The goal of this study was to investigate morphological adaptations associated with hydrostatic elongation of the tongue during feeding in the African pig-nosed frog Hemisus marmoratum. Whereas previous studies had suggested that the tongue of H. marmoratum elongates hydraulically, the anatomical observations reported here favour a muscular hydrostatic mechanism of tongue elongation. H. marmoratum possesses a previously undescribed compartment of the m. genioglossus (m. genioglossus dorsoventralis), which is intrinsic to the tongue and whose muscle fibres are oriented perpendicular to the long axis of the tongue. On the basis of the arrangement and orientation of muscle fibres in the m. genioglossus and m. hyoglossus, we propose a muscular hydrostatic model of tongue movement in which contraction of the m. genioglossus dorsoventralis, together with unfolding of the intrinsic musculature of the tongue, results in a doubling in tongue length. Electron micrographs of sarcomeres from resting and elongated tongues show that no special adaptations of the sarcomeres are necessary to accommodate the observed doubling in tongue length during feeding. Rather, the sarcomeres of the m. genioglossus longitudinalis are strikingly similar to those of anuran limb muscles. The ability to elongate the tongue hydrostatically, conferred by the presence of the m. genioglossus dorsoventralis, is associated with the appearance of several novel aspects of feeding behaviour in H. marmoratum. These include the ability to protract the tongue slowly, thereby increasing capture success, and the ability to aim the tongue in azimuth and elevation relative to the head. Compared with other frogs, the muscular hydrostatic system of H. marmoratum allows more precise, localized and diverse tongue movements. This may explain why the m. genioglossus of H. marmoratum is composed of a larger number of motor units than that of other frogs.

REFERENCES

Deban
S. M.
,
Nishikawa
K. C.
(
1992
).
The kinematics of prey capture and the mechanism of tongue protraction in the green tree frog, Hylacinerea
.
J. Exp. Biol
170
,
235
–.
Gray
L. A.
,
Nishikawa
K. C.
(
1995
).
Feeding kinematics of phyllomedusine tree frogs
.
J. Exp. Biol
198
,
457
–.
Horton
P.
(
1982
).
Diversity and systematic significance of anuran tongue musculature
.
Copeia
1982
,
595
–.
Meyers
J. J.
,
Nishikawa
K. C.
,
O'Reilly
J. C.
(
1996
).
Tongueaiming in the microhylid frog Phrynomerusbifasciatus
.
Am. Zool
36
,
81
–.
Nishikawa
K. C.
(
1997
).
Emergence of novel functions during brain evolution
.
Bioscience
47
,
341
–.
Nishikawa
K. C.
,
Gans
C.
(
1992
).
The role of hypoglossal sensory feedback during feeding in the marine toad, Bufomarinus
.
J. Exp. Zool
264
,
245
–.
Nishikawa
K. C.
,
Gans
C.
(
1996
).
Mechanisms of prey capture and narial closure in the marine toad Bufomarinus
.
J. Exp. Biol
199
,
2511
–.
O'Reilly
S. R.
,
Nishikawa
K. C.
(
1995
).
Mechanism of tongue protraction during prey capture in the spadefoot toad Spea multiplicata (Anura: Pelobatidae)
.
J.Exp.Zool
273
,
282
–.
Regal
P. J.
,
Gans
C.
(
1976
).
Functional aspects of the evolution of frog tongues
.
Evolution
30
,
718
–.
Reynolds
E. S.
(
1963
).
The use of lead citrate at high pH as an electron-opaque stain in electron microscopy
.
J. Cell Biol
17
,
208
–.
Rice
M. J.
(
1973
).
Supercontracting striated muscle in a vertebrate
.
Nature
243
,
238
–.
Ritter
D. A.
,
Nishikawa
K. C.
(
1995
).
The kinematics and mechanism of prey capture in the African pig-nosed frog (Hemisus marmoratum): description of a radically divergent anuran tongue
.
J. Exp. Biol
198
,
2025
–.
Tso
T. A.
,
O'Reilly
J. C.
,
Nishikawa
K. C.
(
1995
).
Conservation of function of the m. hyoglossus during feeding in frogs
.
Am. Zool
35
,
123
–.
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