Skip to main content
SpringerLink
Log in

Feeding in Amphibians: Evolutionary Transformations and Phenotypic Diversity as Drivers of Feeding System Diversity

  • Chapter
  • First Online:
Feeding in Vertebrates

Part of the book series: Fascinating Life Sciences ((FLS))

Abstract

Amphibians are different from most other tetrapods because they have a biphasic life cycle, with larval forms showing a dramatically different cranial anatomy and feeding strategy compared to adults. Amphibians with their exceptional diversity in habitats, lifestyles and reproductive modes are also excellent models for studying the evolutionary divergence in feeding systems. In the present chapter, we review the literature on amphibian feeding anatomy and function published since 2000. We also present some novel unpublished data on caecilian feeding biomechanics. This review shows that over the past two decades important new insights in our understanding of amphibian feeding anatomy and function have been made possible, thanks to a better understanding of the phylogenetic relationships between taxa, analyses of development and the use of biomechanical modelling. In terms of functional analyses, important advances involve the temperature-dependent nature of tongue projection mechanisms and the plasticity exhibited by animals when switching environments (land to water) during their lifetime. Understanding the relationships between cranial and hyobranchial diversity and feeding function, and how these relationships are dependent on lifestyle, habitat use or reproductive mode are questions that remain to be answered. Given the availability of massive online databases with µCT data and robust comprehensive phylogenies, these analyses are becoming possible. Unfortunately, quantitative studies on muscular anatomy, essential to link variation in form to variation in function using modelling approaches, have lagged behind. Future studies quantifying feeding across a wide range of species will provide critical insights into the selective pressures underlying the evolution of the staggering diversity in feeding form and function of amphibians.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adams DC (2010) Parallel evolution of character displacement driven by competitive selection in terrestrial salamanders. BMC Evol Biol 10:1–10

    Google Scholar 

  • Adams DC (2011) Quantitative genetics and evolution of head shape in Plethodon salamanders. Evol Biol 38:278–286

    Google Scholar 

  • Alcalde L, Vera Candioti F, Kolenc F, Borteiro C, Baldo D (2011) Cranial anatomy of tadpoles of five species of Scinax (Hylidae, hylinae). Zootaxa 2787:19–36

    Google Scholar 

  • Anderson CV, Deban SM (2010) Ballistic tongue projection in chameleons maintains high performance at low temperature. Proc Natl Acad Sci USA 107:5495–5499

    CAS  Google Scholar 

  • Anderson CV, LarghiNP Deban SM (2014) Thermal effects on the performance, motor control and muscle dynamics of ballistic feeding in the salamander Eurycea guttolineata. J Exp Biol 217:3146–3158

    PubMed  Google Scholar 

  • Anderson CV, Sheridan T, Deban SM (2012) Scaling of the ballistic tongue apparatus in chameleons. J Morphol 273:1214–1226

    PubMed  Google Scholar 

  • Anzeraey A, Aumont M, Decamps T, Herrel A, Pouydebat E (2017) The effect of food properties on grasping and manipulation in the aquatic frog, Xenopus laevis. J Exp Biol 220:4486–4491

    PubMed  Google Scholar 

  • Bansil R, Turner BS (2006) Mucin structure, aggregation, physiological functions and biomedical applications. Curr Opin Colloid Interface Sci 11:164–170. https://doi.org/10.1016/j.cocis.2005.11.001

    Article  CAS  Google Scholar 

  • Bardua C, Evans SE, Goswami A (2018) Phylogeny, ecology and deep time: 2D outline analysis of anuran skulls from the Early Cretaceous to recent. Palaeontology 1–15

    Google Scholar 

  • Bardua C, Wilkinson M, Gower DJ, Sherratt E, Goswami A (2019) Morphological evolution and modularity of the caecilian skull. BMC Evol Biol 19:1–24

    Google Scholar 

  • Barnes WJP, Oines C, Smith JM (2006) Whole animal measurements of shear and adhesive forces in adult tree frogs: insights into underlying mechanisms of adhesion obtained from studying the effects of size and scale. J Comp Physiol A 192:1179–1191

    Google Scholar 

  • Bemis WE, Schwenk K, Wake MH (1983) Morphology and function of the feeding apparatus in Dermophis mexicanus (Amphibia, gymnophiona). Zool J Linn Soc 77:75–96

    Google Scholar 

  • Birinyi A, Racz N, Kecskes S, Matesz C, Kovalecz G (2018) Neural circuits underlying jaw movements for the prey-catching behavior in frog: distribution of vestibular afferent terminalson motoneurons supplying the jaw. Brain Struct Funct 223:1683–1696

    PubMed  Google Scholar 

  • Biton R, Geffen E, Vences M, Cohen O, Bailon S, Rabinovich R, Malka Y, Oron T, Boistel R, Brumfeld V, Gafny S (2013) The rediscovered Hula painted frog is a living fossil. Nat Com 4:1959

    Google Scholar 

  • Biton R, Boistel R, Rabinovich R, Gafny S, Brumfeld V, Bailon S (2016) Osteological observations on the alytid Anura Latonia nigriventer with comments on functional morphology, biogeography and evolutionary history. J Morphol 277:1131–1145

    PubMed  Google Scholar 

  • Blackburn DC, Bickford DP, Diesmos AC, Iskandar DT, Brown RM (2010) An ancient origin for the enigmatic flat-headed frogs (Bombinatoridae: Barbourula) from the Islands of Southeast Asia. Plos One 5:e12090

    PubMed  PubMed Central  Google Scholar 

  • Bossuyt F, Milinkovitch MC (2000) Convergent radiations in Madagascan and Asian ranid frogs reveal covariation between larval and adult traits. Proc Natl Acad Sci USA 97:6585–6590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Buckley D, Wake MH, Wake DB (2010) Comparative skull osteology of Karsenia koreana (Amphibia, caudata, plethodontidae). J Morphol 271:533–558

    PubMed  Google Scholar 

  • Carreño CA, Nishikawa KC (2010) Aquatic feeding in pipid frogs: the use of suction for prey capture. J Exp Biol 213:2001–2008

    PubMed  PubMed Central  Google Scholar 

  • Carroll RL (2007) The palaeozoic ancestry of salamanders, frogs and caecilians. Zool J Linn Soc 150:1–140

    Google Scholar 

  • Celli J, Gregor B, Turner B, Afdhal NH, Bansil R, Erramilli S (2005) Viscoelastic properties and dynamics of porcine gastric mucin. Biomacromol 6:1329–1333

    CAS  Google Scholar 

  • Clemen G, Greven H (2018) Long-term effects of arrested metamorphosis on dental systems in Salamandra salamandra (Salamandridae: urodela). Vertebr Zool 68:143–155

    Google Scholar 

  • Corbacho F, Nishikawa KC, Weerasuriya A, Liaw J-S, Arbib MA (2005) Schema-based learning of adaptable and flexible prey-catching in anurans. I. The basic architecture. Biol Cybern. https://doi.org/10.1007/s00422-005-0013-0

    PubMed  Google Scholar 

  • Creton C (2003) Pressure-sensitive adhesives: an introductory course. MRS Bull 28:434–439

    CAS  Google Scholar 

  • Dalrymple GH, JuterbockJE La Valley, AL (1985) Function of the atlanto-mandibular ligaments of desmognathine salamanders. Copeia 1985:254–257

    Google Scholar 

  • Darda DM, Wake DB (2015) Osteological variation among extrememorphological forms in the Mexicansalamander genus Chiropterotriton (Amphibia: plethodontidae): morphological evolution and homoplasy. PLoS One 10(6):e0127248. https://doi.org/10.1371/journal.pone.0127248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Groot JH, van Leeuwen JL (2004) Evidence for an elastic projection mechanism in the chameleon tongue. Proc Biol Sci 271:761–770

    PubMed  PubMed Central  Google Scholar 

  • Dean MN (2003) Suction feeding in the pipid frog, Hymenochirus boettgeri: kinematic and behavioural considerations. Copeia 2003:879–886

    Google Scholar 

  • Deban SM (2003) Constraint and convergence in the evolution of salamander feeding. In: Gasc J-P, Casinos A, Bels VL (eds) Vertebrate biomechanics and evolution. BIOS Scientific Publishers, Oxford, pp 163–180

    Google Scholar 

  • Deban SM, Bloom SV (2018) Ballistic tongue projection in a miniaturized salamander. J Exp Zool A 2018:1–10. https://doi.org/10.1002/jez.2171

    Article  Google Scholar 

  • Deban SM, Dicke U (2004) Activation patterns of the tongue-projector muscle during feeding in the imperial cave salamander, Hydromantes imperialis. J Exp Biol 207:2071–2081

    PubMed  Google Scholar 

  • Deban SM, Lappin AK (2011) Thermal effects on the dynamics and motor control of ballistic prey capture in toads: maintaining high performance at low temperature. J Exp Biol 214:1333–1346

    PubMed  Google Scholar 

  • Deban SM, Marks SB (2002) Metamorphosis and evolution of feeding behavior in salamanders of the family plethodontidae. Zool J Linn Soc 134:375–400

    Google Scholar 

  • Deban SM, Nishikawa KC (1992) The kinematics of prey capture and the mechanism of tongue protraction in the green tree frog hyla cinerea. J Exp Biol 170:235–256

    Google Scholar 

  • Deban SM, O’Reilly JC (2005) The ontogeny of feeding kinematics in a giant salamander Cryptobranchus alleganiensis: does current function or phylogenetic relatedness predict the scaling patterns of movement? Zool 108:155–167

    Google Scholar 

  • Deban SM, Olson WM (2002) Suction feeding by a tiny predatory tadpole. Nat 420:41–42

    CAS  Google Scholar 

  • Deban SM, Richardson JC (2011) Cold-blooded snipers: thermal independence of ballistic tongue projection in the salamander Hydromantes platycephalus. J Exp Zool 315:618–630

    Google Scholar 

  • Deban SM, Richardson JC (2017) A peculiar mechanism of bite-force enhancement in lungless salamanders revealed by a new geometric method for modeling muscle moments. J Exp Biol 220:3588–3597

    PubMed  Google Scholar 

  • Deban SM, Scales JA (2016) Dynamics and thermal sensitivity of ballistic and non-ballistic feeding in salamanders. J Exp Biol 219:431–444

    PubMed  Google Scholar 

  • Deban SM, Wake DB (2000) Aquatic Feeding in salamanders. In: Schwenk K (ed) Feeding: form, function and evolution in tetrapod vertebrates. Academic Press, San Diego, pp 65–94

    Google Scholar 

  • Deban SM, Wake DB, Roth G (1997) Salamander with a ballistic tongue. Nat 389:27–28

    CAS  Google Scholar 

  • Deban SM, O’Reilly JC, Nishikawa KC (2001) The evolution of the motor control of feeding in amphibians. Am Zool 41:1280–1298

    Google Scholar 

  • Deban SM, O’Reilly JC, Dicke U, van Leeuwen JL (2007) Extremely high-power tongue projection in plethodontid salamanders. J Exp Biol 210:655–667

    PubMed  Google Scholar 

  • Delêtre M, Measey GJ (2004) Sexual selection vs ecological causation in a sexually dimorphic caecilian, schistometopum thomense (Amphibia, gymnophiona, caeciliidae). Ethol Ecol Evol 16:243–253

    Google Scholar 

  • Denoël M (2002) Paedomorphosis in the alpine newt (Triturus alpestris): decoupling behavioural and morphological change. Behav Ecol Sociobiol 52:394–399

    Google Scholar 

  • Denoël M (2004) Feeding performance in heterochronic alpine newts is consistent with trophic niche and maintenance of polymorphism. Ethol 110:127–136

    Google Scholar 

  • Denoël M, Whiteman HW, Wissinger SA (2006) Temporal shift of diet in alternative cannibalistic morphs of the tiger salamander. Biol J Linn Soc 89:373–382

    Google Scholar 

  • Duellman WE, Lizana M (1994) Biology of a sit-and-wait predator, the leptodactylid frog Ceratophrys cornuta. Herpetol 50:51–64

    Google Scholar 

  • Ehmcke J, Clemen G (2000) The structure and development of the skull of CostaRican plethodontid salamanders (Amphibia: urodela). Ann Anat 182:537–547

    CAS  PubMed  Google Scholar 

  • Ehmcke J, Clemen G (2003) The skull structure of six species of Mesoamerican plethodontid salamanders (Amphibia, urodela). Ann Anat 185:253–261

    PubMed  Google Scholar 

  • Emerson SB, Diehl D (1980) Toe pad morphology and mechanisms of sticking in frogs. Biol J Linn Soc 13:199–216

    Google Scholar 

  • Ericksson R, Olsson L (2004) Patterns of spatial and temporal visceral arch muscle development in the Mexican axolotl (Ambystoma mexicanum). J Morphol 261:131–140

    Google Scholar 

  • Fabrezi M, Quinzio SI, Goldberg J, Cruz JC, Pereyra MC, Wassersug RJ (2016) Developmental changes and noveltiesin ceratophryid frogs. EvoDevo 7:5

    PubMed  PubMed Central  Google Scholar 

  • Fernandez E, Irish F, Cundall D (2017) How a frog, Pipa pipa, succeeds or fails in catching fish. Copeia 105:108–119

    Google Scholar 

  • Fowler JE, Kleinteich T, Franz J, Jaye C, Fischer DA, Gorb SN, Weidner T, Baio JE (2018) Surface chemistry of the frog sticky-tongue mechanism. Biointerphases 13:06E408. https://doi.org/10.1116/1.5052651

    Article  PubMed  Google Scholar 

  • Fritz SA, Rahbek C (2012) Global patterns of amphibian phyloenetic diversity. J Biogeogr 39:1373–1382

    Google Scholar 

  • Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CFB, De Sa RA, Channing A, Wilkinson M, Donnellan SC, Raxworthy CJ, Campbell JA, Blotto BL, Moler P, Drewes RC, Nussbaum RA, Lynch JD, Green DM, Wheeler WC (2006) The amphibian tree of life. Bull Amer Mus Nat Hist 297:1–370

    Google Scholar 

  • Gaborieau O, Measey GJ (2004) Termitivore ordetritivore? A quantitative investigation into the diet of the East African caecilian Boulengerula taitanus (Amphibia: gymnophiona: caeciliidae). Anim Biol 54:45–56

    Google Scholar 

  • Gans C, Gorniak GC (1982a) How does the toad flip its tongue? Test of two hypotheses. Sci 216:1335–1337

    CAS  Google Scholar 

  • Gans C, Gorniak GC (1982b) Functional morphology of lingual protrusion in marine toads (Bufo marinus). Am J Anat 163:195–222

    CAS  PubMed  Google Scholar 

  • Gray LA, O’Reilly JC, Nishikawa KC (1997) Evolution of forelimb movement patterns for prey manipulation in anurans. J Exp Zool 277:417–424

    CAS  PubMed  Google Scholar 

  • Greven H, Richter H, Clemen G (2013) Formation of the secondary tongue in Hynobius leechi and Ambystoma mexicanum (Amphibia: urodela). Vert Zool 63:217–232

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Haas A, Hertwig S, Das I (2006) Extreme tadpoles: the morphology of the fossorial megophryid larva, leptobrachella mjobergi. Zool 109:26–42

    Google Scholar 

  • Haas A, Pohlmeyer J, McLeod DS, Kleinteich T, Hertwig ST, Das I, Buchholz DR (2014) Extreme tadpoles II: the highly derived larval anatomy of Occidozyga baluensis (Boulenger, 1896), an obligate carnivoroustadpole. Zoomorphology 133:321–342

    Google Scholar 

  • Harding S, Rowe A, Creeth J (1983) Further evidence for a flexible and highly expanded spheroidal model for mucus glycoproteins in solution. Biochem J 209:893–896

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heiss E (2017) The alpine “axolotl”: a remarkable example of phenotypic plasticity in the alpine newt, Ichthyosaura alpestris. Salamandra 53:137–141

    Google Scholar 

  • Heiss E, De Vylder M (2016) Dining dichotomy: aquatic and terrestrial prey capture behavior in the Himalayan newt Tylototriton verrucosus. Biol Open 5:1500–1507

    PubMed  PubMed Central  Google Scholar 

  • Heiss E, Natchev N, Gumpenberger M, Weissenbacher A, Van Wassenbergh S (2013a) Biomechanics and hydrodynamics of prey capture in the Chinese giant salamander reveal a high-performance jaw-powered suction feeding mechanism. J R Soc Interface 10:20121028

    PubMed  PubMed Central  Google Scholar 

  • Heiss E, Aerts P, Van Wassenbergh S (2013b) Masters of change: seasonal plasticity in the prey-capture behavior of the alpine newt Ichthyosaura alpestris (Salamandridae). J Exp Biol 216:4426–4434

    PubMed  Google Scholar 

  • Heiss E, Aerts P, Van Wassenbergh S (2015) Flexibility is everything: prey capture throughout the seasonal habitat switches in the smooth newt Lissotriton vulgaris. Org Divers Evol 15:127–142

    PubMed  Google Scholar 

  • Heiss E, Handschuh S, Aerts P, Van Wassenbergh S (2016) Musculoskeletal architecture of the prey-capture apparatus in salamandrid newts with multiphasic lifestyle: does anatomy change during the seasonal habitat switches? J Anat 228:757–770

    PubMed  PubMed Central  Google Scholar 

  • Herrel A, Measey GJ (2012) Feeding underground: kinematics of feeding in caecilians. J Exp Zool A 317:533–539

    Google Scholar 

  • Herrel A, Meyers JJ, Nishikawa KC, De Vree F (2001) Morphology and histochemistry of the hyolingual apparatus in chameleons. J Morphol 249:154–170

    CAS  PubMed  Google Scholar 

  • Herrel A, Meyers JJ, Timmermans J-P, Nishikawa KC (2002) Supercontracting muscle: producing tension over extreme muscle lengths. J Exp Biol 205:2167–2173

    PubMed  Google Scholar 

  • Herrel A, Deban SM, Schaerlaeken V, Timmermans J-P, Adriaens D (2009) Are morphological specializations of the hyolingual system in chameleons and salamanders tuned to demands on performance? Physiol Biochem Zool 82:29–39

    PubMed  Google Scholar 

  • Im S-Y, Je S-H, Lee J-H (2015) Tongue movement and role of frenulum linguae effecting tongue movement during prey capture in Rana nigromaculata. Appl Microsc 45:74–79

    Google Scholar 

  • Irschick DJ, Herrel A, Vanhooydonck B (2006) Whole-organism studies of adhesion in pad-bearing lizards: creative evolutionary solutions to functional problems. J Comp Physiol A 192:1169–1177

    Google Scholar 

  • Ivanović A, Arntzen JW (2014) Evolution of skull and body shape in Triturus newts reconstructed from three-dimensional morphometricdata and phylogeny. Biol J Linn Soc 113:243–255

    Google Scholar 

  • Ivanović A, Arntzen JW (2018) Evolution of skull shape in the family salamandridae (Amphibia: caudata). J Anat 232:359–370

    PubMed  Google Scholar 

  • Ivanović A, Kalezić ML (2010) Testing the hypothesis of morphological integration on a skull of a vertebrate with a biphasic life-cycle: a case-study of the alpine newt. J Exp Zool B 314:527–538

    Google Scholar 

  • Iwasaki S (2002) Evolution of the structure and function of the vertebrate tongue. J Anat 201:1–13

    PubMed  PubMed Central  Google Scholar 

  • Iwasaki S, Iwabuchi Y, Okumura Y (1998) Histological and ultrastructural studies of the effects of tachykinins on protein secretion from the lingual epithelium and the lingual gland of the Tokyo daruma pond frog (Rana porosa porosa). Arch Oral Biol 43:463–471

    CAS  PubMed  Google Scholar 

  • Jefferson DM, Ferrari MCO, Mathis A, Hobson KA, Britzke ER, Crane AL, Blaustein AR, Chivers DP (2014) Shifty salamanders: transient trophic polymorphism and cannibalism within natural populations of larval ambystomatid salamanders. Front Zool 11:76

    PubMed  PubMed Central  Google Scholar 

  • Johnson K, Quiggins J, Barnfield R, Jennings DH (2015) Jaw muscle development and metamorphosis in tadpoles of eastern narrow mouth toads (Gastrophryne carolinensis: microhylidae). Trans Ill Acad Sci 108:29–34

    Google Scholar 

  • Kamei RG, San Mauro D, Gower DJ, Van Bocxlaer I, Sherratt E, Thomas A, Babu S, Bossuyt F, Wilkinson M, Biju SD (2012) Discovery of a new family of amphibians from Northeast India with ancient links to Africa. Proc R Soc B 279:2396–2401

    PubMed  PubMed Central  Google Scholar 

  • Kleinteich T (2010) Ontogenetic differences in the feeding biomechanics of oviparous and viviparous caecilians (Lissamphibia: gymnophiona). Zool 113:283–294

    Google Scholar 

  • Kleinteich T, Gorb SN (2014) Tongue adhesion in the horned frog Ceratophrys sp. Sci Rep 4:5225. https://doi.org/10.1038/srep05225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kleinteich T, Gorb SN (2016) Frog tongue surface microstructures: functional and evolutionary patterns. Beilstein J Nanotechnol 7:893–903. https://doi.org/10.3762/bjnano.7.81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kleinteich T, Haas A (2007) Cranial musculature in the larva of the caecilian, ichthyophis kohtaoensis (Lissamphibia: gymnophiona). J Morphol 268:74–88

    PubMed  Google Scholar 

  • Kleinteich T, Haas A (2011) The hyal and ventral branchial muscles in caecilian and salamander larvae: homologies and evolution. J Morphol 272:598–613

    PubMed  Google Scholar 

  • Kleinteich T, Haas A, Summers AP (2008a) Caecilian jaw-closing mechanics: integrating two muscle systems. J R Soc Interface 5:1491–1504

    PubMed  PubMed Central  Google Scholar 

  • Kleinteich T, Beckmann F, Herzen J, Summers AP, Haas A (2008b) Applying x-ray tomography in the field of vertebrate biology: form, function, and evolution of the skull of caecilians (Lissamphibia: gymnophiona). Proc of SPIE 7078. https://doi.org/10.1117/12.795063

  • Kleinteich T, Maddin HC, Herzen J, Beckmann F, Summers AP (2012) Is solid always best? Cranial performance in solid and fenestrated caecilian skulls. J Exp Biol 215:833–844

    PubMed  Google Scholar 

  • Kleinteich T, Herzen J, Beckmann F, Matsui M, Haas A (2014) Anatomy, function, and evolution of jaw and hyobranchial muscles in cryptobranchoid salamander larvae. J Morphol 275:230–246

    PubMed  Google Scholar 

  • Konietzko-Meier D, Gruntmejer K, Marcé-Nogué J, Bodzioch A, Fortuny J (2018) Merging cranial histology and 3D-computational biomechanics: a review of the feeding ecology of a Late Triassic temnospondyl amphibian. PeerJ 6:e4426. https://doi.org/10.7717/peerj.4426

    Article  PubMed  PubMed Central  Google Scholar 

  • Kucera F, Beisser CJ, Lemell P (2018) Size does matter—intraspecific variation of feeding mechanics in the crested newt Triturus dobrogicus (Kiritzescu, 1903). Acta Sci Nat 5:75–85

    Google Scholar 

  • Kupfer A, Nabhitabhata J, Himstedt W (2005) Fromwater into soil: trophic ecology of a caecilian amphibian (GenusIchthyophis). Acta Oecol 28:95–105

    Google Scholar 

  • Kupfer A, Müller H, Antoniazzi MM, Jared C, Greven H, Nussbaum RA, Wilkinson M (2006) Parental investment by skin feeding in a caecilian amphibian. Nat 440:926–929

    CAS  Google Scholar 

  • Larson PM, Reilly SM (2003) Functional morphology of feeding and gill irrigation in the anuran tadpole: electromyography and muscle function in larval Rana catesbeiana. J Morphol 255:202–214

    Google Scholar 

  • Lakrout H, Creton C, Sergot P (1999) Direct observation of cavitation and fibrillation in a probe tack experiment on model acrylic pressure-sensitive-adhesives. J Adhes 69:307–359

    CAS  Google Scholar 

  • Lappin KL, Monroy JA, Pilarski JQ, Zepnewski ED, Pierotti DJ, Nishikawa KC (2006) Storage and recovery of elastic potential energy powers ballistic prey capture in toads. J Exp Biol 209:2535–2553

    PubMed  Google Scholar 

  • Lappin KL, Wilcox SC, Moriarty DJ, Stoeppler SAR, Evans SE, Jones MEH (2017) Bite force in the horned frog (Ceratophrys cranwelli) with implications for extinct frogs. Sci Rep 7:11963

    PubMed  PubMed Central  Google Scholar 

  • Lombard RE, Wake DB (1976) Tongue evolution in the lungless salamanders, family plethodontidae. I. Introduction, theory and a general model of dynamics. J Morphol 148:265–286

    CAS  PubMed  Google Scholar 

  • Maddin HC (2011) Deciphering morphological variation in the braincase of caecilian amphibians (Gymnophiona). J Morphol 272:850–871

    PubMed  Google Scholar 

  • Maddin HC, Anderson JS (2012) Evolution of the amphibian ear with implications for lissamphibian phylogeny: insight gained from the caecilian inner ear. Fieldiana 5:59–76

    Google Scholar 

  • Maddin HC, Sherratt E (2014) Influence of fossoriality on inner ear morphology: insights from caecilian amphibians. J Anat 225:83–93

    PubMed  PubMed Central  Google Scholar 

  • Maddin HC, Russell AP, Anderson JS (2012a) Phylogenetic implications of the morphology of the braincase of caecilian amphibians (Gymnophiona). Zool J Linn Soc 166:160–201

    Google Scholar 

  • Maddin HC, Jenkins FAJr, Anderson JS (2012b) The braincase of Eocaecilia micropoda (Lissamphibia, Gymnophiona) and the origin of caecilians. Plos One 7:e50743

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mallett ES, Yamaguchi GT, Birch JM, Nishikawa KC (2001) Feeding motor patterns in anurans: insights from biomechanical modelling. Am Zool 41:1364–1374

    Google Scholar 

  • Marshall AF, Bardua C, Gower DJ, Wilkinson M, Sherratt E, Goswami A (2019) High-density three-dimensional morphometric analyses support conserved static (intraspecific) modularity in caecilian (Amphibia: Gymnophiona) crania. Biol J Linn Soc 1–22

    Google Scholar 

  • Measey GJ, Herrel A (2006) Rotational feeding in caecilians: putting a spin on the evolution of cranial design. Biol Lett 2:485–487

    PubMed  PubMed Central  Google Scholar 

  • Measey GJ, Gower DJ, Oommen OM, Wilkinson M (2004) A subterranean generalist predator: diet of the soil-dwelling caecilian Gegeneophis ramaswamii (Amphibia; Gymnophiona; Caeciliidae) in Southern India. CR Biol 327:65–76

    Google Scholar 

  • Meyers JJ, O’Reilly JC, Monroy JA, Nishikawa KC (2004) Mechanism of tongue protraction in microhylid frogs. J Exp Biol 207:21–31

    PubMed  Google Scholar 

  • Moll EO, Smith HM (1967) Lizards in the diet of an American caecilian. Nat Hist Misc Chic Acad Sci 187:1–2

    Google Scholar 

  • Monroy JA, Nishikawa KC (2009) Prey location, biomechanical constraints and motor program choice during prey capture in the Tomato Frog, Dyscophus guineti. J Comp Physiol A 195:843–852

    Google Scholar 

  • Monroy JA, Nishikawa KC (2011) Prey capture in frogs: alternative strategies, biomechanical trade-offs, and hierarchical decision making. J Exp Zool A 315:61–71

    Google Scholar 

  • Müller H, Oomen OV, Bartsch P (2005) Skeletal development of the direct-developing caecilian Gegeneophis ramaswamii (Amphibia: gymnophiona: caeciliidae). Zoomorphology 124:171–188

    Google Scholar 

  • Nishikawa KC (2000) Feeding in frogs. In: Schwenk K (ed) Feeding: form, function and evolution in tetrapod vertebrates. Academic Press, San Diego, pp 117–148

    Google Scholar 

  • Nishikawa KC, Gans C (1996) Mechanisms of tongue protraction and narial closure in the marine toad Bufo marinus. J Exp Biol 199:2511–2529

    CAS  PubMed  Google Scholar 

  • Nishikawa KC, Roth G (1991) The mechanism of tongue protraction during prey capture in the frog Discoglossus pictus. J Exp Biol 159:217–234

    Google Scholar 

  • Nishikawa KC, Deban SM, Anderson CW, O’Reilly JC (1992) The evolution of neural circuits controlling feeding behavior in frogs. Brain Behav Evol 40:125–140

    CAS  PubMed  Google Scholar 

  • Nishimura K (2018) An interaction-driven cannibalistic reaction norm. Ecol Evol 8:2305–2319

    PubMed  PubMed Central  Google Scholar 

  • Noel AC, Guo H-Y, Mandica M, Hu DL (2017) Frogs use a viscoelastic tongue and non-Newtonian saliva to catch prey. J R Soc Interface 14:20160764. https://doi.org/10.1098/rsif.2016.0764

    Article  PubMed  PubMed Central  Google Scholar 

  • Nussbaum RA (1983) The evolution of a unique dual jaw closing mechanism in caecilians (Amphibia: gymnophiona) and its bearing on caecilian ancestry. J Zool 199:545–554

    Google Scholar 

  • O’Reilly JC (2000) Feeding in caecilians. In: Schwenk K (ed) Feeding: form, function and evolution in tetrapod vertebrates. Academic Press, San Diego, pp 95–116

    Google Scholar 

  • O’Reilly JC, Deban SM, Nishikawa KC (2002) Derived life history characteristics constrain the evolution of aquatic feeding behavior in adult amphibians. In: Aerts P, D’Août K, Herrel A, van Damme R (eds) Topics in functional and ecological vertebrate morphology: a tribute to frits de Vree. Shaker Publishing, Maastricht, the Netherlands, pp 153–190

    Google Scholar 

  • Park S-R, Jeong J-Y, Park D (2005) Cannibalism in the Korean salamander (Hynobius leechi: hynobiidae, caudata, amphibia) larvae. Integr Biosci 9:13–18

    Google Scholar 

  • Perez-Vilar J, Hill RL (1999) The structure and assembly of secreted mucins. J Biol Chem 274:31751–31754

    CAS  PubMed  Google Scholar 

  • Pethiyagoda R, Manamendra-Arachchi K, Sudasinghe H (2014) Underwater and terrestrial feeding in the Sri Lankan wart frog, Lanakanectes corrugatus. Ceylon J Sci (Biol. Sci.) 43:79–82

    Google Scholar 

  • Ponssa ML, Vera Candioti MF (2012) Patterns of skull development in anurans: size and shape relationship during post metamorphic cranial ontogeny in five species of the Leptodactylus fuscus Group (Anura: leptodactylidae). Zoomorphology 131:349–362

    Google Scholar 

  • Presswell B, Gower DJ, Oomen OV, Measey GJ, Wilkinson M (2002) Scolecophidian snakes in the diets of South Asian caecilian amphibians. Herpetol Jnl 12:123–126

    Google Scholar 

  • Pyron RA, Wiens JJ (2011) A large-scale phylogeny of amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol Phyl Evol 61:543–583

    Google Scholar 

  • Regal PG, Gans C (1976) Functional aspects of the evolution of frog tongues. Evol 30:718–734

    Google Scholar 

  • Roček Z, Baleeva N, Vazeille A, Bravin A, van Dijk E, Nemoz C, Prikryl T, Smirina EM, Boistel R, Claesssens L (2016) Contributions to the head anatomy of the basal frog, Barbourula busuangensis and the evolution of the Anura. Russ J Herpetol 23:163–194

    Google Scholar 

  • Roelants K, Bossuyt F (2005) Archaeobatrachian paraphyly and Pangean diversification of crown-group frogs. Syst Biol 54:111–126

    PubMed  Google Scholar 

  • Roelants K, Gower DJ, Wilkinson M, Loader SP, Biju SD, Guillaume K, Moriau L, Bossuyt F (2007) Global patterns of diversification in the history of modern amphibians. Proc Natl Acad Sci USA 104:887–892

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roelants K, Haas A, Bossuyt F (2011) Anuran radiations and the evolution of tadpole morphospace. Proc Natl Acad Sci 108:8731–8736

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ryerson WG, Deban SM (2010) Buccal pumping mechanics of Xenopus laevis tadpoles: effects of biotic and abiotic factors. J Exp Biol 213:2444–2452

    PubMed  Google Scholar 

  • San Mauro D, Vences M, Alcobendas M, Zardoya R, Meyer A (2005) Initial diversification of living amphibians predated the breakup of Pangea. Am Nat 165:590–599

    PubMed  Google Scholar 

  • San Mauro D, Gower DJ, Müller H, Loader SP, Zardoya R, Nussbaum RA, Wilkinson M (2014) Life-history evolution and mitogenomic phylogeny of caecilian amphibians. Mol Phyl Evol 73:177–189

    Google Scholar 

  • Sandusky PE, Deban SM (2012) Temperature effects on the biomechanics of prey capture in the frog Rana pipiens. J Exp Zool 317A:595–607

    Google Scholar 

  • Scales JA, Stinson CM, Deban SM (2016) Extreme performance and functional robustness of movement are linked to muscle architecture: comparing elastic and nonelastic feeding movements in salamanders. J Exp Zool A 325:360–376

    CAS  Google Scholar 

  • Schoch RR (2014) Amphibian skull evolution: the developmental and functional context of simplification, bone loss and heterotopy. J Exp Zool 322B:619–630

    Google Scholar 

  • Schwenk K (2000) Feeding: form, function, and evolution in tetrapod vertebrates. Academic Press, San Diego

    Google Scholar 

  • Schwenk K, Rubega MA (2005) Diversity of vertebrate feeding systems. In: Starck MJ, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, p 1–41

    Google Scholar 

  • Sherratt E, Gower DJ, Klingenberg CP, Wilkinson M (2014) Evolution of cranial shape in caecilians (Amphibia: gymnophiona). Evol Biol 41:528–545

    Google Scholar 

  • Stinson CM, Deban SM (2017a) Functional trade-offs in the aquatic feeding performance of salamanders. Zool 125:69–78

    Google Scholar 

  • Stinson CM, Deban SM (2017b) Functional morphology of terrestrial prey capture in salamandrid salamanders. J Exp Biol 220:3896–3907

    PubMed  Google Scholar 

  • Summers AP, Wake MH (2005) The retroarticular process, streptostyly and the caecilian jaw closing system. Zool Anal Complex Syst 108:307–315

    Google Scholar 

  • Thexton AJ, Wake DB, Wake MH (1977) Tongue function in the salamander Bolitoglossa occidentalis. Arch Oral Biol 22:361–366

    CAS  PubMed  Google Scholar 

  • Van Bocxlaer I, Roelants K, Biju SD, Nagaraju J, Bossuyt F (2006) Late Cretaceous vicariance in Gondwanan amphibians. Plos One 1:e74

    PubMed  PubMed Central  Google Scholar 

  • Van Wassenberg S, Heiss E (2016) Phenotypic flexibility of gape anatomy fine-tunes the aquatic prey-capture system of newts. Sci Rep 6:29277

    Google Scholar 

  • Vera Candioti F (2005) Morphology and feeding in tadpoles of Ceratophrys cranwelli (Anura: leptodactylidae). Acta Zool 86:1–11

    Google Scholar 

  • Vera Candioti F (2006) Ecomorphological guilds in anuran larvae: an application of geometric morphometric methods. Herpetol Jnl 16:149–162

    Google Scholar 

  • Vera Candioti F, Lavilla EO, Echeverria DD (2004) Feeding mechanisms in two tree frogs, Hyla nana and Scinax nasicus (Anura: hylidae). J Morphol 261:206–224

    CAS  PubMed  Google Scholar 

  • Vidal-Garcia M, Keogh SJ (2017) Phylogenetic conservatism in skulls and evolutionary lability in limbs—morphological evolution across an ancient frog radiation is shaped by diet, locomotion and burrowing. BMC Evol Biol 17:165

    PubMed  PubMed Central  Google Scholar 

  • Wainwright PC, Bennett AF (1992a) The mechanism of tongue projection in chameleons: II. Role of shape change in a muscular hydrostat. J Exp Biol 168:23–40

    Google Scholar 

  • Wainwright PC, Bennett AF (1992b) The mechanism of tongue projection in chameleons: I. Electromyographic tests of functional hypotheses. J Exp Biol 168:1–21

    Google Scholar 

  • Wainwright DK, Kleinteich T, Kleinteich A, Gorb SN, Summers AP (2013) Stick tight: suction adhesion on irregular surfaces in the northern clingfish. Biol Lett 9:20130234

    PubMed  PubMed Central  Google Scholar 

  • Wake MH (1993) The skull as locomotor organ. In: Hanken J, Hall BK (eds) The skull, functional and evolutionary mechanisms, vol 3. University of Chicago Press, Chicago, pp 197–240

    Google Scholar 

  • Wake DB (2013) The enigmatic history of the European, Asian and American plethodontid salamanders. Amphib Reptil 34:323–336

    Google Scholar 

  • Wake DB, Deban SM (2000) Terrestrial feeding in salamanders. In: Schwenk K (ed) Feeding: form, function and evolution in tetrapod vertebrates. Academic Press, San Diego, pp 95–116

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Wilkinson M, San Mauro D, Sherratt E, Gower DJ (2011) A nine-family classification of caecilians (Amphibia: gymnophiona). Zootaxa 2874:41–64

    Google Scholar 

  • Wilkinson M, Sherratt E, Starace F, Gower DJ (2013) A new species of skin-feeding caecilian and the first report of reproductive mode in Microcaecilia (Amphibia: gymnophiona: siphonopidae). PLoS One 8(3):e57756. https://doi.org/10.1371/journal.pone.0057756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Y, Wang Y, Hanken J (2012) Comparative osteology of the genus Pachytriton (Caudata: salamandridae) from Southeastern China. Asian Herpetol Res 3:83–102

    Google Scholar 

  • Zardoya R, Meyer A (2001) On the origin of and phylogenetic relationships among living amphibians. Proc Natl Acad Sci USA 98:7380–7383

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zosel A (1989) Adhesive failure and deformation behaviour of polymers. J Adhes 30:135–149

    CAS  Google Scholar 

  • Zylberberg L (1977) Histochemistry and ultrastructure of amphibian lingual glands and phylogenetic relations. Histochem J 9:505–520

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dr. Sam Van Wassenbergh for providing feedback on this chapter; Dr. Steve Deban for allowing us to use a video of a bufonid capturing prey using in Fig. 12.6. Jim O’Reilly specifically would like to acknowledge Robert Levine and Skip Bennett for allowing him to include data on the function of the interhyoideus posterior muscle in caecilians in this chapter. He also would like to thank Beth Brainerd, Nate Kley, George Drake, Steve Deban and Eric Silva for help during the acquisition of these data. RB would like to thank Christian Nemoz, Alberto Bravin, Paul Tafforeau, Elodie Boller and Gheylen Daghfous for help with imaging at the ESRF. Finally, we would like to thank Dr. D. Blackburn for providing us with the frog scans, most of which are available on Morphosource (https://www.morphosource.org/).

Author information

Authors and Affiliations

  1. Département Adaptations du Vivant, Muséum national d’Histoire naturelle, UMR 7179 C.N.R.S/M.N.H.N, 55 rue Buffon, 75005, Paris Cedex 05, France

    Anthony Herrel

  2. Department of Biomedical Sciences, Ohio University, Cleveland Campus, Cleveland, Ohio, 334C, USA

    James C. O’Reilly

  3. Life Sciences Department, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK

    Anne-Claire Fabre & Carla Bardua

  4. Department of Biology Evolutionary, Morphology of Vertebrates, Ghent University, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium

    Aurélien Lowie

  5. IPHEP, Université de Poitiers, UMR CNRS 7262, 6 rue Michel brunet, 86073, Poitiers, France

    Renaud Boistel

  6. Department of Functional Morphology and Biomechanics, Christian-Albrechts-Universität Kiel, Am Botanischen Garten 1-9, 24118, Kiel, Germany

    Stanislav N. Gorb

Authors
  1. Anthony Herrel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James C. O’Reilly
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anne-Claire Fabre
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carla Bardua
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aurélien Lowie
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Renaud Boistel
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Stanislav N. Gorb
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anthony Herrel .

Editor information

Editors and Affiliations

  1. Institut Systématique Evolution Biodiversité – UMR 7205 CNRS/MNHN/Sorbonne Université/EPHE/UA, Muséum national d’Histoire naturelle, Paris, France

    Vincent Bels

  2. Canadian Center for Behavioural Neuroscience, University of Lethbridge, Lethbridge, AB, Canada

    Ian Q. Whishaw

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Herrel, A. et al. (2019). Feeding in Amphibians: Evolutionary Transformations and Phenotypic Diversity as Drivers of Feeding System Diversity. In: Bels, V., Whishaw, I. (eds) Feeding in Vertebrates. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-030-13739-7_12

Download citation

Publish with us

Policies and ethics

Search

Navigation