyllomedusa, Physalaemus, Scinax, and Telmatobius, in spite of several differences,
correspond in general terms to that of typical pond-type larvae, with papillar margin, keratinized rostrodonts,
and keratodonts disposed in a LTRF 2/2 to 2/4. The buccopharyngeal cavities differ in the presence and number of prenarial and postnarial structures, spurs, infralabial, lingual, buccal roof and floor papillae, and the
general configuration of dorsal and ventral vela. The oral apparatus of Dendropsophus is very different from
the generalized mouth, devoid of keratodonts and papillar margin. Similarly, Lepidobatrachus tadpoles lack
keratodonts, and have scarce marginal papillae. Conversely, Ceratophrys has numerous keratodonts rows, surrounding well-developed rostrodonts. These three genera have an overall reduction or absence of filtering
structures inside the buccal cavity. Microhylids show an oral and buccopharyngeal morphology relatively uniform, with absence of keratinized structures and a particular combination of characters in the buccal cavity.

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Finally, pipid tadpoles are devoid of keratinized mouthparts, and their buccopharyngeal cavity lacks structures
typical of other tadpoles, such as ridges, papillae, pustules, and tongue anlage.
On the other hand, quantitative ordination analyses reveal a component which group together taxonomically unrelated species, thus reflecting convergence phenomena. This is verified in the skeleton (mainly, in the
hyobranchial skeleton), mm. interhyoideus and orbitohyoideus development, and some features of the oral
apparatus and buccal cavity. Then, there appear a large group of species with generalized morphology, characterized by a branchial basket occupying around 50% of the total hyobranchial area, an intermediate value in
the buccal floor levator-depressor muscles relation (ih/oh ratio), and numerous filtering structures within the
buccal cavity, and several other species that diverge in the shape space. A first group, including microhylids
and Xenopus laevis, diverges because of the great development of the branchial basket and the high ih/oh
ratio. Another group, including tadpoles of Dendropsophus microcephalus group and Ceratophrys, diverges
because of the reduced branchial basket, robust ceratohyals, very low ih/oh ratio, and ample buccal cavity,
with scarce filtering structures. Finally, Lepidobatrachus tadpoles diverge because of the laterally expanded
ceratohyals, and barely reduced branchial basket.
2.In relation to diet, the analysis of qualitative composition showed that the proportion of animal material is
often greater than the vegetal material. The predominance of vegetal content in some forms can be explained
in terms of food availability and opportunism. These results, along with observations of other researchers,
make necessary to reconsider the assumption of tadpoles as being mainly phytophagous, and along with this,
their roles in trophic webs within aquatic communities. Regarding prey size, the concepts of microphagy and
macrophagy commonly employed in literature were discusses, and I have employed here the one that, in my
opinion, best combines internal coherence, applicability and practicity. Thus, I consider that the terms macrophagous and microphagous necessarily should take into account the size of who is ingesting the food item,
and they should be thus defined on the basis of prey size relative to some measurement indicative of the predator size. This allows the comparison across a wide sample including several prey and predator sizes. The
generation of categories, i.e., to determine which relative prey size correspond to microphagous or macrophagous feeding, was effected once the food size range was obtained, and the categories mesophagous and megalophagous (terms already employed in previous studies) were added to the binomial microphagymacrophagy. Then, I consider within: microphagous diet, those forms consuming mainly prey sizes representing <1% of the body size; mesophagous diet, between 1% and 30%; macrophagous and megalophagous,
>50% of the body size. The term megalophagous has been kept to distinguish Lepidobatrachus tadpoles,
which consume whole prey, volumetrically much larger than in the case of macrophagous forms. With larger
samples, the categories would be surely redefined.
3.In the species analyzed in this study, some morphological patterns mentioned in the first point correspond
to a great extent to a prey size gradient. The morphological variables that most contribute to the morphologydiet relation are branchial basket shape, ih/oh ratio, and mouth gape width. The effect of hyobranchial apparatus configuration on prey size is related to a significant historical effect linked to the genus Dendropsophus.
Most chondrocranial features, presence-absence and trajectories of muscles, and some traits in the buccopharyngeal cavity reflect shared historical processes non-related with trophic ecology, excepting some particular
groups. Considering the microphagy-macrophagy definitions and morphological features, four groups of morphology-diet have been considered: (a) Microphagous morphology and diet: with voluminous branchial basket, high ih/oh ratio, large mouth gape, and prey size smaller than 1% of the tadpole body size; (b)
Generalized morphology and mesophagous diet: with branchial basket occupying 50% of the hyobranchial
skeleton, intermediate ih/oh ratio and mouth gape, and prey size between 1% and 30% of the tadpole body
size; (c) Macrophagous morphology and diet: with reduced branchial basket, developed ceratohyals, very low
ih/oh ratio, small (Dendropsophus) to intermediate (Ceratophrys) mouth gape, and prey size larger than 50%

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of the tadpole body size; (d) Megalophagous morphology and diet: with laterally expanded ceratohyals,
slightly reduced branchial basket, very low ih/oh ratio, enormous mouth gape, and prey size larger than 70%
of the tadpole body size.
4.With the addition of more species, obtained from the literature, to the ordination of the hyobranchial skeletons, and considering qualitative information on their diets, the groups formed are generally maintained. An
interesting observation is that the patterns observed in the whole sample, seem to repeat themselves in a
smaller scale, within the generalized morphology group: again, there appear a large group with generalized
traits, and some species deviate, resembling some of the divergent groups in morphology and diet. Two clades
are consistent with this morphological pattern: the group containing all microhylids except Otophryne, and the
group that joins Ceratophrys and Chacophrys.
5.However, besides the general patterns manifested by the mentioned groups, there appear numerous
exceptions, i.e., species where the morphology is not concordant with feeding habits. Thus, some forms with
generalized (e.g, Leptodactylus pentadactylus, Pleurodema nebulosa), and microphagous-like hyobranchial
skeletons (e.g., Rhinophrynus, Scaphiophryne) are reported capable of macrophagous diets.
6.From the points above, it can be concluded that the predictive capacity of ecomorphological studies, i.e.,
to infer diet from morphology, or vice versa, works in some cases and not in others. In several species, the
relation between morphology and diet is consistent, and each level of morphological analysis indicates the
same feeding habit, and in these conditions, the predictive capacity of ecomorphological studies seems to
work. In other species however, there is a combination of morphological and ecological characters that does
not allow the establishing of clear categories, and thus inferences thereof would lead to inaccurate results.
7.Compared with previous studies that refer to ecomorphological guilds built from other variables (external
morphology, microhabitat, developmental mode, digestive tract features), it may be noted that some groups
coincide with those mentioned in this study, whereas others are contained by the mentioned in this work. Ceratophrys, Lepidobatrachus and Dendropsophus tadpoles separate from other species because of the hyobranchial apparatus, external morphology and digestive tract features, in a marked relation with the food type.
Suspension feeding tadpoles have very constant characters in external morphology, buccopharyngeal cavity,
and hyobranchial apparatus structure, such traits being linked to feeding habits; conversely, in the digestive
tract the relation is not clear. The fact that numerous species from varied microhabitats, feeding mechanisms,
external and digestive tract morphologies, share a generalized morphology in the hyobranchial skeleton indicates a more conservative internal morphology regarding external and behavioral characters.
8.Lastly, analyzing results in the general ecological context, among the species studied, tadpoles of Dendropsophus microcephalus, D. nanus, Lepidobatrachus llanensis, and, to a lesser extent, Ceratophrys cranwelli, can be considered functional specialists, where the occurrence of certain type of feeding is associated to
morphological features that optimize some activity, sometimes even reducing the effectiveness in performing
alternative tasks. Most generalized and microphagous-like morphology species frequently consume small and
intermediate-sized food items, but some of them have been reported as being capable of macrophagous feeding. They can be considered behavioral or ecological specialists, where the preference for certain food types
would be explained, not by morpho-physiological aspects, but by ecological interactions, specific behaviors,
and other understudied issues.
As a final comment, this work generates numerous questions about the patterns observed, thus leaving
room for future investigations. Firstly, the selection of the variables employed to account for prey and predator
features can be adjusted, by considering other attributes. For instance, the length (maximum axis) of the prey

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can be replaced by its volume, or better yet, some shape descriptor, as employed in the recent paper by Vincent et al. (2006). The variable selected to represent the predator size can also be improved, recording other
variables or ratios between them. On the other hand, multivariate canonical analyses, broadly used to investigate the relation among various datasets (e.g., species distribution regarding environmental parameters, morphology-environment relation), have shown in this case, their usefulness in trophic ecomorphology, linking
predator morphology to prey size. The recording of other morphological and ecological variables, and their
inclusion in this kind of analysis would allow for the definition of new patterns and the relations among them.
It would be interesting also, to circumscribe shape variation and diet-morphology relationship analyses to the
generalized species, thus profiting from the accuracy of such methods to reveal more subtle changes. Addressing intraspecific variation studies would provide valuable information about the diet-morphology relationship
through ontogenetic development, or among populations, which would render a comprehensive characterization of species. On the other hand, it would also be interesting to investigate the physiological mechanisms
regulating anatomical and behavioral aspects, involved in several processes such as prey detection, recognition, capture and handling. Regarding this last point, developmental biology can contribute valuable information on genic and molecular mechanisms determining certain morphologies; for instance, Trbulo et al. (2004)
have identified an apoptotic pathway in the neural crest of Xenopus laevis, where the experimental expression
of some genes leads to phenotypes that are similar to the macrophagous-like morphology mentioned in this
study. Additionally, the integration of these results into a phylogenetic context (through comparative methods
e.g., Harvey & Pagel 1991; Larson & Losos 1999; Giannini 2003), and the consideration of general ecological theories of resource use, such as optimal foraging and optimal diet theories (e.g., MacArthur & Pianka
1966; Sih & Christensen 2001), can supply information about the origin of specializations in an evolutionary
frame, and thus better contribute to our understanding of biological diversity.

Acknowledgments
I would like to thank all people and institutions that help me in many ways in this project: Consejo Nacional
de Investigaciones Cientficas y Tcnicas (CONICET), Fundacin Miguel Lillo (FML), Universidad Nacional
de Tucumn (UNT), Laboratorio de Microscopa Electrnica del Noroeste Argentino (LAMENOA), Instituto
Superior de Investigaciones Biolgicas (INSIBIO), Smithsonian Tropical Research Institute (STRI), Deutscher Akademischer Austauschdienst (DAAD), E. Lavilla, V. Abdala, D. Echeverra, R. Montero, M. Fabrezi,
S. Snchez, E. Luque, A. Haas, and all researchers from the Instituto de Herpetologa (FML), Instituto de
Morfologa Animal (FML) and Instituto de Bio y Geociencias (IBIGEO); N. Vera Candioti helped me with
English translation; R. Altig, M. Vences, and an anonymous reviewer made valuable suggestions that greatly
improved an early version of this manuscript.

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