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Research Article
Mechanism of tongue protraction in microhylid frogs
Jay J. Meyers, James C. O'Reilly, Jenna A. Monroy, Kiisa C. Nishikawa
Journal of Experimental Biology 2004 207: 21-31; doi: 10.1242/jeb.00715
Jay J. Meyers
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James C. O'Reilly
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Jenna A. Monroy
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Kiisa C. Nishikawa
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Figures

  • Fig. 1.
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    Fig. 1.

    Tongue aiming ability was quantified by having individuals of Phrynomantis bifasciatus aim into five quadrants: (A) left– 46° to –105°, (B) left –6° to –45°, (C) 0° to 5° to either side, (D) right 6° to 45°, (E) right 46° to 105°. The quadrant is essentially a bib, with the midline of the head designating 0°. As the head of the animal turns, the quadrant follows this movement so that a line drawn down the midline of the head would always be located at 0°.

  • Fig. 2.
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    Fig. 2.

    Ventral view of the buccal region of a cleared and stained specimen of Phrynomantis bifasciatus. Left and right sides are nearly identical. Major cranial nerves are labeled on the left side and rami of the nerves that innervate the tongue and hyobranchial musculature are labeled on the right side. Branches of the trigeminal nerve (V) innervate the m. submentalis (1) and the m. intermandibularis (2). Branches of the hypoglossal nerve (XII) innervate the m. genioglossus dorsoventralis, longitudinalis and transversalis (3) and the m. hyoglossus (4). The glossopharyngeal nerve (IX) is dorsal to the hypoglossal nerve and innervates other hyobranchial musculature and the tongue pad. Numbers 1 and 3 are located at the approximate sites of nerve transection for denervation of the m. intermandibularis and m. genioglossus lateralis and dorsoventralis, respectively.

  • Fig. 3.
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    Fig. 3.

    Ventral view of the superficial throat musculature in two anurans. (A) Undifferentiated m. intermandibularis posterior of a typical frog. (B) Differentiation of the m. intermandibularis posterior into two separate accessory slips in Phrynomantis bifasciatus. mm, mentomeckelian element; sm, m. submentalis; ip, m. intermandibularis posterior; m, mandible; ih, m. interhyoideus; ipa1, m. intermandibularis posterior accessory 1; ipa2, m. intermandibularis posterior accessory 2.

  • Fig. 4.
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    Fig. 4.

    Sagittal section of the tongue of Phrynomantis bifasciatus. (A) Note that the fibers of the m. genioglossus dorsoventralis are directed longitudinally and then dorso-ventrally. (B) Magnified view of the m. genioglossus dorsoventralis. Single fibers run in both the longitudinal and vertical planes. d, dentary; gh, m. geniohyoideus; ggdv, m. genioglossus dorsoventralis; ggl, genioglossus longitudinalis; h, hyobranchium; hg, m. hyoglossus; im, m. intermandibularis; ggt, m. genioglossus transversalis; m, mucosal layer. Scale bar, 1 mm.

  • Table 1.

    Mean ± s.d. of tongue angles in each quadrant for six individuals of Phrynomerus bifasciatus, together with the results of a t-test examining the effect on aiming after right unilateral M. genioglossus denervation on one individual

    IndividualQuadrant A (—105° to —46°)Quadrant B (—45° to —6°)Quadrant C (—5° to +5°)Quadrant D (+6° to +45°)Quadrant E (+46° to +105°)
    Normal
    1—57.0±10.9—33.8±8.50.4±0.5+32.2±8.4+62.0±14.8
    2—51.2±3.0—32.8±8.90.8±0.8+32.4±6.1+57.8±4.3
    3—60.0±1.4—33.0±3.42.0±2.1+37.3±4.6+67.5±20.0
    4—60.2±18.2—36.4±6.90.2±0.4+32.6±3.5+84.2±21.3
    5—52.2±5.6—30.4±8.21.0±1.4+35.4±8.1+51.0±5.5
    6—55.3±11.4—30.5±9.50.8±1.3+36.8±5.1+62.3±6.3
    After right unilateral M. genioglossus denervation
    3+30.0±16.5*+38.0±9.4*+34.6±4.0*+38.6±5.9+64.3±19.0
    • ↵* Aiming was significantly (P<0.05) affected in quadrants A, B and C, in which the tongue consistently deviated towards the intact side (animal's right side)

  • Table 2.

    Species in which tongue aiming ability was examined, including the number of animals observed, presence or absence of aiming, maximum tongue angle when aiming, mean angle of tongue deviation after unilateral m. genioglossus denervation (when prey is presented directly in front of the frog) and direction of deviation after unilateral denervation

    SpeciesNAimingMaximum tongue angleUnilateral m. genioglossusSide of deviation
    Bufonidae
          Bufo woodhousii3No00No deviation
    Ranidae
          Rana pipiens3Little520Active side
    Microhylidae
       Brevicipitinae
          Breviceps mossambicus7Yes83——
          Callulina kreffti4Yes52——
          Probreviceps sp.1Yes44——
       Cophylinae
          Platypelis tuberifera1Yes29——
       Dyscophinae
          Dyscophus guineti5Yes536Inactive side
       Microhylinae
          Dermatonotus muelleri5Yes10947Inactive side
          Gastrophryne olivacea5Yes777Inactive side
          Gastrophryne carolinensis2Yes48——
          Hypopachus variolosus1Yes42——
          Kaloula pulchra5Yes329Inactive side
          Microhyla achatina3Yes53——
          Microhyla pulchra9Yes———
       Phrynomerinae
          Phrynomantis bifasciatus20Yes10344Inactive side
          Phrynomantis microps3Yes———
       Scaphiophryninae
          Scaphiophryne calcarata1Yes23——
          Scaphiophryne gottlebei3Yes———
          Scaphiophryne marmorata2Yes62—Inactive side
          Scaphiophryne pustulosa7Yes3322Inactive side
  • Fig. 5.
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    Fig. 5.

    Examples of tongue aiming in microhylid frogs: (A) Phrynomantis bifasciatus; (B) Dyscophus insularis; (C) Scaphiophryne marmorata; (D) Dermatonotus muelleri; (E) Kaloula pulchra; (F) Callulina sp.; (G) Gastrophryne olivacea; (H) Breviceps adspersus; (I) Microhyla sp.; (J) Probreviceps sp. Note the angle of the tongue in relation to the midline of the head. All pictures were taken with the camera positioned at 45°, except H and J, which were head-on profiles.

  • Fig. 6.
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    Fig. 6.

    Tongue protraction in Phrynomantis bifasciatus when prey is placed directly in front of the animal. (A) Normal feeding. There is no deviation of the tongue when attempting to capture prey. (B) After right unilateral m. submentalis and m. intermandibularis denervation, the tongue is protracted normally. (C) After right unilateral m. genioglossus (both longitudinalis and dorsoventralis) denervation, the tongue deviates towards the right (inactive) side. Animals are no longer able to capture prey placed directly in front of the head or towards the active side.

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Research Article
Mechanism of tongue protraction in microhylid frogs
Jay J. Meyers, James C. O'Reilly, Jenna A. Monroy, Kiisa C. Nishikawa
Journal of Experimental Biology 2004 207: 21-31; doi: 10.1242/jeb.00715
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Research Article
Mechanism of tongue protraction in microhylid frogs
Jay J. Meyers, James C. O'Reilly, Jenna A. Monroy, Kiisa C. Nishikawa
Journal of Experimental Biology 2004 207: 21-31; doi: 10.1242/jeb.00715

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