zoological Journal ofthe I.iunpau Soczrp (1983;, 77: 75-96. 'Il.'ith 9 figures
Morphology and function of the feeding
apparatus in Dermophis mexicanus
(Amphibia: Gymnophiona)
W. E. BEMIS, K. SCHWENK
AND
M. H. WAKE*
Department of zoology and Museum of
Berkeley, California 94720, U.S.A.
Vertebi-ate ~ o o l o c g y ,University of California,
Accepted f o r publication June 1982
The morphology and mechanics of feeding in Demophzs mexicanus were studied using descriptive
anatomical, cinematographic and electromyographic approaches. The lower jaw has a retroarticular
process extending one-third of the total jaw length, and an articulation that restricts anteroposterior
movements. Muscles from three anatomically distinct sites, the temporal fossa, the lateral surface of the
neck, and the subvertebral region, act to execute the bite during feeding on earthworms. Muscles in the
first of these sites are comparable to the jaw adductors of other vertebrates, while those in the second
two represent morphological and functional departures. l'he large interhyoideus muscle and the
elongate retroarticular process are modified to function in jaw closing. The longus capitis muscles
appear to act to depress the cranium at the cranio-vertebral joint, a motion that occurs simultaneously
with maximum jaw closing. The latter two muscles appear to have greater importance for feeding in
Demophis than do the temporal adductors, and the evolution of this specialized arrangement may be
related to the demands for a reduced cross-sectional area of the head in these burrowing vertebrates.
KEY WORDS :-Gymnophiona
-
Demophis
-
feeding
-
electromyography
- jaw
adduction
C0NTEN TS
Introduction . . . . . . . . . . .
. . . . . . . .
Materials and methods,
Osteology.
. . . . . . . . . . .
The skull . . . . . . . . . . .
The lower jaw and articulation.
. . . . .
The teeth,
. . . . . . . . . .
The hyoid
. . . . . . . . . .
The cranio-vertebraljoint and anterior trunk vertebrae
The oral cavity and the tongue.
. . . . . .
Myology.
. . . . . . . . . . .
Functional morphology of feeding .
. . . . .
Diet and prey capture.
. . . . . . .
Motion analysis of prey handling .
. . . .
Electromyography.
. . . . . . . .
Discussion . . . . . . . . . . . . .
Summary of feeding in Demophis . . . . .
Static pressure system of caecilians and its evolution
Acknowledgements. .
. . . . . . . .
References.
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*Please address reprint requests to M. H. Wake.
+
00244082/83/010075 22$03.00/0
75
0 1983 The Linnean Society of London
76
W E HEMIS E l r l l ,
INTRODUC'I ION
Caecilians (Amphibia : Gymnophiona) are limbless, terrestrial or aquatic
carnivores. They consume invertebrate prey primarily, especially earthworms,
termites, etc. (Taylor, 1968; Wake, 1980b), but little attention has been paid to the
mechanics of feeding. The dentition of caecilians is pedicellate, bicuspid or
monocuspid, and may be specialized for prey capture (Oltmann, 1952; Wake,
1978; Wake & Wurst, 1979). The jaw and its musculature are complex (Luther,
1914; Eifertinger, 1933; Edgeworth, 1935; De Villiers, 1936, 1938; De Jager,
1938, 1939a, b, c). We have examined feeding in Demophis mexicanus and present
data based on dissection, osteological examination, analysis of sectioned heads,
filmed activity and electromyography. We present an analysis of biting and
chewing, and a model for feeding kinematics in terrestrial caecilians.
Our work is designed to provide the groundwork for analysis of the evolution of
caecilian feeding systems. Because caecilians show a highly modified system of jaw
adduction relative to both fossil and extant amphibians, the nature of this system
and its functional significance may indicate the appearance of a key morphological
inno\ration in the evolutionary history of the group. Secondly, it will be possible to
compare the diversification of feeding mechanisms in all three of the orders of
amphibians. Caecilians are >aw feeders', while salamanders and frogs have a
variety of feeding systems ranging from aquatic gape-and-suck to elaborate tongue
projection mechanisms. Finally, evolutionary convergence in feeding mechanisms
shown by terrestrial and aquatic forms that have secondarily lost their limbs can be
evaluated. Caecilians can now be compared with amphisbaeneans (Gans, 1960,
1968, 1974, 1975) and with the extensive work on prey capture in snakes.
MATERIALS AND ME'IHODS
Animals were collected at two sites in Guatemala and southern Mexico. The
majority of specimens were fixed in 1004 neutral buffered formalin, although
approximately 75 juvenile- to adult-sized animals have been maintained in
captivity in the laboratory. A complete ontogenetic series has been available for
studies of skull development and morphometrics (Wake & Hanken, 1982; Wake,
in prep.). Specimens of adult size (250+ mm) were used for the majority of the
anatomical and experimental work reported here, though considerations of
ontogeny hare not been neglected.
A variety of anatomical preparations were utilized. Cleaned, intact skeletal
material was available for 1 1 individuals, and two completely macerated skulls
were used for studies of the individual bony elements. The relationships between
cartilaginous and bony elements of the head region were studied in a series of
cleared and double stained specimens from embryos to 310 mm adults. Dissections
of the head region of several individuals allowed identification of muscles and the
relationships among major soft tissue elements, features which were subsequently
confirmed by examination of serial frontal and sagittal celloidin sections of 267 and
380 mm specimens. Finally, the normal relationships of skeletal elements were
studied in radiographs of anaesthetized and freshly dead individuals. These
specimens were manipulated to conform to patterns of movement identified during
normal feeding secluences.
Laboratory maintained specimens were housed in plastic boxes in a mixture of
moistened vermiculite, potting soil and sand. Animals were fed weekly on
FUNCTIONAL MORPHOLOGY O F CAECILIAN FEEDING
77
earthworms (Lumbricus sp.). Temperature and photoperiod were room ambient.
Animals were observed during regular weekly feedings, and were photographed
following normal prey capture. Photographs taken with a motor-driven 35 mm
Nikon at a rate of three s-’ were particularly useful for studies of the feeding cycle.
These photographs were compared with tracings from 16 mm movies taken with a
Redlake LOCAM at 30 and 100 frames s-’. Either tungsten photofloods or high
repetition rate electronic flash units provided illumination; no difference in
behaviour was detected. Once prey had been taken into the mouth, an individual
would usually continue feeding, and such an animal could be picked up, moved
into a feeding arena or even washed off without deterring completion of feeding.
Photography of feeding sequences was therefore relatively straightforward.
Three individuals were used for electromyographic (emg) studies ofjaw muscles.
Four channels of electromyograms were recorded simultaneously on magnetic tape
along with a synchronization signal from the camera. Bipolar electrodes were
either 0.1 mm teflon-coated stainless steel or enamel-coated gauge 40 copper
magnet wire. Tip sizes of between 1 and 2 mm were used. During typical emg
studies, animals were anaesthetized with MS222 and the electrodes were inserted
into as many as eight different muscles. While still anaesthetized, a worm would be
placed in the animal’s mouth. During recovery from anaesthesia, movements of the
jaw would increase, and the four most successful electrode placements could be
selected. With ultimate recovery, apparently normal biting sequences would
ensue. Comparison of movie tracings from normal and emg runs failed to reveal
any differences that might be attributable directly to anaesthesia. Following a
series of successful runs, electrode placement was checked by X-ray.
OSTEOLOCY
The skull
The skull in caecilians is the product of fusion of numerous elements (Marcus,
1922; Marcus, Winsauer & Heuber, 1933; Marcus, Stimmelmayr & Porsch, 1935;
Edgeworth, 1935; De Beer, 1937; Wake & Hanken, 1982). Important to
consideration of the feeding apparatus are the relationships of the basal bone, the
quadrate, the squamosal, the anterior part of the skull, and the lower jaw. The os
basale is the result of fusion of numerous occipital and parasphenoid elements, and
the otic capsules. The quadrate is adjacent to it, and articulates as well with the
stapes and the lower jaw. The quadrate is in fact a pterygoquadrate, the pterygoid
flange appearing late in development in D. mexicanus and fusing to the quadrate
(Wake & Hanken, 1982). The squamosal overlies much of the quadrate and in
adult D. mexicanuJ nearly completely roofs the temporal fossa. All of the elements of
the anterior part of the skull constitute a single functional unit in terms of some
aspects of feeding mechanics (Marcus et al., 1935).
A major consideration in analysis of caecilian skull morphology has involved
questions of degree and origin of stegokrotaphy and of skull kinesis. Wake &
Hanken (1982) have concluded that stegokrotaphy (complete roofing of the
temporal fossa) in Dermophis is an ontogenetically progressive feature, and suggest
that stegokrotaphy in caecilians is a derived, not ancestral, condition, correlated
with the burrowing habitus. Kinesis, or movement of the anterior and lateral
78
W. E. BEMIS E 7 AL
elements of the skull relative to the basal bone, was considered by Marcus et al.
(1935) to be a property of the skull associated with stegokrotaphy, and they
concluded that the caecilian skull is streptostylic, with movement of the quadrate
on the 0s basale.Wake & Hanken (1982) have reviewed the debate about caecilian
skull kinesis, and present evidence that kinesis is a major functional feature of the
foetal skull, and that kinesis is evident, though much more limited than in foetuses,
in the adult skull. They suggest that such movement of the quadrate and therefore
the lower jaw is important in the intra-oviducal feeding of foetuses, and may occur
in prey capture in adults.
T h e lower j a w and articulation
In adult Dermophis, the lower jaw is composed of two large, composite, dermal
bones, an anterior pseudodentary and posterior pseudoangular. A description of
the formation of these elements from several separate centres of ossification along
with a discussion of the homologies of the separate units is provided by Wake &
Hanken (1982).The pseudodentary and pseudoangular are firmly attached to one
another by fibrous connective tissue and a small remnant of Meckel’s cartilage,
though they can be separated by maceration. The contact between these two
elements is very broad, and is similar to the spline joint used in woodworking. The
percentage of overlap between the two elements relative to the total lower jaw
length in a 369 mm adult was 57Y0. Because of this long and broad overlap, it is
probable that the lower jaw functions as a single, stiff mechanical unit. Other
features which suggest that these elements function together as a solid beam are the
heavy flange on the lingual side of the pseudodentary, which is continuous with the
anterior portion of the pseudoangular, and the generally robust construction of
the entire lower jaw. The flange on the lingual side of the pseudodentary gives the
anterior portion of the jaw an L-beam cross-section, perhaps offering greater
strength at a location which probably receives the greatest resistance forces from
prey during powerful jaw adduction.
The mandibular symphysis is a simple butt-joint between the two halves of the
jaw. The area of contact is larger than the cross-section of the pseudodentary. The
fibrous connective tissue of the joint does not appear to be particularly strong, and
would probably allow some independent movement of the two sides of the jaw in
life if the jaw articulation allowed.
The articulation of the lower jaw is complex. The entire suspension system of the
adult consists of the quadrate, which is tightly bound to the squamosal, and
connected by a synovial joint to the stapes. The degree to which movement of the
quadrate/squamosal unit may influence feeding can only be surmised, for no direct
evidence for streptostyly is apparent fiom our studies of filmed sequences.
However, some degree of quadrate/squamosal movement relative to the rest of the
skull is apparent in dissected specimens (see Wake & Hanken, 1982).
The articulation consists of the blade-like articular process of the quadrate
which fits into a deep, U-shaped groove on the pseudoangular. The groove is
located approximately two-thirds of the way along the lower jaw, and is bounded
anteriorly and posteriorly by short flanges. The combination of the groove and
flanges composes the complete articular facet. The entire inner surface of the
groove is lined by cartilage, as is the articular process of the quadrate, and the joint
is enclosed in a stout connective tissue capsule. The articular facet is not
80
W. E. BEMIS E’T AL.
The teeth
The teeth of adult D. mexicanus are pedicellate, monocuspid, and roughly
arrowhead-shaped, with lateral flanges that taper to an apical point (Wake &
Wurst, 1979). They are slightly recurved, and arrayed in two rows on the upper
jaw (27--33,X = 29.6 teeth in the premaxillary-maxillary row, and 27-29,? = 28.4
in the inner vomeropalatine row of adults of the size we used for this study) and a
single row on the margin of the pseudodentary of the lower jaw (23-27, X =24.2
teeth in adults; n = 5 ; specimens 375 mm total length (T.L.) + 5 mm). The number
of teeth increases slightly with age; replacement has been analysed by Wake
(1980a). The tooth crown is held to the pedicel in close approximation by
ligaments (Wake, 1976, 1980a; Greven & Clemen, 1980, for Siphonops annulatus;
Casey & Lawson, 1981, for Hypogeophis rostratus) . It has been suggested that there is
some flexibility between crown and pedicel (Casey & Lawson, 1981), and in
manipulating the teeth of freshly dead or anaesthetized Demzophis, the teeth are
demonstrably hinged so that they may fold inward slightly but do not fold out.
This in effect allows the teeth to act as a ratchet on prey items, so that struggling
prey find movement into the mouth easier than movement out.
‘I’he lower jaw is underslung relative to the upper in many caecilians, as it is in
D. mpxicanus. Therefore the tooth row of the lower jaw does not occlude directly
with either tooth row of the upper jaw, but fits between the two. This therefore
provides an interlocking system of three rows of recurved teeth when the jaw is
closed, which we consider a major feature of the modified static pressure feeding
system of caecilians (see below).
The hyoid
‘I’he hyobranchial elements of D . mexicanus are cartilaginous throughout life, as
in most caecilian species. The skeleton includes paired cerathyals fused to
basibranchial I , which is in turn fused to paired ceratobranchials.
Ceratobranchials I1 are fused at the midline with a small median anterior
extension indicating a basibranchialI1. Ceratobranchial (CB) pairs 111, IV and V
are fused together. Ceratobranchial I11 is a rod of nearly uniform thickness during
early development, as are I and 11. Ceratobranchial IV is shorter and thicker
proportionally, and it fuses medially to CB 111. Ceratobranchial V is a small,
medial component fused to CB IV. The cartilage spreads, filling in the spaces
between CB 111, I V and V and resulting in CB 111-IV-V having a broadly
dilated shape (Wake & Schwenk, in prep.). ‘I’he larynx lies in the CB 111-IV-V
arc. Development in Demzophis is similar to that in Hypogeophis (Gehwolf, 1923).
The craniouertebraljoint and anterior tiunk vertebrae
l’he craniovertebral joint of caecilians is unusual in that it has large, medially
located atlantal cotyles. The joint has been considered by Wake (1970) and
Lawson (1966) and is thought to be distinctly different from that of other
amphibians. Caecilians lack a tuberculum interglenoideum as noted by Peter
(1894), though Gadow (1933) called the cartilaginous notochordal component an
“odon toid”.
l’he skull is tightly bound to the atlas by ligaments in D. mexicanuJ (and other
FUNCTIONAL MORPHOLOGY OF CAECILIAN FEEDING
81
caecilians). The head movement that we have observed in feeding, as well as in
burrowing and in locomotion is largely vertical. Lateral movement occurs during
feeding, but it involves an arc that includes the first six to 10 vertebrae, rather than
rotation specifically behind the atlas. The dorsal trunk musculature that effects
raising of the head, and some lateral motion, inserts on the nuchal keels of those
vertebrae (Wake, 1980c, and below).
Anterior trunk vertebrae of caecilians are more stoutly constructed than those of
the posterior trunk (Wake, 1980c) and the first 10-15 vertebrae may show slight
enlargement of the basapophyses for attachment of the m. longus capitis. This
enlargement may also facilitate the lateral movement in the ‘neck’ region noted by
Wake ( 1 9 8 0 ~ ) .
T H E ORAL CAVITY AND T H E TONGUE
The tongue, the buccal cavity and their glands, and the pharynx have been
described for Hypogeophis rostratus (tongue : Marcus, 1932 ; Tiepel, 1932 ; Lawson,
1965 (some); buccal cavity and oral glands: Mang, 1935; pharynx, especially
development of pharyngeal pouch derivatives : Marcus, 1908 ; pharynx and lung
development : Marcus, 1922) and for Ichthyophis glutinosus (oral glands and tongue :
Sarasin & Sarasin, 1887 1890; lingual glands: Zylberberg, 1972, 1977).
The tongue is a large muscular structure, non-protrusable, its margin only
slightly free of the lower jaw. Tiepel (1932) reported a single tongue muscle, the
genioglossus, originating on the inner margin of the lower jaw and inserting on the
fascia below the glandular field of the surface of the tongue, innervated by the
hypoglossal nerve. Sensory innervation is from the glossopharyngeal and
mandibulus internus (a union of facial and trigeminal fibres). A large venous
plexus lies in the centre of the tongue muscle mass. The geniohyoideus lies below
the tongue proper (Tiepel, 1932). Tiepel considered the tongue to be functional in
respiration, rather than glandular secretion in feeding, though Zylberberg (1977)
suggests that the secretions function in prey capture and feeding. Glands are
confined to the dorsal surface of the tongue (Marcus, 1932; Zylberberg, 1972,
1977) and produce mixed mucoid and proteinaceous secretion (Zylberberg, 1972,
1977). The buccal cavity is lined with a mucosal epithelium, and Mang (1935)
reported mucous glands located between the teeth, in the intermaxillary region,
and behind the choanae and tongue glands. He considered these to be modified
skin glands.
In D.mexicanus we find a similar condition. The muscle mass of the tongue is
large, but only slightly free at its margins. The glandular field is dorsal, and
distributed over the entire surface of the tongue, in contrast to the median
distribution reported by Marcus (1932) in Hypogeophis. The buccal and pharyngeal
mucosa is thin, and contains numerous mucous glands, diminishing in number
posteriorly in the pharynx. The pharyngeal mucosa is ciliated. T h e origin of the
glands is from the oral mucosa, but they are confined to the epithelium only at the
margins of the tongue. T h e glands are embedded deeply among muscle fibres and
near blood sinuses in the body of the tongue. The venous sinuses are extensive
and throughout the tongue muscle mass, rather than the paired lateral
components found in Hypogeophis (Marcus, 1932; Tiepel, 1932). The genioglossus
forms the body of the tongue. It originates on the inner margin of the lower jaw at
the mandibular symphysis and the connective tissue overlying the geniohyoideus
W. E. BEMIS E7- .4L.
82
muscle, and inserts on the epithelium of the tongue surface. The muscle fibres are
dispersed vertically among the blood sinuses and the bases of the lingual glands.
Contraction of these fibres would (1) depress the tongue pad, increase pressure in
the blood sinuses and perhaps partially evacuate them, (2) facilitate extrusion of
lingual gland secretion by compressing the bases of the glands, (3) aid in food
transport, and probably respiration (Wake & Schwenk, in prep.).
The tongue facilitates prey transport in conjunction with the intermandibular
and hypobranchial musculature. The mucous secretion lubricates the mouth and
pharynx for prey transport.
MYOLOGY
There is considerable literature on the cranial and anterior trunk muscles of
caecilians. Particularly important among these are papers by Wiedersheim ( 1879:
Caeciliu and others), Luther (1914: Siphonops), Norris & Hughes (1918: Demophis,
Oscaecilia, Caecilia, Geotypetes, Zchthyophis), De Jaeger ( 1939a : Dermophis), Nishi
(1938 : Zcht/yophis) and Lawson (1965 : Hypogeophis). Most of these works have
emphasized the recognition of muscle homologies, and no study has focused on the
interpretation of muscle function. Because of the number of studies, there are
several different sets of available terms for the muscles, some purely descriptive and
others reflecting a particular author’s views on the homologies of cranial muscles in
general. Edgeworth (1935) provides a good synonomy of names for cranial
muscles, and because the further analysis of caecilian muscle homologies lies
Table 1. A list and partial synonomy of major cranial and anterior trunk muscles of
Demophis
~~~
Muscle name
Functional group
-
_.
Group I :
Group 11:
Group 111 :
Lateral adductor
Dorsal depressor
Group I\’:
Buccal and hyoid
musculature
~ r ~ J l \‘:
l[l
Dorsal trunk
Group V I :
Ventral trunk
musculature*
I
-r
~
Synonyms
~~
M. pseudotemporaliss
M. levator mandibulae anterior7 M . adductor mandibulae externus5
M. levator mandibulae externust M . adductor mandibulae externus
minors
M. levator mandibulae posterior? M. pterygoideuss
M . levator quadratit
M. interhyoideust
M . CPVDs
M. depressor mandibulaet
M. intermandibularist
M. geniohyoideust
M. rectus cervicist
M. genioglossust
M. levator arcus branchialest
Anterior portion called m. rectus
M. dorsalis trunci:
capitis superior:
,kf. cutaneous dorsalis:
M . rectus lateralis7
M. longus capitis et colli:
M. flexor colli et capitis11
*Partial list-only components thz* attach to the cranium.
tEdgeworth, 1935.
:Nishi, 1938.
$f,u[lier, I9 14.
“Naylor & Nusshaum, 1980.
:lWiedersheim, 1879.
FUNCTIONAL MORPHOLOGY OF CAECILIAN FEEDING
83
outside the scope of this paper, we have chosen to use Edgeworth’s terminology
where possible. Because Edgeworth did not consider anterior trunk muscles in his
review, we have taken the names of those muscles from Nishi (1938). We do not use
the terminology of Lawson (1965) for the reasons mentioned by Naylor &
Nussbaum (1980) ; the latter work did not include anterior musculature. O f the
cranial muscles discussed by Edgeworth, we have considered neither those of the
laryngeal apparatus nor minor elements of the hyoid apparatus. While many of the
trunk muscles may play roles in feeding, either by providing movement during
prey capture or by acting in series with muscles that act directly on the cranium,
we name only the major elements of this group. T h e 14 muscles discussed are listed
along with a partial synonomy in Table 1. Because the primary emphasis of this
paper is the clarification of function, the muscles are broken down into six
functional groups, listed on the left in Table 1. Four of these groups include
muscles that attach directly to the mandible, while the last two groups contain
muscles passing from the trunk to the cranium. These groups are considered in
detail below.
Group I: Internal adductors
The internal adductor musculature is comparable to the major jaw adductors
of other tetrapods and includes mm. levator mandibulae (1.m.) anterior, 1.m.
externus, and 1.m. posterior. All of these muscles are of mandibular arch origin,
and all except the m. levator quadrati insert on the mandible. These four muscles
originate on the lateral wall of the braincase, the inner surface of the
dermatocranium (primarily the squamosal), and the pterygoid process of the
quadrate. Within the adductor cavity, the muscles are distinguished by their
relationship to nerve V. The levator mandibulate anterior muscle fills most of the
dorsal portion of the ca\zity and is much larger than the m. levator mandibulae
externus, though the latter is derived embryologically from the former
cd
I
di
lob
I
seo
ih
Figure 2. Dorsolateral view of cranial and anterior trunk musculature. Superficial trunk musculature
shown removed posteriorly. cd: M. cutaneous dorsalis; seo: superficial portion of the M. externus
ohliquus; lab: M. levator arcus branchiales; d m : M. depressor mandibulae; ih: M. interhyoideus; dt :
M. dorsalis trunci; p : parietal; f frontal; npm : nasopremaxilla; s: squamosal; m p : maxillopalatine;
pa: pseudoangular; pd: pseudodentary.
W. E. BEMIS E l AL.
84
rc
99
Figure 3 . Ventrolateral view of cranial, hyoid and anterior trunk musculature. Muscles and other
tissues have been removed on the animal's right side to reveal the basal bone of the skull, the insertion
of the M. longus capitis, and the origin and course of t h e Mm. levator rnandibulae externus and
anterior. Ic: hl. longiis capitis; I m p : 1LI Icvator posterior; Irne: M. levator mandibulae externus: h a .
M. levator mandibulae anterior; irn: M. intermandibularis; gh: M. geniuhyoideus; gg: M.
genioglossus; M. rectus cervicis; pa : pseudoangular; pd: pseudodentary.
(Edgeworth, 1935), and the two appear to f h c t i o n as a unit. These muscles have
fibres orientated in a fan shape dorsally, which pass out through a restricted
subtemporal fenestra to insert on the lower jaw just anterior to the jaw
articulation. The m. le\.ator quadrati is a straight, parallel fibred muscle
connecting the wall of the braincase to the pterygoid process of the quadrate. The
m. le\,ator posterior originates on the ventromedial surface of the quadrate, then
exits through the subtemporal fenestra, passes ventral to the internal process of
the mandible and inserts on the ventromedial surface of the retroarticular process
(Figs 2, 3 ) .
Functionally, the internal adductors fall into three categories. The anterior and
external levators act almost entirely in raising the lower jaw because of the position
of the subtemporal fenestra directly above the attachment site of the muscles. The
posterior levator imparts a jaw closing action as well as a slight anterior pull.
Anterior movement of the mandible is limited both by the structure of the jaw joint
and by the pulley-like action of the internal process, which tends to direct the line
ofaction ofthe muscle into a dorsoventral direction. The role ofthe levator quadrati
muscle is not clear by inspection; it may act to restrict the downward rotation of
the quadrate during contraction of the other two components of this groupparticularly the posterior levator. I t is also possible that this muscle functions in
dorsal rotation of the quadrate during feeding, as noted above.
Group 11: Lateral ailductor
The large lateral adductor, or m. interhyoideus, takes its origin on the fascia of
the ventral and lateral body wall and inserts by a stout tendon onto the ventral
surface of the retroarticular process (Figs 2, 3 ) . The bulk of this muscle lies within a
FUYCTION.4L MORPHOLOGY O F CABCILIAN FEEDING
85
concavity of the lateral body wall. Posteriorly, its fibres run longitudinally, while
those more anterior run transversely. I n some caecilians, notably ichthyophiids,
the posterior, longitudinal portion is a separate muscle, the interhyoideus posterior
(Edgeworth, 1935; Nussbaum, 1977). I n Dermophis, the transition between
longitudinal and transverse fibres is smooth and undemarcated, hence we treat it
as a single pinnate muscle. However, because of this pinnation and the muscle’s
broad insertion on the retroarticular process, the possibility of heterogeneity in
function cannot be eliminated. Anteriorly, transverse fibres of the interhyoideus
blend insensibly with those of the m. intermandibularis (see Group IV, below).
Due to its position directly behind the retroarticular process, the action of the
interhyoideus is to close the lower jaw, a s noted by Nussbaum (1977) and
confirmed by electromyography (below). This function of the interhyoideus in
caecilians is unique among tetrapods. It seems unlikely that this muscle plays an
important role in lateral movements of the head, as suggested by Lawson (1965),
due to the limited lateral movement allowed by the craniovertebral joint. The
interhyoideus muscle is considerably larger than the internal adductors (Group I)
and seems to be the major muscle of adduction. In fresh specimens, it is paler in
colour than the adjacent body wall musculature, suggesting that its fibres
may have less oxidative capability than other muscles of Dermophis.
Gtoup 111: Dorsal deflieuor
‘The large m. depressor mandibulae originates on the posterolateral surface of
the skull and passes to the dorsal surface of the retroarticular process as shown in
Fig. 3. As in other tetrapods that possess this muscle, i t is innervated by nerve
VII, and it functions during jaw opening.
Group IV: Buccal and hyoid musrulature
Our understanding of the fiinctions of this group of muscles is limited both by
their small size and complex arrangement. The muscles of this region function
during respiration and feeding. Gular pumping occurs more-or-less regularly
during normal resting of the animal. These muscles are deep red in colour,
suggesting an oxidative metabolism well suited for continuous activity. Omitting
the smaller muscles of the hyoid apparatus and the larynx, there are four major
muscles of this region. T h e most superficial of these is the m. intermandibularis,
which, a s in other amphibians, forms a thin sheet between the medial borders of
the jaw and functions in the ele\ration of the buccal floor during respiration and
feeding. ‘I’he rectus cervicis and geniohyoideus muscles are connected in series at
the hyoid apparatus, and function in jaw depression in many vertebrates.
However, our electromyographic records indicate firnction during respiration but
not during jaw depression. The genioglossus muscle makes up most of the body of
the tongue, and is described in that section. T h e complex m. levator arcus
branchiales has a fan shaped origin in the dorsal fhscia of the trunk, from which it
passes ventrally beneath the interhyoideus posterior to insert on the hyoid
apparatus. The predominant action of this muscle appears to be the elevation of
the hyoid region, and it probably plays a major role in respiration as well as
feeding.
86
W . E. BEMIS ET AL
Group V: Dorsal trunk musculature
The primary functions of the trunk musculature are in locomotion and
burrowing. However, trunk muscles attaching directly to the cranium also
function during feeding. The plane of intersection between the ribs and vertebrae
divides the trunk muscles into dorsal and ventral components. This division is not
absolute, in that some muscles cross the plane of the ribs, but it is adequate for
understanding the role of these muscles in feeding. Caecilian trunk muscles have
been figured and described by Nishi (1938), Lawson (1965) and Naylor &
Nussbaum (1980).
The two most prominent elements of the dorsal trunk musculature are the m.
cutaneous dorsalis and m. dorsalis trunci. Dorsolaterally, the sheath-like cutaneous
dorsalis muscle covers the deeper and more massive dorsalis trunci. Both muscles
are segmented, and continue anteriorly to insert on the posterodorsal region of the
cranium between the depressor mandibulae muscles. The dorsal trunk muscles
have several possible actions, including the elevation of the cranium at the
craniovertebral joint,
Group 171: Ventral trunk musculature
Moft of the ventral trunk musculature does not play a major role in feeding. The
thick bentral body wall of Dermophzs is composed of the usual tetrapod body wall
muscles (mm. obliquus externus, obliquus internus, transversus abdominis and
rectus ‘ibdominis). Ventrally, the connective tissue sheath of these muscles serves ;is
the site of origin for the rectus cervicis muscles mentioned above.
‘I’he only component of the ventral trunk musculature which inserts directly on
the cranium is the large, parallel-fibred, non-segmented m. longus cnpitis
(Wiedersheim, 1879; Nishi, 1938). This muscle originates from the basapophyses
of the first 12-16 trunk vertebrae and inserts on the cranium ventral to the
craniovertebral joint (Fig. 3). Because of its insertion and large size, this muscle is a
powerful ventral flexor of the neck and cranium, functions which are probably of
importance in burrowing as well as in feeding.
FUNCTIONAL MORPHOLOGY O F FEEDING
Diet and prgy capture
Checilians have been reported to be opportunistic carnivores (Taylor, 1968),
but may also be specialized (Wake, 1978). There are indications that prey
abundance and size influence diet. Barbour & Loveridge (1928) reported that
Roulmgerula appeared to eat termites primarily. Gymnobis multiplicata, based on gut
analyses (Wake, unpubl. data), takes diverse prey, including earthworms, termites,
and large (30 mm T.L.) orthopteran instars. Moll & Smith (1967) reported that a
D. mexicanus had consumed a Sceloporus; gut analyses of numerous specimens from
one Guatemalan population show that those D. mexicanus consumed only
earthworms, which were in great abundance (Wake, 1980b, and unpubl. data).
Prey capture involves a slow approach to the prey item until contact is almost
effected, then seizure by the jaws in a powerful bite. The caecilian usually does not
lunge at its prey, though there may be some anterior movement. The head is often
turned to one side to position the prey. Most caecilian prey are elongate, and
therefore can be seized at either end or along the body. In the laboratory, and
FUNCTIONAL MORPHOLOGY O F CAECILIAN FEEDING
87
presumably in nature, if the caecilian is not completely emerged from its burrow
when the prey is seized, it retreats backward into the burrow, spinning in
corkscrew fashion around its body axis, thus using the friction of the sides of the
burrow to constrict and shear the prey item to approximately the width of the
predator’s gape. When a caecilian feeds in a non-burrow experimental situation
and captures the prey along the body, ingestion activity rarely involves the
shearing behaviour, though we have observed it in one out of five
electromyography experiments.
Motion analysis of prg handling
In this section, we refer to two types of illustrations. The first (Fig. 4) is a series of
‘stills’ taken with the motor-driven Nikon at three frames s-’ . Two complete bite
sequences are presented in these photographs which reveal bulging of muscles
during feeding activity, the position of the head relative to the trunk and substrate,
and the general position of the tongue and hyoid apparatus. T h e second series of
illustrations (Fig. 5) is a set of tracings prepared from a 16 mm movie taken at 100
frames s-I, in which every tenth frame has been traced. In this illustration, the
frames illustrate head movements during a typical ‘strong bite’ sequence that
occurred during 1 s of a complete feeding event.
Once a prey item has been taken into the mouth, it is difficult to discourage the
animal from completing ingestion, even though this may occasionally require
several minutes. Normal feeding is composed of a number of bites interposed with
swallowing movements. Although feeding consists of a number of bite-swallow
cycles, which may be interrupted by pauses of variable length, the general
impression is one of relatively continuous and smooth passage of the worm into the
oesophagus.
In a normal bite sequence, the animal is resting with the anterior part of the
body-usually at least the lower jaw-in
contact with the substrate (Fig. 4D).
During opening, the mandibular symphysis remains in contact with the substrate
while the cranium is rotated dorsally. Maximum gape angles measured from
photographs are between 30 and 40”. As the jaw is closed, depression of the buccal
floor occurs (Figs 4C-G, 5C-E). ‘lhis action appears to be primarily passive, and
occiirs as the worm is forced between the palate and the tongue. There is no
musculature capable of producing the extreme depression seen in some sequences.
Subsequent raising of the buccal floor and hyoid region occurs briefly after
maximum distension of this region (1;igs 4D, H, 5E), and often simultaneously
with the maximum ‘strong biting’. Much of the musculature of the hyoid region,
including in particular the levator arcus branchialis, probably acts to compress the
tiyoid region.
During closing of the lower jaw, the neck is arched and the lower jaw may be
pulled away from the substrate (Fig. 4B, C). If the bite is a strong one, vertical
flexure of the craniovertebral joint may become pronounced (Fig. 5C-E). This
probably reflects contraction of the m. longus capitis. A visible tremor of the head
and neck region often takes place during this phase, giving the impression that
strong muscular contractions are occurring.
As noted above, an earthworm is drawn into the mouth in a relatively
continuous motion. Soft-bodied prey, such as worms, are forced into the pharynx
by squeezing with the teeth and tongue during bite sequences. Subsequent
\V. E. BEMIS E T 4 L .
88
- -
-.
FiSiii-r ,I. :35i i l m \tills 0 1
ii
cypiciil tkeding sequence, three frames s-'. Ser text for explanation
89
A
B
E
F
G
2GzzzL
D
H
Figure 5. Tracings from 16 mm movie taken at 100 frames s-’. Every tenth frame trared
movement of the prey into the throat seems to be caused by oesophageal peristalsis,
as suggested by Gans (1962). One observation, in particular, lends circumstantial
support to this supposition. The end of a worm was placed well into the mouth of a
specimen under MS222 anaesthesia sufficient to prevent normal biting
movements. Without any apparent external movement of the caecilian, the worm
was transported into its throat and completely ‘swallowed’. Occasionally, strong
lateral bending of the anterior part of the body occurred late in a normal feeding
sequence. Such movements may further facilitate prey transport.
Electromyography
Because many of the muscles described are either very small (e.g. m. levator
mandibulae externus) or deeply placed (e.g. m. longus capitis), we were unable to
do a complete electromyographic survey of all of the potentially interesting
muscles used in feeding. Instead, we focused on groups of muscles, trying in
particular to explore the function and period of activity of the interhyoideus
muscle (Group 11)and its relationship to the activities of the depressor mandibulae
(Group 111), internal adductors (Group I) and hypobranchial muscles (Group
IV) during normal biting cycles.
Electrode placement for Group I1 and Group I11 muscles was as shown in Fig.
6. For Group I muscles, the most effective electrode placement was at the insertion
site of the m. levator mandibulae anterior and m. levator mandibulae externus.
This placement did not allow study of either the m. levator quadrati or levator
6
w.E. BEMIS E T .If.
m
A
..
I
II
Figure 6. Lateral and ventral X-ray photographs showing electrode placement. Muscle group numbers
cctrl-rrporrd to t h r in the text and in Table I .
mandibulae posterior components of the Group I muscles. Group IV mucles were
studied by simply placing electrodes in the floor of the mouth, where most of the
activity recorded presumably reflected contractions of the geniohyoid and
intermandibularis. Muscles of Groups V and VI were not studied
electromyographically.
Figure 7 shows a representative tracing from the oscilloscope screen; a
Group
I
Group
II
Group
III
Group
I
Fiqire 7. Simultaneous electromyographic record of five bite sequences showing activity in muscles of
Group I (levator mandibulae anterior and levatnr mandibulae externus), Group I1 (interhyoidrusj,
Group IT1 (depressor mandibulae'i, and Group IV (intermandibularis and geniohyoideus). Total
eliipscd time = 12 s.
Hyoid/buccal bulge;
-
Neck bendina
Close
1
1
1
I
I
8
I
I
I
1
I
I
I
l
I
l
Jaw displacement I
Time
(5)
Figure 8. Summary diagram of electroinvog~aptiicactivity, head, and lower jaw movements during
three bite sequences. Muscle activity of Groups I through IV is shown by solid blocks; height of block
represents relative spike amplitude. Periods of hyoid/buccal bulging and vertical neck bending are
shown as determined from film records. j a w displacement (the relative position of the tip of the
mandible relative tn the maxillary tooth row) was measured from these same film sequences. As
cxplained in the text, vertical neck bending is thought to reflect contraction of thc longus capitis.
diagrammatic summary of electromyographic activities and jaw opening is shown
in Fig. 8. During a single biting cycle, jaw opening is initiated by activity in the m.
depressor mandibulae. This phase is very brief, usually complete within 0.5 s, and is
followed almost immediately by strong activity of Group I and Group I1
adductors. I n some records, the Group I adductors fired slightly in advance of the
Group I1 adductors, but the general pattern is one of sudden, continuous activity
in both groups. Bilateral activity of these muscles occurred simultaneously. T h e
actiiity of Groups I and I1 is often greatest (as judged by spike amplitude and
frequency) during the first 0.1 s of contraction during which jaw closing takes
place. High levels of acti\ ity in the adductors may be maintained throughout the
static pressure portion of the cycle during strong biting (which may continue for
between 0.3 and 1 .O 5) or may taper off either gradually or sharply, depending on
the strength of the bite.
Group IV muscles show \rery limited activity during depression of the lower jaw.
Such activity as we recorded may represent geniohyoid contractions. Following
the jaw closing phase, Group IV muscles begin contraction, often with a relatively
low level of activity, which increases throughout the remainder of the biting cycle.
92
L2.’ E REMIS E T .4L.
The level of activity recorded during this period was of greater amplitude and
fi-equency than that seen during normal gular pumping movements.
Following the end of the static pressure phase, all myographic activity may cease
for periods of 0.5 s to several seconds, after which another biting cycle may
occur.
DISCUSSION
Summary of feeding in Dermophis
In the preceding sections, aspects of the caecilian feeding apparatus have been
analysed by a variety of approaches. Caecilians are jaw feeders, and utilize the
bone and muscle systems of the head for both prey capture and most of prey
processing. Derrnoflhis mexicanus is known to feed primarily on earthworms, at least
in the population from which our samples were drawn, so earthworms were used as
prey items in this study. Once an earthworm is seized, it may be sheared against
the walls of the burrow by rotations of the body, or it may be ingested whole. l h e
sharp, recurved, ratchet-action teeth of adult Dermophis engage the prey, which is
then compressed into the pharynx by extremely forceful bites and constrictions of
the buccal floor.
Feeding movements are the consequences of activity in muscles belonging to six
major functional groups (Table 1 ) . Groups I, I1 and VI are used in adduction of
the jaw, while Groups I11 and V fbnction during jaw opening. Group I V muscles
are primarily invol\red in shifting food items from the mouth into the anterior part
of the oesophagus. During normal biting movements, four phases may be
recognized. During the jaw opening phase, the cranium is raised as a result of
activity in the depressor mandibulae muscle and probably dorsal trunk muscles as
well. Activity of the depressor mandibulae muscle peaks at maximum jaw opening,
then stops sharply as the levators mandibulae externus and anterior fire along with
the interhyoideus muscle to begin the very short jaw closing phase. By the end of
jaw closing, the hyoid/buccal bulge has reached its greatest extent, and ventral
bending of the head, presumably reflecting activity of the longus capitis muscles, is
well under way. During the subsequent static pressure phase, the hyoid bulge is
reduced as a result of activity in intermandibularis and geniohyoideus muscles;
other components of the hypobranchial musculature probably also play a role in
this action. The jaw may remain near its maximum closure for brief periods during
the static pressure phase, but as activity of first the Group I and then the Group I1
adductors drops out, the jaw tends to open slightly, perhaps as a result of elastic
recoil. Low level activity in the depressor mandibulae muscle may begin before
activity in the hypobranchial muscles is complete. Hypobranchial activity is taken
to reflect movements of the tongue in transferring food into the pharynx and
anterior part of the oesophagous. Transport appears to be a result of oesophageal
peristalsis. Some seyuences reveal a well-defined fourth phase of the biting cycle, a
pause phase interposed between the end of Group IV activity and the beginning of
strong Group I11 activity. A summary diagram of biting sequences showing
myograms, lower jaw movements, and interpretations is presented in Fig. 8.
In many respects, the feeding apparatus of Derrnophis is an extremely simple
mechanical system. Due to the strength and rigidity of the tooth-bearing bones and
the skull in general, bending or other deformation of the bony elements and their
I L‘\C
I 1 0 1 \I. RIORPHOI OGI 0 1 C \PA ILI 1 1 EEE,DIhG
93
Groupm
Group
I
Group II
Figure 9. Schematic diiigriirn illiistratiiig mechanism ofjaw closing. Musclcs in three distinct sites act
spricrgistically to produce ;I strong bite.
sutures with one another appears to play little or no role in feeding. The jaw joint
itself restricts movements of the lower jaw to ‘1 large extent, essentially a vertical
plane. The one major exception to this overall simplicity is the as yet
undocumented role of streptostyly during feeding.
If streptostyly is defined simply as the possession of a moveable quadrate, then
DermophiJ meets this requirement (Wake & Hanken, 1982). While many
niorpliologists have considered the role that streptostyly may play during
moL7ements of the lower jaw in a variety of vertebrates, most of this work has
involved interpretation of fiinction from anatomical material and not
documentation based on libing animals. In our own work, we have been unable to
demonstrate movements of the quadrate in adult caecilians during actual feeding
sequences since the quadrate is almost completely covered by the squamosal, and
the covered anterior component is that which is movable (Wake & Hanken, 1982).
Such an intriguing anatomical arrangement requires further investigation of
fiinction. The moveable quadrate may play a role in hearing, for it is the largest
element to articulate directly with the stapes.
L41though the mechanical arrangement of the caecilian skull and feeding
apparatus is essentially simple, three anatomically distinct groups of muscles are
involved in closing the lower jaw (Fig. 9). Of the muscles belonging to these three
groups, the interhyoideus (Group 11) and longus capitis (Group V I ) muscles are
the largest and probably the most important muscles used in applying pressure to
food items. ‘The particular arrangement found in caecilians does not occur in other
t’ertebrates.
Static pwssuie Cystems in caecilianJ and their evolution
Olson (1961) distinguished between two mechanically distinct methods of jaw
feeding in tetrapods. In the kinetic inertial method prey is stabilized by its inertia
while the jaws are rapidly moved around it. Such a mechanism is widely utilized
among various tetrapods. The alternative extreme recognized by Olson is the static
pressure method, in which large jaw muscles and teeth are used to apply large
forces to the prey item to crush, shear or otherwise break down food items prior to
swallowing. Basing his conclusions on the morphology of the skulls of extinct
rhipidistians, labyrinthodonts and various reptiles, Olson characterized the kinetic
inertial method ( K I ) as the primitkre tetrapod system, and pointed out some of the
many modifications of the K I system that have occurred in different tetrapod
94
W. E BEMIS ET A/..
lineages. From these examples, it appears that many different evolutionary
solutions have been reached to problems posed by the need for static pressure
systems (SP). Most of these solutions have in common the enlargement and
differentiation of pterygoideus musculature.
While recognizing the limitations of Olson's categorization of jaw mechanisms,
we note that Dermojhis and other caecilians have arrived at a particularly forceful
SP system using a completely different mechanical arrangement than Olson found
in various reptilian and mammalian lineages. This observation gives further
support to the idea that there may have been evolutionary premium placed on the
development of SP systems in certain vertebrate lineages.
Further, it would appear that the premium for powerful jaw adductors was great
enough in caecilians to force the conversion of the retroarticular process, a
structure which functions in jaw depression in other vertebrates, into a
structure that plays a role in both jaw opening and jaw closing. In achieving this
adaptation, a muscle already present in caecilians and present primitively in all
amphibians, but playing no prior role in jaw closing, was modified to become the
major muscle for that function. There is variation in the form and associations of
this muscle in primitive caecilians as noted by Nussbaum (1977).
The combined use of the retroarticular process and interhyoideus posterior
muscle in jaw closing may represent an adaptive solution to problems of packaging
jaw adductor muscles in a burrowing animal. The adductor muscle fossa in adult
Dermobhis and in most other caecilians is virtually completely roofed by bone.
There has been some question whether this represents the retention of the primitive
tetrapod solid skull roof or whether a solid roof has been independently re-derived
in some caecilian lineages as a special adaptation for burrowing (see Wake &
Hanken, 1982, for discussion). I n any event, one functional consequence of a solid
skull roof is that there is limited volume for the jaw adductors of the mandibular
arch to expand, either during function or phylogeny. O n e way to achieve larger
jaw muscles-and consequently larger static pressure forces-would be to increase
the size of the skull. But as Gans ( 1968, 1974) has shown for amphisbaenids, another
group of limbless burrowing tetrapods, energy expended in burrow construction
goes up exponentially as burrow diameter is increased. By having the major jaw
closing muscles outside of the temporal fossa, caecilians have 'solved' the problem
of static pressure generation without increasing the cross-sectional area of the head.
Speculation about how this transition may have occurred is premature for
although all extant caecilians have well-developed retroarticular processes, no
fossil caecilian material is available to document changes in the form of this
feature. Carroll & Currie (1975) propose that a Permian microsaur, Goniorhynchus,
may be close to the ancestry of caecilians, and as one piece of evidence, they note
the presence of a retroarticular process in this form and its absence in other
microsaurs. Based on their illustrations, however, the retroarticular process of
G'onioihynchur is a small element, giving little evidence of how evolutionary
elongation and change of function might have occurred. By almost any measure,
such a conversion represents a key innovation in morphology which has probably
fkcilitated the subsequent radiation of caecilians.
ACKNOWLEDGEMENTS
We thank David 8. Wake, Thomas A. Wake, Theodore Papenfuss and Robert
Seib for collecting the material used in this study; James Hanken and Katherine
FUNCTION t L MORPHOLOGY OF CAECILIAN FEEDI’VG
95
Thomas for preparing reference material; Hank Fujishige for assistance
with electronics; Gene Christman for preparing the figures; the Scientific
Photograph Laboratory at the University of California, Berkeley, for assistance
with photographic reproduction ; and Teriann Asami-Oki for typing the
manuscript. We thank various colleagues in the Departments of Zoology and
Physiology-Anatomy for the loan of various pieces of equipment, and especially
Harry Greene for use of his camera and electronic flash material. We appreciate D.
B. Wake’s critical review of the manuscript. All material will be deposited in the
Museum of Vertebrate Zoology, University of California, Berkeley. This work was
supported by National Science Foundation grant DEB 80-05905 to M.H.W., an
NSF Predoctoral Fellowship to W.E.B., and by funds from a Biomedical Research
Support grant via the Graduate Division to D.B.W. and M.H.W. for purchase of
the electromyographic equipment.
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