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Skeletal development of the direct-developing caecilian Gegeneophis ramaswamii (Amphibia: Gymnophiona: Caeciliidae)

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Abstract

A few previous studies of skeletal and especially skull development in Gymnophiona often provided contradictory results. We studied the development of the skull and vertebral column of Gegeneophis ramaswamii, a direct-developing Indian caeciliid, based on 13 specimens. The chondrocranium forms at (Brauer in Zool Jahrb Anat 12:477-508,1899) stage 38. First dermal and perichondral ossifications occur at stage 40. The first dermal bones to form are the mentomeckelian, dentary, angular, vomer, and premaxillary. These are followed by the coronoid, palatine, pterygoid, maxillary, and the skull-roofing bones. The last occurring dermal ossifications are the parasphenoid and the squamosal. We present evidence for the occurrence of a lacrimal bone. No ectopterygoid, basioccipital, supraoccipital, pleurosphenoid, postorbital, or supratemporal elements were found. We assess the homology of the bones constituting the caecilian skull and discuss the above-mentioned terminologies. The phylogenetic implications of our findings are briefly discussed and we conclude that the evidence from developmental morphology is at present consistent with a monophyletic Lissamphibia of temnospondyl origin.

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References

  • Anderson JS (2001) The phylogenetic trunk: maximal inclusion of taxa with missing data in an analysis of the Lepospondyli (Vertebrata, Tetrapoda). Syst Biol 50:170–193

    Article  PubMed  CAS  Google Scholar 

  • Arratia G, Schultze HP (1991) Palatoquadrate and its ossifications: development and homology within osteichthyans. J Morphol 208:1–81

    Article  Google Scholar 

  • Bartsch P, Gemballa S, Piotrowski T (1997) The embryonic and larval development of Polypterus senegalus Cuvier, 1829; its staging with reference to external and skeletal features, behavior and locomotory habits. Acta Zool 78:309–328

    Article  Google Scholar 

  • de Beer GR (1937) The development of the vertebrate skull. Oxford University Press, Oxford, p 554

    Google Scholar 

  • Billo R, Wake MH (1987) Tentacle development in Dermophis mexicanus (Amphibia, Gymnophiona) with a hypothesis of tentacle origin. J Morphol 192:101–110

    Article  Google Scholar 

  • Boy JA (1986) Studien über die Branchiosauridae (Amphibia: Temnospondyli). I. Neue und wenig bekannte Arten aus dem mitteleuropäischen Rotliegenden (?oberstes Karbon bis unteres Perm). Paläont Z 60:131–166

    Google Scholar 

  • Brand DJ (1956) The cranial morphology of Scolecomorphus ulugurensis (Barbour and Loveridge). Ann Univ Stellenbosch 32:1–25

    Google Scholar 

  • Brauer A (1899) Beiträge zur Kenntniss der Entwicklung und Anatomie der Gymnophionen. Zool Jahrb Anat 12:477–508

    Google Scholar 

  • Carrol RL, Currie PJ (1975) Microsaurs as possible apodan ancestors. Zool J Linn Soc 57:229–247

    Google Scholar 

  • Carroll RL (2000): Eocaecilia and the Origin of Caecilians. In: Heatwole H, Carroll RL (eds) Amphibian biology, vol 4. Palaeontology: the evolutionary history of amphibians. Chipping Norton, Surrey Beatty, pp 1402–1411

  • Duellmann WE, Trueb L (1986) Biology of amphibians. McGraw–Hill Book Co., New York, p 670

    Google Scholar 

  • Dünker N, Wake MH, Olson WM (2000) Embryonic and larval development in the caecilian Ichthyophis kohtaoensis (Amphibia, Gymnophiona): a staging table. J Morphol 243:3–34

    Article  PubMed  Google Scholar 

  • Eifertinger L (1933) Die Entwicklung des knöchernen Unterkiefers von Hypogeophis Beitrag zur Kenntnis der Gymnophionen XX. Z Anat Entwicklungsgesch 101:534–552

    Article  Google Scholar 

  • Gaupp E (1906) Die Entwickelung des Kopfskelettes. In: Hertwig O (ed) Handbuch der Vergleichenden und Experimentellen Entwickelungslehre der Wirbeltiere. G Fischer Verlag, Jena, pp 573–874

    Google Scholar 

  • Goodrich ES (1930) Studies on the structure and development of vertebrates. Macmillan, London, p 837

    Google Scholar 

  • Hanken J, Klymkowsky MW, Summers CH, Seufert W, Ingebrigtsen N (1992) Cranial ontogeny in the direct-developing frog, Eleutherodactylus coqui (Anura: Leptodactylidae), analyzed using whole-mount immunohistochemistry. J Morphol 211:95–118

    Article  PubMed  CAS  Google Scholar 

  • Hass CA, Nussbaum RA, Maxson LR (1993) Immunological insights into the evolutionary history of caecilians (Amphibia: Gymnophiona): relationships of the Seychellean caecilians and a preliminary report on family-level relationships. Herpetol Monogr 7:56–63

    Article  Google Scholar 

  • Himstedt W, Simon D (1995) Sensory basis of foraging behaviour in the caecilian Ichthyophis kohtaoensis (Amphibia: Gymnophiona). Herpetol J 5:266–270

    Google Scholar 

  • Jarvik E (1980) Basic structure and evolution of vertebrates, vol I. Academic, New York, pp 575

  • Kingsley JS (1902) The systematic position of the caecilians. Tufts College Studies, Sci Ser No 7:323–344

    Google Scholar 

  • Laurin M (1998) The importance of global parsimony and historical bias in understanding tetrapod evolution. Part I. Systematics, middle ear evolution and jaw suspension. Ann Sci Nat 1998:1–42

  • Lawson R (1963) The anatomy of Hypogeophis rostratus Cuvier. Part I. The skin and skeleton. Proc Univ Durham Phil Soc 13A:254–273

    Google Scholar 

  • Lebedkina NS (1979) Evolyuziya cherepa amfibij K problem’e morfologicheskoj intergrazij. Nauka, Moskwa, p 283

    Google Scholar 

  • Løvtrup S (1985) On the classification of the taxon Tetrapoda. Syst Zool 34:463–470

    Article  Google Scholar 

  • Marcus H (1933) Zur Entstehung des Unterkiefers von Hypogeophis Beitrag zur Kenntnis der Gymnophionen XX. Anat Anz 77:178–184

    Google Scholar 

  • Marcus H, Stimmelmayr E, Porsch G (1935) Die Ossifikation des Hypogeophisschädels Beitrag zur Kenntnis der Gymnophionen XXV. Gegenbaurs Morphol Jb 76:375–420

    Google Scholar 

  • Marks SB, Collazo A (1998) Direct development in Desmognathus aeneus (Caudata: Plethodontidae): a staging table. Copeia 1998:637–648

    Article  Google Scholar 

  • Milner AR (1988) The relationships and origin of living amphibians. In: Benton MJ (ed) The phylogeny and classification of the tetrapods, vol 1: Amphibians, reptiles, birds. Systematics association special, vol 35A, Clarendon Press, Oxford, pp 59–102

  • Milner AR (1993) The paleozoic relatives of lissamphibians. Herpetol Monogr 7:8–27

    Article  Google Scholar 

  • Milner AR, Sequeira SEK (1994) The temnospondyl amphibians from the Viséan of East Kirkton, Scotland. Trans Roy Soc Edinb 84:331–361

    Google Scholar 

  • Müller J (1831) Kiemenlöcher an einer jungen Coecilia hypocyanea im Museum der Naturgeschichte zu Leyden beobachtet. Isis von Oken 24:709–710

    Google Scholar 

  • Norris HW, Hughes SP (1918) The cranial and anterior spinal nerves of the caecilian amphibians. J Morphol 31:488–560

    Google Scholar 

  • Nussbaum RA (1977) Rhinatrematidae: a new family of caecilians (Amphibia: Gymnophiona). Occas Pap Mus Zool Univ Mich 682:1–30

    Google Scholar 

  • Nussbaum RA (1979) The taxonomic status of the caecilian genus Uraeotyphlus Peters. Occas Pap Mus Zool Univ Mich 687:1–20

    Google Scholar 

  • Nussbaum RA, Gans C (1980) On the Ichthyophis (Amphibia: Gymnophiona) of Sri Lanka. Spolia Zeylanica 35:137–154

    Google Scholar 

  • Parker HW (1958) Caecilians of the Seychelles Islands with description of a new subspecies. Copeia 1958:71–76

    Article  Google Scholar 

  • Patterson C (1977) Cartilage bones, dermal bones, and membrane bones, or the exoskeleton versus the endoskeleton. In: Andrews SM, Miles RS, Walker, AD (eds) Problems in vertebrate evolution. Academic, London, pp 77–121

    Google Scholar 

  • Peter K (1898) Die Entwicklung und funktionelle Gestaltung des Schädels von Ichthyophis glutinosus. Morphol Jahrb 25:555–628

    Google Scholar 

  • Peters WCH (1880) Über die Eintheilung der Caecilien und insbesondere über die Gattungen Rhinatrema und Gymnopis. Mber Königl Preuss Akad Wiss Berlin 1879 (Nov):924–943

    Google Scholar 

  • Pillai RS, Ravichandran MS (1999) Gymnophiona (Amphibia) of India: a taxonomic study. Rec Zool Survey India, Occ Paper 172:1–117

    Google Scholar 

  • Ramaswami LS (1947) Apodous Amphibia from the Eastern Ghats, South India. Curr Sci 16:8–10

    Google Scholar 

  • Ramaswami LS (1948) The chondrocranium of Gegenophis [sic] (Apoda, Amphibia). Proc Zool Soc Lond 118:752–760

    Google Scholar 

  • Ramaswamii LS (1943) An account of the head morphology of Gegeneophis carnosus (Beddome, Apoda. J Mysore Univ 3:205–220

    Google Scholar 

  • Reiss J (1996) Palatal metamorphosis in basal caecilians (Amphibia: Gymnophiona) as evidence for lissamphibian monophyly. J Herpetol 30:27–39

    Article  Google Scholar 

  • Romeis B (1989) Mikroskopische Technik. 17 Aufl. Urban und Schwarzenberg, München, Wien, Baltimore

    Google Scholar 

  • Ruta M, Coates MI, Quicke DLJ (2003) Early tetrapod relationships revisited. Biol Rev 78:251–345

    Article  PubMed  Google Scholar 

  • Sammouri R, Renous S, Exbrayat JM, Lescure J (1990) Développement embryonnaire de Typhlonectes compressicaudus [sic] (Amphibia, Gymnophiona). Ann Sci Nat Zool Paris 11:135–163

    Google Scholar 

  • Sarasin P, Sarasin F (1887–1890) Ergebnisse Naturwissenschaftlicher Forschungen auf Ceylon in den Jahren 1884–1886. Band 2: Zur Entwicklungsgeschichte und Anatomie der ceylonesischen Blindwühle Ichthyophis glutinosus. C.W. Kreidel’s Verlag, Wiesbaden, pp 263

  • Schmalhausen II (1968) The origin of terrestrial vertebrates. Academic, New York

    Google Scholar 

  • Schoch RR (2002) The early formation of the skull in extant and Paleozoic amphibians. Paleobiology 28:278–296

    Article  Google Scholar 

  • Schoch RR, Milner AR (2000) Stereospondyli. In: Wellnhofer P (ed): Handbuch der Paläoherpetologie, Vol 3B Friedrich Pfeil Verlag, München, pp 1–203

  • Seba A (1735) Locupeltissimi rerum naturalium Thesauri. Vol 2, Amsterdam

  • Sokol O (1981) The larval chondrocranium of Pelodytes punctatus, with a review of tadpole chondrocrania. J Morphol 169:161–183

    Article  Google Scholar 

  • Stadtmüller F (1936) Kranium und Visceralskelett der Stegocephalen und Amphibien. In: Bölk L, Göppert E, Kallius E, Lubosch W (eds) Handbuch der Vergleichenden Anatomie der Wirbeltiere. Urban und Schwarzenberg, Berlin, pp 501–698

    Google Scholar 

  • Starck D (1975) Embryologie. Georg Thieme, Stuttgart, p 704

    Google Scholar 

  • Starck D (1979) Vergleichende Anatomie der Wirbeltiere auf evolutionsbiologischer Grundlage, vol. 2: Das Skelettsystem. Springer, Berlin, Heidelberg, New York, p 776

  • Taylor EH (1960) On the caecilian species Ichthyophis monochrous and Ichthyophis glutinosus and related species. Univ Kans Sci Bull 40:37–120

    Google Scholar 

  • Taylor EH (1964) A new species of caecilian from India. Senck Biol 45:227–231

    Google Scholar 

  • Taylor EH (1968) The caecilians of the world: a taxonomic review. University of Kansas Press, Lawrence, pp 848

    Google Scholar 

  • Taylor EH (1969a) A new family of African Gymnophiona. Univ Kans Sci Bull 48:297–305

    Google Scholar 

  • Taylor EH (1969b) Skulls of Gymnophiona and their significance in the taxonomy of the group. Univ Kans Sci Bull 48:585–687

    Google Scholar 

  • Taylor WR, Van Dyke GC (1985) Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium 9:107–119

    Google Scholar 

  • Townsend DS, Stewart MM (1985) Direct development in Eleutherodactylus coqui (Anura: Leptodactylidae): a staging table. Copeia 1985:423–436

    Article  Google Scholar 

  • Trueb L (1993) Patterns of cranial diversity among the Lissamphibia. In: Hanken J, Hall BK (eds) The skull, volume 2: Patterns of structural and systematic diversity. University of Chicago Press, Chicago and London, pp 255–343

  • Trueb L, Cloutier R (1991) A phylogenetic investigation of the inter- and intrarelationships of the Lissamphibia (Amphibia: Temnospondyli). In: Schultze H-P, Trueb L (eds) Origin of the higher groups of tetrapods: controversy and consensus. Cornell University Press, Ithaca, pp 175–188

    Google Scholar 

  • Venkatesh B, Erdmann MV, Brenner S (2001) Molecular synapomorphies resolve evolutionary relationships of extant jawed vertebrates. Proc Nat Acad Sci 98:11382–11387

    Article  PubMed  CAS  Google Scholar 

  • Visser MHC (1963) The cranial morphology of Ichthyophis glutinosus (Linné) and Ichthyophis monochrous (Bleeker). Ann Univ Stellenbosch. A 38:67–102

    Google Scholar 

  • Wacker K, Bartsch P, Clemen G (2001) The development of the tooth pattern and dentigerous bones in Polypterus senegalus (Cladistia, Actinopterygii). Ann Anat 183:37–52

    Article  PubMed  CAS  Google Scholar 

  • Wake MH (1987) A new genus of African caecilian (Amphibia: Gymnophiona). J Herpetol 21:6–15

    Article  Google Scholar 

  • Wake MH (1989) Metamorphosis of the hyobranchial apparatus in Epicrionops (Amphibia: Gymnophiona: Rhinatrematidae): replacement of bone by cartilage. Ann Sci nat Zool 10:171–182

    Google Scholar 

  • Wake MH (2003) The osteology of caecilians. In: Heatwole H, Davis, M (eds) Amphibian Biology, vol 5 Osteology. Surrey Beatty, Chipping Norton, pp 1809–1876

  • Wake MH, Hanken J (1982) Development of the skull of Dermophis mexicanus (Amphibia: Gymnophiona), with comments on skull kinesis and amphibian relationships. J Morphol 173:203–223

    Article  Google Scholar 

  • Wake DB, Hanken J (1996) Direct development in the lungless salamanders: what are the consequences for developmental biology, evolution and phylogenesis? Int J Dev Biol 40:859–869

    PubMed  CAS  Google Scholar 

  • Wake MH, Exbrayat J-M, Delsol M (1985) The development of the chondrocranium of Typhlonectes commpressicaudus [sic] (Gymnophiona), with comparison to other species. J Herpetol 19:68–77

    Article  Google Scholar 

  • Wiedersheim R (1879) Die Anatomie der Gymnophionen. Gustav Fischer, Jena, pp 101

    Google Scholar 

  • Wilkinson M (1989) On the status of Nectocaecilia fasciata Taylor with a discussion of the phylogeny of the Typhlonectidae (Amphibia: Gymnophiona). Herpetologica 45:23–36

    Google Scholar 

  • Wilkinson M, Nussbaum RA (1992) Taxonomic status of Pseudosiphonops ptychodermis Taylor and Mimosiphonops vermiculatus Taylor (Amphibia: Gymnophiona: Caeciliaidae) with description of a new species. J Nat Hist 26:675–688

    Article  Google Scholar 

  • Wilkinson M, Nussbaum RA (1997) Comparative morphology and evolution of the lungless caecilian Atretochoana eiselti (Taylor) (Amphibia: Gymnophiona: Typhlonectidae). Biol J Linn Soc 62:39–109

    Article  Google Scholar 

  • Wilkinson M, Nussbaum RA (1999) Evolutionary relationships of the lungless caecilian Atretochoana eiselti (Amphibia: Gymnophiona: Typhlonectidae). Zool J Linn Soc 126:191–223

    Article  Google Scholar 

  • Wilkinson M, Sheps JA, Oommen OV, Cohen BL (2002) Phylogenetic relationships of Indian caecilians (Amphibia: Gymnophiona) inferred from mitochondrial rRNA gene sequences. Mol Phyl Evo 23:401–407

    Article  CAS  Google Scholar 

  • Zardoya R, Meyer A (2000) Mitochondrial evidence on the phylogenetic position of caecilians (Amphibia: Gymnophiona). Genetics 155:765–77

    PubMed  CAS  Google Scholar 

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Acknowledgements

The technical assistance of Jutta Zeller, Gabriele Drescher, Vera Heinrich, and Nils Hoff (all Institute of Zoology, Berlin) is gratefully acknowledged. Ulrich Zeller provided resources for laboratory work at the Institute of Zoology, MfN. Peter Olson (London) is thanked for his help with the PC and DCI microscopy. We further wish to thank Ralf Britz, David Gower, Stefan Richter, Rainer Schoch, and Mark Wilkinson and two anonymous reviewers for fruitful discussions and very valuable comments on earlier drafts of the manuscript.

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Müller, H., Oommen, O.V. & Bartsch, P. Skeletal development of the direct-developing caecilian Gegeneophis ramaswamii (Amphibia: Gymnophiona: Caeciliidae). Zoomorphology 124, 171–188 (2005). https://doi.org/10.1007/s00435-005-0005-6

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