Vera Candioti 07 Tesis Okkkkkkkkkkkkk

ZOOTAXA

Anatomy of anuran tadpoles from lentic water bodies: systematic relevance and correlation with feeding habits

M. FLORENCIA VERA CANDIOTI

Magnolia PressAuckland, New Zealand

1600

TERM OF USEThis pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website site is prohibited.

VERA CANDIOTI2 Zootaxa 1600 2007 Magnolia Press

M. FLORENCIA VERA CANDIOTIAnatomy of anuran tadpoles from lentic water bodies: systematic relevance and correlation with feeding habits(Zootaxa 1600)175 pp.; 30 cm.

28 Sept. 2007

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

ZOOTAXAISSN 1175-5326 (print edition)

ISSN 1175-5334 (online edition)Copyright 2007 Magnolia Press

Zootaxa 1600: 1175 (2007) www.mapress.com/zootaxa/

Anatomy of anuran tadpoles from lentic water bodies: systematic relevance and correlation with feeding habits

M. FLORENCIA VERA CANDIOTICONICET, Instituto de Herpetologa, Fundacin Miguel Lillo, Miguel Lillo 251, Tucumn, Argentina. [email protected]

Table of contents

ABSTRACT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5INTRODUCTION. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5MATERIALS AND METHODS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7

Specimens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7Chondrocranium and hyobranchial skeleton. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9Gut content . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10Data analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

Morphological variation. Geometric morphometrics. Relative warp analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10Gut content variation. Correspondence analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11Gut content-morphology relationship. Partial canonical phylogenetic ordination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

RESULTS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13Morphological descriptions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

Bufonidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13Chaunus arenarum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13Chaunus spinulosus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19

Ceratophryidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26Ceratophrys cranwelli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26Lepidobatrachus llanensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32Telmatobius cf. atacamensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37

Hylidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43Dendropsophus microcephalus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43Dendropsophus nanus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49Hypsiboas rosenbergi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54Lysapsus limellum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61Phyllomedusa hypochondrialis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67Phyllomedusa sauvagii . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72Pseudis paradoxus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78Scinax boulengeri . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83Scinax nasicus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89

Leiuperidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96Physalaemus santafecinus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96

Microhylidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102Chiasmocleis panamensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102Dermatonotus muelleri . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107Elachistocleis bicolor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113

Pipidae. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119Xenopus laevis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119

Morphological variation. Geometric morphometrics. Relative warp analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 124Gut content variation. Correspondence analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 128Gut content-morphology relationship. Partial canonical phylogenetic ordination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130



DISCUSSION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132Interspecific variation. Morphology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132Interspecific variation. Diet . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 144Ecomorphological considerations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147

CONCLUSIONS AND PERSPECTIVES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162ACKNOWLEDGMENTS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 166REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 166

Index of Figures per species

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


Zootaxa 1600 2007 Magnolia Press 5ANATOMY OF ANURAN TADPOLES

Figure 58. Chiasmocleis panamensis. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102Figure 59. Chiasmocleis panamensis. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105Figure 60. Chiasmocleis panamensis. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106Figure 61. Chiasmocleis panamensis. Oral apparatus and buccopharyngeal cavity. SEM micrographies . . . . . . . . . . . . . . . . . . . . . . 107Figure 62. Dermatonotus muelleri. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108Figure 63. Dermatonotus muelleri. Musculature. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111Figure 64. Dermatonotus muelleri. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 112Figure 66. Elachistocleis bicolor. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 114Figure 67. Elachistocleis bicolor. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 117Figure 68. Elachistocleis bicolor. Oral apparatus and buccopharyngeal cavity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118Figure 69. Xenopus laevis. Chondrocranium and hyobranchial skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 119Figure 70. Xenopus laevis. Musculature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122Figure 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 (mainlyGosner stages 3136) of nineteen species from various lentic environments were selected. Morphological charactersfrom the skeleton, musculature, oral apparatus and buccopharyngeal cavity were recorded, and a gut content analysis wasperformed, with emphasis on food size distribution. Ordination techniques were applied in order to find patterns of simi-larity in morphology and gut content. Canonical ordination methods were used to investigate the relationship among gutcontent, morphology, and phylogeny in the species considered. The results show that several skeletal, muscular, and buc-cal characters are relatively maintained within genera. Other features, which have appeared independently in differentlineages, reflect convergence phenomena in some cases related to ecological aspects. The configuration of the hyobran-chial skeleton, the development of the buccal floor depressor and levator muscles, and mouth gape width correlate withprey size. In some species, morphology is clearly related with feeding. Tadpoles that ingest large food particles relative totheir body length present morphological traits attributable to macrophagy. Taxonomically unrelated tadpoles of Dendrop-sophus nanus, D. microcephalus and Ceratophrys cranwelli possess hyobranchial skeletons with robust, rostrocaudallylong 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 thejaws, result in a very wide oral apparatus and an ample buccopharyngeal cavity that allows the tadpole to ingest large andwhole prey; the branchial basket, although its ceratobranchials lack lateral projections and spicules, is slightly reduced inarea. The four species mentioned have a noticeable development of the buccal floor depressor muscles, and buccal cavi-ties with scarce filtering and entrapping structures. In Elachistocleis bicolor, Dermatonotus muelleri, Chiasmocleis pan-amensis, and Xenopus laevis tadpoles, the branchial basket occupies >70% of the total hyobranchial skeleton area, andthe hypobranchial plates are highly reduced; the buccal floor levator muscles are well-developed, with an increased siteof attachment on the ventral expansion of the lateral process of the ceratohyal; the scarcity of the filtering structures inthe buccopharyngeal cavity are balanced with the great development of the branchial filters and secretory zones; all thesefeatures 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 whenretaining minute particles. Finally, a large group of species present generalized morphological characters, such as a bran-chial basket occupying about 50% of the total hyobranchial apparatus, intermediate values of mouth gape width and buc-cal floor levator / depressor muscles ratio, and abundant filtering structures in the buccopharyngeal cavity; these speciesfeed frequently on food particles between 130% of the tadpole body length; however, in some of the species, macroph-agous 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; gutcontent; interspecific variation; ecomorphology

Introduction

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



logical parameters. Altig and Johnston (1989; updated in McDiarmid & Altig 1999) considered that, amongexotrophic species from lotic and lentic environments, there exist several categories defined on the basis ofgeneral morphological characters, such as body shape, eye position, and configuration and orientation of theoral disc. Lentic larvae include groups such as benthic, nektonic, neustonic, arboreal, carnivores, macropha-gous, suspension-rasper, and suspension feeder tadpoles. Most of these categories are based on morphologicalsimilarity and on known or presumable information about larval feeding and ecology. Other researchers havefound that not only external, but internal features can be related to anuran larvae ecology. Thus, some studiesinquire 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 Candiotiet 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 therelationship between them. The hypothesis that underlies such an approach holds that morphological variationcorresponds with ecological variation (Harmon et al. 2005). In other words, linked to certain ecologicalaspects, there appear to be morphological characters capable of determining ranges of resource intake in someof the environment dimensions: temporal, spatial or trophic. To address an ecomorphological approach, varia-tion 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 descrip-tions. In skeletal morphology, geometric morphometric methods offer an approach complementary to qualita-tive studies, and combined with several statistical multivariate tests, allow for quantitative study of shapevariation. In zoology, these methods have been employed to describe shape change associated to ontogeny andallometry (e.g., Monteiro & Abe 1997; Monteiro et al. 1999; Larson 2002, 2005), variation among popula-tions, 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 & Collins2004; Zelditch et al. 2004; Anderson & Roopnarine 2005; Beszteri et al. 2005; Stayton 2005; Vera Candioti etal. 2007), and morphological variation related to ecological features (e.g., Adams and Rohlf 2000; Claude etal. 2004; Dayton et al. 2005). On the other hand, in several studies that analyze the morphology-ecology rela-tion, although morphology is exhaustively examined, ecological variables are described qualitatively orinferred from morpho-functional aspects. Some studies, however, quantify both sets of variables, and performstatistical tests to investigate the relation among them; studies of this kind have been carried out mainly onfishes (e.g., Motta et al. 1995b; Wainwright & Richard 1995; Shoup & Hill 1997; Clifton & Motta 1998; Huy-sentruyt 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 charactersof the cartilaginous skeleton, oral apparatus and buccopharyngeal cavity (e.g., Fiorito de Lpez & Echeverra1984; 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 & Vaira1997; Alcalde & Rosset 1998; 2003; Lavilla & De S 1999; Perotti & Cspedez 1999; Echeverra & Lavilla2000; Sandoval 2000; Alcalde 2001). Muscle studies were long ignored, but in recent years interest has beenrevived; 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). Larvalmorphology 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 aninteresting contribution to help resolve relationships in understudied groups. As to feeding, this issue isaddressed 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; VeraCandioti & Lajmanovich 1998; Arias et al. 2002). Despite the abundance of data, very few studies integrate



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 rela-

tionship with the feeding habits. I selected a set of lentic exotrophic species that may be assigned to the eco-morphological guilds proposed by Altig and Johnston (1989) and Altig and McDiarmid (1999a,b); the studyof internal morphology and a quantitative analysis of gut content composition may afford additional informa-tion to help redefine these categories. Most larvae I studied are common inhabitants from varied regions fromArgentina, and five species from other geographic regions have been included. Chaunus arenarum, C. spinu-losus, Telmatobius cf. atacamensis, Hypsiboas rosenbergi, and Physalaemus santafecinus are generalizedpond 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 col-umn and feed by filtering suspended particles and rasping submerged surfaces; Ceratophrys cranwelli andLepidobatrachus llanensis are carnivorous tadpoles that inhabit temporary ponds in arid regions from North-western Argentina; Dendropsophus nanus and D. microcephalus are small hylid tadpoles, known to be mid-water macrophagous forms; Chiasmocleis panamensis, Dermatonotus muelleri, Elachistocleis bicolor, andXenopus laevis tadpoles feed by floating in the water column and pumping water through buccopharyngealstructures to entrap suspended particles. First in this work, I provide basic information about anatomy and gutcontent of these nineteen species; regarding morphology, I included descriptions of the chondrocranium, hyo-branchial skeleton, associated musculature, oral apparatus and buccopharyngeal cavity, recording some traitsfrom which it is possible to infer functional mechanisms, related to prey capture and handling; regarding feed-ing, 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 canbe 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 whichcould be addressed from multiple disciplines such as developmental biology, systematics and ecology arise.

Materials and Methods

SpecimensI 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 adjacentyounger 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 inTable 1 and Figure 1. Larvae were collected with a net, fixed with 10% formalin, and then processed for fur-ther analyses. All dissections and drawings were made with a stereomicroscope and a camera lucida. Speciesnaming is that employed in Frost (2007). In the case of Chaunus species, results in the recent paper by Chap-arro et al. (2007) suggest that most species groups of South American toads should wear the precedent nameRhinella; in the present work, the name Chaunus is maintained waiting for further systematic studies on thefamily.

Chondrocranium and hyobranchial skeletonSpecimens 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 thatemployed by Haas (2003). Latin terms are used only if English terms were not available.



FIGURE 1. Tadpoles of 19 species studied, grouped according to the ecomorphological guilds of Altig & Johnston (1989). CA Chau-nus 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 limel-lum, LLL Lepidobatrachus llanensis, PH Phyllomedusa hypochondrialis, PHS Phyllomedusa sauvagii, PP Pseudis paradoxus, PSPhysalaemus santafecinus, SB Scinax boulengeri, SN Scinax nasicus, TA Telmatobius cf. atacamensis, XL Xenopus laevis. Scale lines= 1 mm.



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

MusculatureSpecimens 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 nomencla-ture 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 lineardimensions. The ih/oh ratio was calculated in order to evaluate buccal pumping abilities. According to Sateland Wassersug (1981), buccal floor levator muscles in microphagous tadpoles are more developed than thedepressors, which results in a high ih/oh ratio. Macrophagous tadpoles exhibit larger depressor muscles, andthus 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 werestained with methyl blue. Oral and buccal terminology follows that of Wassersug (1976), Altig and McDi-armid (1999a), Viertel and Richter (1999), and Altig (2007). Specimens of some species were prepared forscanning electron microscopy according to Fiorito de Lpez and Echeverra (1984). The observations andmicrographs were made with a JEOL 35 CF scanning electron microscope.

Site Date N GuildBUFONIDAEChaunus arenarum Salta, Argentina December 2003 15 benthicChaunus spinulosus Jujuy, Argentina November 2001 15 benthicCERATOPHRYIDAECeratophrys cranwelli Salta, Argentina December 2003 15 carnivore

Salta, Argentina January 1996 10Lepidobatrachus llanensis Salta, Argentina November 1996 7 carnivoreTelmatobius cf. atacamensis Salta, Argentina November 2003 4 benthicHYLIDAEDendropsophus microcephalus Gamboa, Panam July-August 2001 8 macrophagousDendropsophus nanus Santa Fe, Argentina January-February 2001 15 macrophagousHypsiboas rosenbergi Gamboa, Panam July-August 2001 7 benthicLysapsus limellum Santa Fe, Argentina January-February 2001 8 nektonicPhyllomedusa hypochondrialis Formosa, Argentina January 2004 7 suspension-rasperPhyllomedusa sauvagii Salta, Argentina January 2005 10 suspension-rasperPseudis paradoxus Formosa, Argentina January 2004 2 nektonicScinax boulengeri Gamboa, Panam July-August 2001 7 suspension-rasperScinax nasicus Santa Fe, Argentina January-February 2001 15 suspension-rasperLEIUPERIDAEPhysalaemus santafecinus Santa Fe, Argentina January-February 2001 15 benthicMICROHYLIDAEChiasmocleis panamensis Gamboa, Panam July-August 2001 15 suspension-feederDermatonotus muelleri Salta, Argentina January 2005 15 suspension-feederElachistocleis bicolor Santa Fe, Argentina January-February 2001 15 suspension-feederPIPIDAEXenopus laevis Captive population December 2005 10 suspension-feeder



Gut contentTadpole 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 nextfixed 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 fooddye similar to eosin Y, and it stains organic material with a conspicuous cherry-pink color. Three drops ofdigestive content per tadpole were analyzed. Each food item was identified at a general taxonomic level (dia-toms, chlorophytes, rotifers, etc.) and then measured with a micrometric ocular to analyze the distribution offood item sizes. In order not to overemphasize the contribution of small prey taken in large amounts, volumeswere estimated from linear dimensions by comparison with the three-dimensional shape each item mostclosely resembled (Hyslop 1980). The contribution of each item is then expressed as a percentage of the over-all 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 thesnout to the end of the body). As a result of the quantification of gut contents of all the species, a food typematrix and a food size matrix were constructed. In these matrices, each variable (column) is a qualitative fooditem 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 analysisMorphological variation. Geometric morphometrics. Relative warp analysis. To quantify variation in the

shape of the skeletons across species, I applied the landmark-based geometric morphometric methoddescribed in Rohlf and Bookstein (1990). On the right half of the chondrocrania and hyobranchial skeletons, aset of landmarks was marked and digitized with the software tpsDig2 (Rohlf 2005). A requirement of geomet-ric 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, thewide shape variation includes appearances, losses and fusion of structures (e.g., posterolateral process of thepalatoquadrate in microhylids, fusion of trabecular horns and suprarostral cartilage in Xenopus laevis), andthis makes possible the definition of only a few comparable landmarks. Twelve landmarks in the chondrocra-nium and 16 in the hyobranchial skeleton are as follows (Fig. 2): Chondrocranium: (1) point of maximumwidth of the base of the trabecular horns; (2) medial point of the palatoquadrate-Meckels cartilage articula-tion; (3) most anterior point of the quadratocranial commissure; (4) most anterior point of the muscular pro-cess of the palatoquadrate; (5) most dorsal point of the muscular process; (6) most lateral, medial point of themuscular process; (7) most posterior point of the muscular process; (8) most anterior point of the subocularfenestra; (9) most anterior point of the otic capsule; (10) most lateral point of the otic capsule; (11) most pos-terior point of the otic capsule; (12) most medial point of the otic capsule; Hyobranchial skeleton: (1) anteriormargin 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 poste-rior point of branchial slit II; (8) most caudal and medial point of ceratobranchial III; (9) most rostral andmedial point of ceratobranchial IV; (10) most caudal point of hypobranchial plates junction; (11) most caudalpoint of basibranchial; (12) lateral point of hypobranchial plate - basibranchial junction; (13) tip of the poste-rior process; (14) most caudal point of ceratobranchial I - hypobranchial plate junction; (15) most caudal pointof ceratobranchial II - hypobranchial plate junction; (16) most caudal point of ceratobranchial III hypobran-chial plate junction.

The configurations of landmarks were next translated, standarized to centroid size = 1, and alignedthrough the generalized Procrustes analysis (GPA) to produce a consensus configuration, with tpsRelw (Rohlf2003). A relative warp analysis (RWA, i.e., principal component analysis on the residuals from superimposi-tion) was performed to obtain a plot of specimens scattered in a space defined by variation axes (the relative



warps). Variation in shapes was depicted with thin-plate spline deformation grids which reveal the modifiedshape compared to the consensus configuration, using tpsSplin (Rohlf 2004). For detailed explanations on thismethodology, see Rohlf and Bookstein (1990), Bookstein (1991), Fink and Zelditch (1995), Monteiro andFurtado 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 tad-poles of each species. A lateral portion of the ceratohyal, B ceratohyal width, CB ceratobranchials area, CH ceratohyal area, HP hypo-branchial area. Landmarks, see definition in text.

For comparative purposes, some measurements with functional correlations with feeding were recordedfor the hyobranchial skeletons: in-lever arm proportion: lateral portion of the ceratohyal (distance between thetip of the lateral process and the articular condyle) projected on the total width of the ceratohyal; ceratohyalarea, defined by the landmarks 14, 1113; hypobranchial area, defined by the landmarks 4, 916; and cerato-branchial area, defined by the landmarks 49, 1416 (Fig. 2). The in-lever arm proportion gives an idea of themechanical advantage of the ceratohyals during the lowering and raising of the buccal floor, and the hyobran-chial areas indicate the relative importance of the suction and filtering processes. The measurements weretaken from drawings or photographs, with Image Tool (Wilcox et al. 1995).

Gut content variation. Correspondence analysis. As was the case with morphological variables, an ordi-nation technique was applied to food variables. Correspondence analysis (CA) is suitable to analyze censusmatrices, 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 abun-dance of food particles of each type or size in each tadpole. The interpretation of the output and plots of CA issimilar to that of other indirect ordination techniques.

Gut content-morphology relationship. Partial canonical phylogenetic ordination. In the data matrix, thereare 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 phy-logenetic structure matrix (assigning 0s and 1s according to their belonging to monophyletic clades); thismatrix can then be employed as an external or covariate matrix in statistical tests. I worked with the phyloge-netic hypothesis proposed for Anura by Frost et al. (2006), and in the case of microhylids, the phylogeny byDonnelly et al. (1990) was considered (Fig. 3). Secondly, the use of ordination axes (PCs, RWs, etc.) as vari-ables in statistical tests implies a problem of non-independence of the scores on the axes. This can be treatedwith permutation methods, which test the significance of variables through resampling.



FIGURE 3. Phylogenetic hypothesis for Anura based in Frost et al. (2006) and Donnelly et al. (1990), employed for phylogeneticcanonical ordination method (Giannini 2003).

I tested the relationship between food size, predator morphological characters, and phylogeny by perform-ing a partial canonical phylogenetic ordination (pCPO; Giannini 2003), a variant of the canonical correspon-dence analysis (CCA). The CCA combines a correspondence analysis with a multiple regression (Ter Braak1986; Jongman et al. 1995; McGarigal et al. 2000) so that given two sets of variables (main and externalmatrices), it ordinates the first set on axes that are linear combinations of variables of the second set. In thisway, the analysis extracts the major gradients in the data that can be accounted for by explanatory variables. Ifa second external matrix is included (partial CCA pCCA or partial CPO if a phylogenetic matrix isinvolved), variation can be partitioned and percentages exclusive and shared by each external matrices areobtained. In this study, the main matrix includes food data; variables are the percentages of food sizesexpressed as a percentage of tadpole body length. The first external matrix joins morphological variables fromthe hyobranchial skeleton, musculature and buccopharyngeal cavity; variables are: hyobranchial skeletonshape (summarized as the scores of specimens on the first relative warps resulting from hyobranchial skeletonRWA; the number of warps retained is such that at least 90% of variation is accumulated), ih/oh ratio, mouthgape, and total number of filtering structures inside the buccal cavity. The chondrocranium shape, quantifiedthrough landmark-based geometric morphometrics, was not included, because the landmarks selected are notrepresentative 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 partiallyredundant with that provided by other variables included in the analysis (e.g., size of muscular process of thepalatoquadrate, described by landmarks 47, is usually associated with the development of the m. orbitohyoi-deus; the articulation between Meckels cartilage and the palatoquadrate, described by landmark 2, gives anapproximate idea of mouth gape). Morphological variables were standarized to fulfill the non-dimensionalityrequired by linear combination. Finally, the second external matrix is a phylogenetic matrix constructed byGiannini (2003) method, considering the anuran phylogeny of Frost et al. (2006). The significance of morpho-logical variables and taxonomic groups was tested through a Monte Carlo permutation test. Including the sig-



nificant variables, a pCPO was performed, to identify variation explained by morphology, by phylogeny, andthe shared variation. The pCPO was performed adding variables successively (forward stepwise), whichyielded 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 morpho-logical variables are placed in a space defined by ordination axes.

Ordination and canonical ordination analyses were performed with CANOCO 4.5 (Ter Braak & Smilauer1997); 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 fromthose that appear in previous studies, complete descriptions for each species are included, as well as a list ofprevious publications.

BUFONIDAE

Chaunus arenarum. Previous literature on the skeleton and musculature of this species includes Fabrezi andVera (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 theselarvae represents 43% of the body length. The maximum width is at the level of posterior part of the subocularbar. The suprarostral cartilage has a single, U-shaped corpus that is fused dorsally to the alae. The alae arewell-defined, ventrally rounded, and bear a well-developed processus dorsalis posterior. The trabecular hornsare 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 trabec-ulae 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 theintertrabecular plate. In the posterior margin of the cranial floor, the notochordal canal reaches 20% of thechondrocranium length. The lateral walls of the chondrocranium are formed by the orbital cartilages. Thechondrocranium is open dorsally, and the frontoparietal fenestra is bordered on both sides by the taeniae tectimarginales. The otic capsules are ovoid, occupy nearly 29% of the chondrocranium total length, and bear anacute anterolateral process. A large fenestra ovalis (45% of capsule length) is located ventrolaterally on eachotic capsule. The otic capsules are dorsally joined by the tectum synoticum. The palatoquadrate is long andrelatively narrow. It has a long, thin articular process, and a wide, dorsally rounded muscular process. Thesubocular bar has a smooth margin and it is posterolaterally rounded. The palatoquadrate attaches to the brain-case via three points: the quadratocranial commissure, the quadratoorbital commissure, and the ascending pro-cess. 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 attach-ment). The lower jaw includes the Meckels and infrarostral cartilages joined by a cartilaginous intermandibu-lar commissure. Meckels cartilages are sigmoid, with dorsomedial and ventromedial processes, and articulatewith the articular process via the retroarticular process. The infrarostral cartilages are short, rectangular andindependent. In the hyobranchial skeleton, the ceratohyals are long and have a tall anterior process, a roundedanterolateral process, an acute lateral process, and a large and wide posterior process; the articular condyle isa rounded, robust projection visible from a dorsal view. The ceratohyals are joined medially by the pars reu-



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

FIGURE 4. Chaunus arenarum, stage 34. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B) Chon-drocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral carti-lage. 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, LPTlateral process of trabecular horn, MC Meckels cartilage, MP muscular process, NC notochordal canal, OC otic capsule, PDP proces-sus dorsalis posterior, PPC posterior process of ceratohyal, PR pars reuniens, QCC quadratocranial commissure, QOC quadratoorbitalcommissure, QP quadratoethmoid process, RP retroarticular process, S spicule, SB subocular bar, SC suprarostral cartilage, SF suboc-ular fenestra, TC terminal commissure, TH trabecular horn, TS tectum synoticum, TTM taenia tecti marginalis, UP urobranchial pro-cess. Scale lines = 1 mm.



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



FIGURE 5. Chaunus arenarum, stage 34. Musculature (A) Dorsal view, superficial plane, (B) Dorsal view, middle plane, (C) Dorsalview, 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 arcuumbranchialium, LMA levator mandibulae articularis, LMEP levator mandibulae externus profundus, LMES levator mandibulae exter-nus 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 abdomi-nis, SA suspensorioangularis, SH suspensoriohyoideus, SO subarcualis obliquus, SRI subarcualis rectus I, SRII-IV subarcualis rectusII-IV, TP tympanopharyngeus. Scale lines = 1 mm.

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

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

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



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 roofarena papilla, C choana, DG dorsal gap, DV dorsal velum, GZ glandular zone, ILP infralabial papilla, IR infrarostrodont, LK lowerkeratodonts, 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 ventralgap, VV ventral velum. Scale lines = 1 mm.

Oral apparatus and buccopharyngeal cavity (N = 2, stage 35. Fig. 6). The width of the oral disc repre-sents nearly 22% of the body length, and gape width reaches 22% of the body length. The oral disc is emar-ginate, with a simple papillar margin interrupted in wide dorsal and ventral gaps; there are a few submarginalpapillae in the commissural region. Papillae are conical, with smooth, rounded tips. The rostrodonts are well-developed 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, mediangap, 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 thereare four pairs of conical postnarial papillae, the two most anterior pairs smaller and closer to each other. Thelateral 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 45tall, conical marginal papillae; numerous pustules are scattered among the papillae. The secretory pits arearranged in a V-shaped display located near the posterior margin of the dorsal velum. The dorsal velum isshort 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, andwith 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



shorter than the lateral one. The prepocket region, on the lateral portion of the ceratohyals, shows numerouspustules and one pair of prepocket papillae. The buccal floor arena is delimited on both sides by 1214 tallpapillae accompanied by numerous pustules and small papillae. The buccal pockets are elongate and transver-sally arranged. The ventral velum is semicircular and supported by spicules. Three main marginal projectionsappear on each side, over each filter plates; the median notch is absent, and secretory pits appear on the edgeof 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 percentagesranged from below 1-2% of the tadpole body length. The abundance of sand-grains in the gut contents sug-gests bottom feeding.

Chaunus spinulosus. Ulloa Kreisel (2003) described the buccopharyngeal cavity of this species; the remainingdata are unpublished.

Chondrocranium and hyobranchial skeleton (N = 5, stages 34 and 36. Fig. 7). The chondrocranium ofthese larvae represents 57% of the body length. The maximum width is at the level of posterior part of the sub-ocular bar. The suprarostral cartilage has a single, U-shaped corpus dorsally fused to the alae. The alae arewell-defined, ventrally rounded, and bear an acute processus dorsalis posterior. The trabecular horns corre-spond to nearly 23% of the total length of the chondrocranium and diverge from the ethmoid plate. They haverelatively straight anterior margins, and on the lateroventral margin, the processus lateralis trabeculae isslightly outlined. The cranial floor is completely cartilaginous with thin cartilage in the central area. Thecarotid foramen is visible, but the craniopalatine foramen is not clearly identifiable, because of light chondri-fication of the intertrabecular plate. On the posterior margin of the cranial floor, the notochordal canal extends19% of the chondrocranium length. The lateral walls of the chondrocranium are formed by the orbital carti-lages. The optic foramen, posteroinferiorly placed, the oculomotor foramen, slightly smaller, and the trochlearforamen, small and dorsally placed, are visible on the posterior part of the orbital cartilage. The chondrocra-nium is dorsally open through the frontoparietal fenestra lined on both sides by the taeniae tecti marginales. Inthe stages analyzed, the taenia tectis transversalis and the taenia tectis medialis are also present. The otic cap-sules are ovoid, occupy nearly 27% of the chondrocranium total length, and bear an acute anterolateral pro-cess. A large fenestra ovalis (44% of the capsule length) is located ventrolaterally on each otic capsule. Theotic capsules are dorsally joined by the tectum synoticum. The palatoquadrate is long and relatively narrow. Ithas a long and thin articular process, and a wide, dorsally rounded muscular process. The subocular bar has asmooth margin, and it is posterolaterally wider and rounded. The palatoquadrate attaches to the braincase viathree points: the quadratocranial commissure, the quadratoorbital commissure, and the ascending process. Thequadratocranial commissure is thin and bears a well-developed, triangular quadratoethmoid process. Theascending process attaches to the braincase ventrally and posteriorly to the oculomotor foramen (low attach-ment). The lower jaw includes Meckels and infrarostral cartilages, joined by a cartilaginous intermandibularcommissure. Meckels cartilages are sigmoid in shape and show well-developed ventromedial and retroarticu-lar 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, ashort 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 nearlyas long as the basibranchial. The basihyal is small, visible as a narrow sliver of cartilage, and the basibranchialis short and bears a short, quadrangular urobranchial process (23% of basibranchial length). The basibranchialis fused to the hyobranchial plates. The hypobranchial plates are flat and triangular, and they articulate medi-ally with a posterior triangular, narrow gap remaining. The ceratobranchials are long, thin, and have numerouslateral projections. They are distally joined by terminal commissures. Four cartilaginous spicules arise dor-sally from each ceratobranchial, the third one being reduced.



FIGURE 7. Chaunus spinulosus, stage 34. Chondrocranium and hyobranchial skeleton (A) Chondrocranium, dorsal view, (B) Chon-drocranium, ventral view, (C) Chondrocranium, lateral view, (D) Hyobranchial skeleton, ventral view, (E) Detail of suprarostral carti-lage. 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 fora-men, CH ceratohyal, FF frontoparietal fenestra, FO fenestra ovalis, HP hypobranchial plate, IC infrarostral cartilage, IMC interman-dibular commissure, LPC lateral process of ceratohyal, LPT lateral process of trabecular horn, MC Meckels cartilage, MP muscularprocess, NC notochordal canal, OC otic capsule, OF oculomotor foramen, OPF optic foramen, PDP processus dorsalis posterior, PFprootic foramen, PPC posterior process of ceratohyal, PR pars reuniens, QCC quadratocranial commissure, QOC quadratoorbital com-missure, QP quadratoethmoid process, RP retroarticular process, S spicule, SB subocular bar, SC suprarostral cartilage, SF subocularfenestra, 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.



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

the whole structure is U-shaped, and in the central region shows a thick, resistant, alcianophilic connective tissue

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

it is formed of parallel, transverse fibers, disposed in a plane nearly perpendicular to the chondrocranial longitudinal axis

...... continued



FIGURE 8. Chaunus spinulosus, stage 34. Musculature (A) Dorsal view, superficial plane, (B) Dorsal view, middle plane, (C) Dorsalview, 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 arcuumbranchialium, LMA levator mandibulae articularis, LMEP levator mandibulae externus profundus, LMES levator mandibulae exter-nus 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 abdomi-nis, RC rectus cervicis, SA suspensorioangularis, SH suspensoriohyoideus, SM submentalis, SO subarcualis obliquus, SRI subarcualisrectus I, SRII-IV subarcualis rectus II-IV, TP tympanopharyngeus. Scale lines = 1 mm.

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 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 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

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

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



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 buccalroof arena papilla, C choana, DG dorsal gap, DV dorsal velum, ILP infralabial papilla, IR infrarostrodont, LK lower keratodonts, LPlingual 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 ventralgap, 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 widthrepresents nearly 24% of the body length, and gape width reaches 23% of the body length. The lateral marginshave deep indentations in the commissural region. The papillar margin is simple with wide dorsal and ventralgaps; 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 sharppoints. The keratodonts are arranged in five rows, two upper (anterior) and three lower (posterior), resulting ina LTRF 2(2)/3. The row A2 is interrupted by a wide, median gap, and P3 is slightly shorter than the otherrows. The keratodonts have an elongate and convex head with 1012 cusps and a sheath shorter and widerthan the head. In the buccal roof, the prenarial arena shows a small, quadrangular ridge accompanied by pus-tules. The choanae are large, obliquely arranged at an angle of 37 from the transversal line. The anterior mar-gin has small prenarial papillae, and the narial valve is scarcely visible. In the postnarial arena there are fourpairs of conical or slightly bifid postnarial papillae. The lateral ridge papillae are well-developed, with threeor four pustulate tips. The median ridge is rectangular, twice as long as wide, and with an irregular free mar-gin. The buccal roof arena is delimited on both sides by 34 tall, conical marginal papillae. Some pustulesappear anteriorly and posteriorly to the papillae. The secretory pits are arranged in a V-shaped array, locatednear the posterior margin of the buccal roof. The dorsal velum is smooth and short. In the buccal floor, poste-



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, thereare four tall, conical, transversally arranged lingual papillae. The prepocket region, on the lateral portion ofthe ceratohyal, has numerous pustules and 12 prepocket papillae. The buccal floor arena is delimited on bothsides by 45 peripheral, tall, conical papillae accompanied by pustules and small papillae. The buccal pocketsare elongate and transversally arranged. The ventral velum is long and supported by spicules; it has three mainpronounced marginal projections on each filter plate, and two small ones on each side of the middle line; themedian 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, frontalview, (B) Detail of left commissure, (C) Detail of the spur, (D) Detail of the serrations of the suprarostrodont, (E) Detail of upper kerat-odonts, (F) Buccal roof, detail of choanae region. C choana, IR infrarostrodont, LK lower keratodonts, LRP lateral ridge papilla, MPmarginal papilla, MR median ridge, S spur.



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 Fab-rezi (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, muscula-ture, oral apparatus, buccal cavity, and feeding of a new set of tadpoles were analyzed. Regarding this latterpaper, 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 suprarostralcartilage. ALPC anterolateral process of ceratohyal, ANP antorbital process, APC anterior process of ceratohyal, ARP articular pro-cess, 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, NCnotochordal canal, OC otic capsule, PF prootic foramen, PPC posterior process of ceratohyal, PR pars reuniens, QCC quadratocranialcommissure, QP quadratoethmoid process, RP retroarticular process, SB subocular bar, SC suprarostral cartilage, SF subocular fenes-tra, TC terminal commissure, TH trabecular horn, UP urobranchial process. Scale lines = 1 mm.



Chondrocranium and hyobranchial skeleton (N = 5, stage 33. Fig. 11). The chondrocranium of these lar-vae represents 32% of the body length, and it shows a robust construction. The maximum width is at the planeof posterior part of the subocular bar. The suprarostral cartilage is a single, posteriorly curved structure with amedian constriction. The region of articulation with the trabecular horns is represented by two dorsal depres-sions. In the middle, ventral part, there is a stout spike ventrally oriented. The trabecular horns are quadrangu-lar, 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 com-pletely cartilaginous, and on its posterior margin, the notochordal canal extends 15% of the chondrocraniumlength. The lateral walls of the chondrocranium are formed by the orbital cartilages. The chondrocranium isdorsally 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 locatedventrolaterally 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 andslightly 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 awell-developed quadratoethmoid process. The ascending process attaches to the braincase below the oculo-motor foramen (low attachment). The lower jaw includes the Meckels and infrarostral cartilages, joined by acartilaginous intermandibular commissure. Meckels cartilages are s

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