Zoological Journalofthe Linnean Society, 68: 1-40. With 29 figures
January 1980
The skull and jaw musculature as guides to
the ancestry of salamanders
ROBERT L. CARROLL
AND
ROBERT HOLMES
Redpath Museam, M ~ G i l lUniversity, M ~ ~ t r e Canada
a~,
AccepledJor publication October 1978
~ I ~ l lossil
ic
record provides no evidence supporting a unique common ancestry for frogs, salamanders
arid apudans. The ancestors of the modern orders may have diverged trom one another as recently as
250 inillion years ago, or as long ago as 400 million years according to current theories of various
authors. In order to evaluate the evolutiohary patterns of the modern orders it is necessary to
determine whether their last common ancestor was a rhipidistian fish, a very primitive amphibian, a
labyrinthodont or a ‘lissamphibian’. The broad cranial similarities of frogs and salamanders,
especially the dominance of the braincase as a supporting element, can be associated with the small
size of the skull in their immediate ancestors. Hynobiids show the most primitive cranial pattern
known among the living salamander families andprovide a model for determining the nature of the
.~~icestors
of the entire order. Features expected in ancestral salamanders include: ( 1) Emargination
01’ the cheek; (2) Movable suspensorium formed by the quadrate, squamosal and pterygoid;
( 3 ) Occipital condyle posterior to jaw articulation; (4) Distinct prootic and opisthotic; (5) Absence
(11 otic notch; ( 6 ) Stapes forming a structural link between braincase and cheek. In the otic region,
cheek and jaw suspension, the primitive salamander patternkesembles most closely the microsaurs
among known Paleozoic amphibians, and shows no significant features in common with either
ailcestral tkogs or the majority of labyrinthodonts. The basic pattern of the adductor jaw musculature
is consistent within both frogs and salamanders, but major differences are evident between the two
groups. The dominance of the adductor mandibulae externus in salamanders can be associated with
the open cheek in all members of that order, and the small size of this musck in frogs can be
associated with the large otic notch. The spread of different muscles over the otic capsule, the longus
liead ol the adductor mandibulae posterior in frogs and the superficial head of the adductor
inandibulae internus in salamanders, indicates that fenestration of the skull posterodorsal to the
orbit occurred separately in the ancestors of the two groups. Reconstruction of the probable pattern
01’ the jaw inusculature in Paleozoic amphibians indicates that frogs and salamanders might have
evolved from a condition hypothesized for primitive labyrinthodonts, but the presence of a large otic
iiutcli i n dissorophids suggests specialization toward the anuran, not the urodele condition. The
prcwnce o t either an einarginated cheek or an embayment of the lateral surface of the dentary and
the absence 0 1 an otic notch in microsaurs indicate a salamander-like distribution of the adductor
jaw muscles. The ancestors of frogs and salamanders probably diverged from one another in the early
Cdmiiiterous, Frogs later evolved from small lpbyrinthodonts and salamanders from microsaurs.
Feature, coilsidered typical of lissamphibians evolved separately in the two groups in the late Permian
ailti .ri-iassic.
KEY WORDS:- urodeles -jaw muscles - Paleozoic amphibians - modern amphibians - cranial
iiiorphology - phylogeny - microsaws - labyrinthodonts.
CONTENTS
. .
Introduction
Cranial comparisons
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0024-4082/80/0 1000 1-40/$02.00/0
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0 1980 The Linnean Society of London
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R. L. CARROLL AND R. HOLMES
Adductor jaw inuscles . . . . . . . . . .
Adductorjawinusclesofurodeles
. . . . .
Adductorinandibulaeexternus . . . . .
Adductor inandibulae posterior
. . . . .
Adductormandibulaeinternus
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Adductorjaw inusclesofanurans
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Adductorinandibulaeexternus . . . . .
Adductor inandibulae posterior
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Adductorinandibulaeinternus
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Adductor jaw inusculature in Paleozoic amphibians
Pedicellatr teeth
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Conclusions
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Atltleiitluin
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Acknowledgements . . . . . . . . . . .
References
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Abbreviations used in figures . . . . . . . .
Abbreviations used for muscles
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40
I NTRO DUCT1 0 N
Despite numerous recent publications concerning the origin and relationships
of the modern amphibian orders-Eaton (19591, Szarski (19621, Reig (19641,
Estes (19651, Cox (1967), Shishkin (1970),Jurgens (197 1) and most influentially,
Parsons & Williams (1963) - little can be said with confidence concerning the
specific relationships of frogs, salamanders and apodans. Following the revival of
the Lissamphibia concept by Parsons 8c Williams, many authors have accepted
the assumption that the three orders are closely related, having descended from a
common ancestor, itself distinguishable from other, more primitive, amphibians.
Fossil evidence is not yet available that conclusively supports either this view or
the alternative possibility of a distinct origin of the three groups. In view of the
extensive work currently being undertaken on the behaviour and physiology of
modern amphibians, it would be extremely useful to know the nature of their
relationships more specifically. Were the characteristics by which we recognize
frogs, salamanders and apodans largely achieved separately, or are they the result
of inheritance from a common ancestor that would be readily recognizable as
such?
According to current theories of the origin of modern amphibians, the initial
divergence of the three orders may have occurred as long as 400 million years
ago or as recently as 250 million years ago. Jarvik (1942, 1954, 1963) has argued
that anurans and urodeles evolved ultimately from different groups of
rhipidistian fishes, already distinct at the base of the Devonian. The time of initial
divergence may be assumed to have been late Silurian. Romer ( 19451, and many
others previously, had suggested that modern amphibians had evolved from
different groups of Paleozoic amphibians : frogs from labyrinthodonts and
salamanders from lepospondyls. Such ancestry would suggest an initial
divergence in the Lower Carboniferous or possibly Upper Devonian - approximately 340 million years ago. Noble (19311, Estes (1965) and others have
proposed an origin of both frogs and salamanders from among small Paleozoic
labyrinthodonts. If such a common origin does not imply a specificially
‘lissamphibian’ ancestor, the point of divergence might have been about 300
million years ago. Parsons 8c Williams ( 1963) argued that all modern amphibians
evolved from a common ancestor already specialized beyond the level of any
know group of Paleozoic amphibians. If the Lower Permian and Carboniferous
A N C t 5 I K? O F SALAMANDERS
62
I30
180
Triadobatrachus
z
2
LL
.(a
Do1e s e r p e t o n
p l a u s i b l e ancestor
o f lissamphibians).
z
z
a
W
x
z
I
Period during which microsaurs
may have d i v e r g e d from
a n c e s t o r s of l a b y r i n t h o d o n t s .
m
m
2
2 30
I
P e r i o d d u r i n g which urodeles and
f r o g s m i g h t Ilave d i v e r g e d f r o m
common 1issamphi b i a n a n c e s t o r .
280
-
y e r i o d o f time d u r i n g
w h i c h u r o d e l e ancestors
m i g h t have d i v e r g e d from
f r o g ancestors i f
lissamphibian hypothesis
i s incorrect.
31 0
34 0
z
0
>
w
a
z
Occurence o f d i s t i n c t l i n e a g e s
l e a d i n g t o f r o g s and salamanders
according to Jarvik.
400
4
LL
1
2
m
450
Time s c a l e i n
millions o f
y e a r s , from
Romer 1966.
Figut-e 1. Geological ranges of modern amphibian orders and possible times of divergence of the
dncestorb ( ~ frogs
t
a n d salamanders according to various theories. A recently described larval
salamander from Russia (Ivakhnenko, 1978) extends the range of urodeles back to the late Triassic.
do provide a good record of the types of amphibians living during this time
(Carroll, 19771, it is probable that a lissamphibian ancestor such as Parsons 8c
Williams proposed evolved subsequent to about 250 million years ago. The
possible time of divergence differs by approximately 150 million years according
to the various theories (Fig. 1).
Frogs and salamanders did unquestionably share a single common ancestor at
some stage. Difficulties arise in establishing the probable time of original
divergence, and in determining to what extent the anatomy of the ancestral
group is shared by its living descendants. Our appreciation of the evolutionary
position of frogs and salamanders would presumably differ considerably
4
R. L. CARROLL A N D R. HOLMES
depending o n whether their last common ancestor was a rhipidistian fish, a very
primitive Paleozoic amphibian, a labyrinthodont, or a ‘lissamphibian’.
The earliest known frog, the LowerJurassicgenus Vieraellu (Estes8c Reig, 1973)is
known from a single, nearly complete skeleton which can be included in the most
primitive family of living frogs, the Ascaphidae. All of the major groups of frogs
may have differentiated by the end of the Jurassic. The only known fossil apodan is
represented by a single vertebra from the Paleocene (Estes 8c Wake, 1973). It is
placed in a distinct genus, but is closely related to the living forms.
The earliest remains of salamanders consist of a cervical vertebra from the Middle
Jurassic (Seiffert, 1969: Estes 8c Hoffstetter, 1976)a complete and beautifidly preserved
skeleton from the Upper Jurassic of Russia, a tiny lawal stage from the Upper Triassic
(Ivakhnenko,I978)and a femur from the Upper Jurassic (Hecht 8c Estes, 1960).Fossils
from the Cretaceous include some apparently primitive genera, such as Romonellus
(Nevo 8c Estes, 1969jand Albanerpeton (Estes 8c Hoffstetter, 1976)and others (Estes,
1965, 1969 c, 1975)that clearly demonstrate the presence ofmodern families. The
early fossils of frogs, salamanders and apodans provide little more anatomical
information regarding the ultimate origin of these groups or their degree of interrelationship than do living genera. They simply establish a minimum time for
the achievement of the definitive features of each group. In the absence of any
fossils definitely linking the three modern orders with one another, it is necessary
to appraise our knowledge of the origin of each group separately.
The only fossil that establishes any connection between modern and Paleozoic
amphibians is the genus Triadobatrachus[Protobutrachus]from the Lower Triassic of
Madagascar (Piveteau, 1937). Estes 8c Reig (1973) in the most recent appraisal of
the origin of frogs, accept this genus as belonging to the group from which the
modern order evolved. Watson (1940) had previously stressed the affinities of
Triadobatrachus with labyrinthodont amphibians. The discovery of a labyrinthodont amphibian with pedicellate teeth (Bolt, 1969, 1977) further supports the
contention that this group may include the ancestors of frogs.
I t has recently been suggested that apodans might have evolved from a group
of elongate, burrowing amphibians such as the lepospondyl microsaur family
Goniorhynchidae (Carroll 8c Currie, 1975). Such an origin has not, however,
been confirmed by the discovery of any genera intermediate in morphology
between Paleozoic microsaurs and Tertiary apodans.
There are no fossils linking salamanders with any of the Paleozoic amphibians,
but arguments have been made for their relationship with both lepospondyls
(Shishkin, 1970) and with labyrinthodonts (Estes, 1965). Derivation from
labyrinthodonts implies relatively closer affinities with frogs (presuming frogs to
be of labyrinthodont origins), although it does not necessitate a common
‘lissamphibian’ ancestry. The ancestry of salamanders and the nature of their
relationship with frogs remain among the most important unsolved questions
associated with the problem of the affinities of the modern amphibian orders.
Although continued reference to frogs will be made, the major effort of this
paper is to determine what information the skull and jaw muscles of living
salamanders may offer regarding the probable origin of urodeles.
Although knowledge of all aspects of anatomy, physiology and behaviour
would be useful in evaluating the degree of relationship of the modern
amphibians, little more than the skeleton is preserved in fossil forms, and final
assessment of ancestry must be determined primarily on the basis of that system.
ANCESTRY OF SALAMANDERS
5
Postcranially, the dif€erences between frogs and salamanders are very great,
reflecting strong habitus divergence whatever the ultimate relationship. Only the
general nature of the vertebrae suggests a common pattern (Wake, 1970). In
contrast, the skulls of frogs and salamanders are similar, at least in so far as they
differ from those of other vertebrate groups. There are, however, some
consistent differences which suggest that further study would be profitable. I t is
surprising that relatively little attention has been paid to the question of the
origin of the skull pattern in either frogs or salamanders, aside from assuming
general reduction in ossification from that of Paleozoic amphibians. The
structure of the skull, particularly of the temporal region and the area of the jaw
musculature, has proved of extreme importance in elucidating the pattern of
evolution in bony fishes (Schaeffer 8c Rosen, 19611, reptiles (Romer, 1956) and
the origin of mammals (Barghusen, 1972; Crompton & Parker, 1978). Because of
the readily visualized importance of this area, and the generally conservative
nature of the jaw musculature, it is probable that study of this system would also
cast some light on the origin of the modern amphibian groups.
CRANIAL COMPARISONS
There are several significant features of the general cranial anatomy that unite
frogs and salamanders and distinguish them from all Paleozoic amphibians. The
primitive amphibian skull (Fig. 21, like that of primitive reptiles and early bony
fish, is composed of a nearly continuous covering of dermal bone, with only
orbital, narial and pineal openings dorsally, and the internal nares and openings
for the adductor jaw musculature on the palatal surface. Inside the dermal box is
suspended the endochondral braincase. In frogs and salamanders, the dermal
ossification of the skull roof and palate is much reduced, and the braincase,
which incorporates dermal bone along the midline, forms a major structural
element of the skull. It serves as a longitudinal beam, extending from the occiput
to the snout, with the otic capsules extending laterally to support the cheek
dorsally and the pterygoid ventrally.
The relatively large size of the braincase and its structural significance can be
associated with the absolutely small size of the skull. It is almost certain that the
initiation of the cranial patterns of frogs and salamanders was associated with
small skull size. The few larger members of these orders are almost certainly
specialized in this feature. The minimum functional size of the semicircular
canals (Jones & Spells, 1963) and the brainstem require that the braincase occupy
much of the skull in small vertebrates. With a skull less than about 2 cm in length
and width, the otic capsules extend close to the cheeks and the braincase
approaches the snout anteriorly. Such relative expansion of the braincase
compared with the remainder of the skull permits a different pattern of the
surrounding support structures than that seen in most Paleozoic amphibians.
Another aspect of small skull size is the relative expansion of the orbits and
nasal capsules. Similarities of the skull in the ancestors of frogs and salamanders
that can be attributed to small size do not, of themselves, imply common
ancestry, since grossly similar patterns might have evolved in descendants of
different Paleozoic amphibian groups with primitively solidly roofed skulls.
Watson ( 1940), for example, illustrated both labyrinthodonts and a lepospondyl
(termed Hylonomus geinitzi) as possible anuran ancestors.
R. L. CARROLL A N D R. HOLMES
6
A
L
D
Figure 2. The skulls of Paleozoic and modern amphibians. A. Rana catesbeiana. 8 .Ambystoma manrlatum.
C. The labyrinthodont Dendrerpelon. D. The lepospondyl microsaur Asaphestra. Although both ma'or
groups of Paleozoic amphibians exhibit considerable diversity, these genera are representative oflthe
basic patterns from which frogs and salamanders may ultimately have evolved.
Other features that are common to primitive frogs and salamanders include a
movable articulation between the base of the braincase and the pterygoid, and
large palatal vacuities. These characteristics are known among both labyrinthodont and lepospondyl amphibians.
Within this general pattern, common to the two groups, there are also
consistent differences that distinguish the skulls of all urodeles from those of
anurans. In both groups there is considerable diversity. This is particularly true
of the frogs (Trueb, 1973). The fossil record of frogs (Estes 8c Reig, 1973)does,
however, provide a reasonable basis for establishing the primitive pattern for the
group. The fossil record of salamanders does not give much evidence as to the
primitive skull pattern of the group, but the anatomy of the living families is
sufficiently conservative to suggest a similar basic pattern for the common
ancestral stock.
Frogs (Figs 2, 31, including the ancestral form Triadobatruchus (Fig. 27),in so far
as it is known, have similar cranial specializations. All have a fused frontoparietal
A N C E S r K Y O F SALAMANDERS
a
Figure 3 . Representative skulls of the most primitive frog family Ascaphidae. A. The living genus
Ascaphus in dorsal, palatal, lateral and occipital views. B. Vieradla, the oldest known frog, Lower
Jurassic (From Estes & Reig, 1973). In Ascaphus the otico-occipital region is not fully ossified and
t l i i - w distinct centers of ossification are evident. This genus lacks the stapes, the tympanum and the
iiiiddle ear cavity. In these features it is specialized over the condition seen in Jurassic ascaphids.
bone and a well defined otic notch formed by the squamosal. The palatal margin
o f the skull is nearly always continuous, with the quadrate characteristically
joined to the maxilla by a quadratojugal. The quadrate is characteristically at
the posterior margin of the skull and the gape of the jaw (primitively defined by
the length of the tooth row) is very great, with the jaw angle behind the rear
margin of the orbit. The otic capsule is always ossified as a single unit in the
adult. The stapes is a rod-shaped structure, characteristically activated by a
tympanum. As in salamanders, there is frequently a second ear ossicle, the
operculum, making up a portion of the otic capsule adjacent to the base of the
stapes.
Among salamanders (Figs 4-12), there is never an otic notch and the frontals
and parietals are not fused. The jaw articulation is generally well anterior to the
level of the occipital condyle and the gape of the jaw and the tooth row are comparatively short. Of particular importance is the cheek region. There is only
rarely an independent quadratojugal, and there is always a gap between the
quadrate and the maxilla. (A quadratojugal is present in TyEototrzton and the
closely related Oligo-Miocene salamandrid Chelotriton (Estes, pers. comm.). This
bone ossifies late in ontogeny and its general absence in urodeles may be
8
R. L. CARROLL A N D R. HOLMES
attributed to paedomorphism.) Among some hynobiids, ambystomatids and
proteids, the otic capsule is made up of distinct opisthotic and prootic ossifications. In other genera, it is ossified as a unit. The stapes, in contrast to that
of frogs, has a very large foot-plate and a short stem. There is never a middle ear
cavity or tympanum.
The similarities and differences between the skulls of frogs and salamanders
may be interpreted as resulting from simple divergence from a common
ancestral pattern, or as resulting from a long period of convergence and
parallelism from clearly distinct ancestral stocks. Current evidence strongly
suggests evolution of the frog cranial pattern from that of small labyrinthodonts
such as the dissorophid genus Doleserpeton (Bolt, 1977). The question of
salamander ancestry can be evaluated by considering whether or not their cranial
anatomy supports derivation from the same stock.
In order to investigate this problem in detail, it is necessary to determine the
primitive cranial configuration for salamanders as a group. Unfortunately, the
fossil record of urodele skulls is very incomplete, and most adequately preserved
specimens from the Mesozoic show specific similarities only with the more
specialized modern families - Sirenidae, Proteidae and Amphiumidae. It is
commonly accepted that hynobiids are the most primitive of living salamanders
in terms of both their general anatomy and biology (Hecht & Edwards, 1977).
Examination of a number of species (Fig. 4) shows a relatively constant structure
that, compared with skulls of all other salamander families (fossil and living),
appears closest to that seen in Paleozoic amphibians.
The general configuration of the skull resembles that of small labyrinthodonts
and lepospondyls in the large extent of dermal bone, with relatively limited
dorsal exposure of the endochondral braincase. Of the bones present in most
Paleozoic amphibians, only those at the posterior orbital margin (postfrontal,
jugal, postorbital and quadratojugal) and at the posterior margin of the skull
table (postparietal, tabular and supratemporal) have been lost, together with
the ectopterygoid on the palatal surface. The palatine bone appears during
development in most salamander groups, but is lost in most adults except
sirenids, the axolotl and other neotenic forms. In hynobiid larvae (Fox, 1959) the
palatine occupies a position comparable to that bone in most Paleozoic
amphibians. As in several microsaurian lepospondyls (Carroll & Gaskill, 1978)
and some labyrinthodonts (Romer, 1947) it bears a row of teeth parallel with
those of the jaw margin.
The parietal, frontal, prefrontal, nasal, lacrimal, premaxilla, septomaxilla,
maxilla and vomer retain their primitive configuration and relationships. The
pterygoid is small, but has a well-defined articulation with the base of the
braincase. The base of the epipterygoid is closely integrated with the pterygoid,
but in Hynobius naeviw, the stem retains its primitive character as a narrow rod,
extending vertically alongside the braincase, just anterior to the prootic foramen
(Fig.4).
The major differences from Paleozoic amphibians are in the area of the cheek
and the posterior portion of the braincase. The squamosal is in contact with the
parietal dorsally, without intervention of any of the primitive temporal series
(tabular or supratemporal). The otic capsule underlies the squamosal anteriorly
and together with the parietal forms a surface for its attachment which appears to
allow the distal end of the squamosal to swing in a very restricted medio-lateral
ANCESTKY OF SALAMANDERS
A
B
P
Figure 4. Representative skulls of the most primitive family of living salamanders, the Hynobiidae. A.
Hynobivr lsvensrs (British Museum no. 1902-5-19-6), skull roof and posterior palatal surface, bones
of right suspensorium (squamosal, quadrate and pterygoid) are dotted. B. Batrachuperus sinasis
(British Museum no. 94-9-15-15) skull roof and palate (lateral view of this specimen shown in Fig.
15 B). C. Hynobius naevius (Paris Museum no. 1969-loti), skull in dorsal and lateral views and in
sagittal section (occiput of this specimen shown in Fig. 15 E). Cartilage and connective tissue coarsely
stippled.
9
10
R. L. CARROLL A N D R. HOLMES
I
m”
Figure 5. Skull of Cryptobranchus allegheniewis in dorsal, palatal, lateral and occipital views. The cryp
tobranchid pattern is generally considered to be directly derived from that of hynobiids. The skull is
much inore open and flattened. The squamosal retains a broad contact with the parietal. Ventrally,
the pterygoid has a very broad contact with the parasphenoid and sphenethmoid, precluding
movement of the suspensoriurn. This family is neotenic and an operculum is not developed.
arc. Anteroposterior movement would appear to be precluded by the hinge-like
nature of the joint.
In hynobiids, the squamosal forms a closely integrated unit with the quadrate
and pterygoid. The pterygoid is free to move across the articulating surface of the
basicraniurn as the squamosal swings on the parietal and prootic. On the basis of
manipulation of dissected specimens and observations of dried skulls, it seems
possible that the movement is limited to one or two millimetres, or a few degrees
of arc. Confirmation of skull movement requires quantitative study of living
material. Acceptance of this configuration of the squamosal as primitive for
salamanders as a group is based on broad similarities of its shape and position
relative to other bones in all salamander families. Some support for the
assumption that there was a movable suspensorium in ancestral salamanders is
provided by the presence in all salamanders, in contrast with frogs, of a large
muscle, the interhyoideus posterior (Fig. 61, connecting the base of the jaw
suspension with the midline and the gular fold. In addition to other functions,
this muscle could act to adduct the suspensorium, an action very unlikely in
frogs, in which mediolateral movement of the squamosal would interfere with
the function of the middle ear.
In species of Batrachuperus and Hynobius, the otic capsule is composed of two
clearly separate ossifications. Anteriorly, the prootic appears to have
incorporated the basisphenoid area of more primitive amphibians and like that
unit, bears a well-developed facet for articulation with the pterygoid. Posteriorly,
ANCESTRY O F SALAMANDERS
A
Figure 6. A. Skull of Ambystoma maculutum in dorsal, palatal, lateral and occipital views. Amhystornatids are considered among the more advanced salamanders because of their practice of
internal fertilization (in contrast with hynobiids and cryptobranchids), but the skull is basically
similar tu that of hynobiids in the configuration a n d distribution of the individual bones. The otic
capsule is typically ossified as a single unit, and the squamosal is not in contact with the parietal. The
pterygoid typically retains a well developed area of articulation with the base of the otic capsule. B.
Interniandibular musculature of Ambystoma tzgrinum (from Larsen & Guthrie, 1975). This pattern is
characteristic of primarily terrestrial salamanders. The interhyoideus posterior is not present in adult
murans, but is a n important muscle in all urodeles. Abbreviations used only in this figure: ap,
aponeurosis; gh, geniohyoideus; gm, genioglossus, medial division; ih, interhyoideus; im, intermandibularis posterior; ip, interhyoideus posterior.
a single ossification incorporates areas that were more primitively recognizable as
separate exoccipital and opisthotic. In the fusion of these elements, hynobiids
might be considered advanced above the condition seen in living proteids (Fig. 9 )
where they are separate, although it is usually considered that proteids retain a
larval condition rather than one that was expressed in primitive adult
salamanders (see Hecht & Edwards, 1977 for discussion). Fox (1959) has
demonstrated the incorporation of the exoccipitals into the opisthotic during
development in Hynobius. As in frogs, the occipital condyles in all salamanders
are formed by posterior projections of the exoccipitals, and the basioccipital
(present in the majority of Paleozoic amphibians) does not ossify. Primitive
12
R. L. CARROLL AND R. HOLMES
salamanders (Fox, 1959)retain a distinct XIIth cranial nerve, exiting through the
exoccipital, as in most Paleozoic amphibians.
As in all other salamanders, hynobiids have no tympanum or middle ear
cavity. The stapes has a wide foot-plate and a short stem, attached by a ligament
to a posterior process of the squamosal. Embryological evidence presented by
Fox ( 1959) shows a close connection between the stapes and the palatoquadrate
in a variety of salamanders. This may be interpreted as a retention of a primitive
condition, such as that seen in rhipidistians and early reptiles (Heaton, 1978)in
which the hyomandibular-stapes supports the braincase against the cheek.
Structurally, the stapes continues to serve as a link between the cheek and the
braincase in the adults of many salamander groups.
Hynobiids show a variety of patterns in the area of the operculum (Monath,
1965). Salarnandrella keyserlingz and Onychodactylus japonicus have no muscular
attachment from the fenestral plate to the shoulder girdle and no element that
can be considered an operculum. Batrachuperus pinchonii lacks a distinct
operculum, but has a cartilaginous area of the otic capsule ventral to the fenestra
vestibuli to which is attached the levator scapulae (the ‘opercularis’ muscle). In
a variety of species of Hynobius, there is a distinct, but cartilaginous, operculum to
which is attached the levator scapulae.
Selection of certain hynobiids as representing the most primitive cranial
configuration among living salamanders is based primarily on broad similarities
with Paleozoic amphibians. It is supported by surprisingly strong similarities
among some genera within the families Ambystomatidae and Salamandridae
(Figs 6 , 8) suggesting divergence from a close common ancestor. In most
ambystomatids and salamandrids, the lacrimal is lost and the otic capsule is
Figure 7 . Skull of Phaeognathur hubrichti in dorsal and palatal views (from Wake, 1966). The
plethodontids are the most numerous and varied of the modern salamander families. The pattern of
the skull varies widely from genus to genus. It is generally accepted (Regal, 1966: Hecht & Edwards,
1977) that plethodontids were derived from the base of the ambystomatid stock. They show a
continuation of trends evident between hynobiids and ambystomatids to reduce the extent of dermal
ossification, with the otic capsule, in particular, forming a very substantial portion of the skull.
Dorsally, the pattern of the suspensorium can be seen as an extension of that seen in ambystomatids,
but ventrally it differs greatly in the loss of the pterygoid.
A
W
oper
P
C
Figure 8 . Skulls otsalamandridae.A. Sdamandra aka, from Wiedersheim (187 7). in dorsal and ventral
views. I n its general anatomy, the skull of Sdamandra atra resembles those of ambystomatids.
According to Regal ( 1966) the embryological development of the vomer is fundamentally different,
iridicatiiig d separate evolution from a hynobiid level. 8 . Nolophthdmur urridescenr in dorsal, palatal,
lateral and occipital views. Other members of the family Salamandridae show an increase in
ossilication from that of Sdamandra (which is presumed to be primitive for the family on the basis of
siniilarities with hynobiids). The frontal has grown back to reach the squamosal, forming a bar
separating the posterior extent of the adductor mandibulae internus superficialis from the adductor
riiandibulae externus. The suspensorium is immobilized. C. Tylototrilon, palatal view, from Noble
(1951). Shows extension of the maxilla nearly to the quadrate. This condition was considered
primitive by Noble, but in view of the secondary elaboration of the frontal and squamosal. the great
length of the masilla is more likely to be a specialized feature. The specialized nature of the frontosquamosal arc is discussed by Naylor 11978).
14
R. L. CARROLL AND R. HOLMES
A
Figure 9. Representative skulls of the neotenic family Proteidae. Necturus and Proteus are among a
number ofsalamanders that have a highly specialized skull and whose relationships with other families
are uncertain. In the living genera, the maxillae are lost and functionally replaced by denticulate
palatopterygoids. A. Necturus in dorsal, palatal, lateral and occipital views; this genus appears
primitive in the retention of three distinct centers of ossification in the area of the otic-occipital:
exoccipital, opisthotic and prootic. A distinct area of articulation is evident between the prootic and
the palatopterygoid, but unlike the condition in hynobiids, ambystomatids and primitive salamandrids, the pterygoid is integrated with the remainder of the palate by an anterior contact with the
vonier and parasphenoid; movement of the suspensorium may be possible, however. B. Opistotriton;
this skull from the Paleocene shows general resemblances with Necturw (Estes, 1975) but is primitive
in retaining contact of the parietal and squamosal above the otic capsule and in having a well
developed maxilla. As in hynobiids and cryptobranchids, proteids retain a columellar process of the
squamosal.
ANCESI’KY OF SALAMANDERS
15
Figure 10. Skull of Amphiuma in dorsal, palatal, lateral and occipital views. Amphiuma is the
only living representative of a further family of specialized aquatic salamanders. Unlike Necturus, the
nidxilla is a large element, but the pterygoid is small and articulates with the base of the braincase.
Tlic squainosal is firmly integrated with the otic capsule. The otic capsule is almost completely covered
doi-sally by the parietal. This genus has a ligament joining the stem of the stapes with the quadrate.
A n anterior portion of a n amphiurnid skull from the Upper Cretaceous, described by Estes i 1 9 6 9 ~ )
indicates the early establishment of this basic configuration.
ossified as a unit. Functionally the dermal skull roof remains basically the same.
In most species, the otic capsule comes to be exposed between the parietal and
the squamosal and the squamosal now attaches solely to the unitary otic
capsule. One major change seen between hynobiids and even the most
conservative of salamandrids and ambystomatids is in the pattern of the
vomerine teeth. In ambystomatids, they form a transverse series, nearly reaching
the maxillae. In salamandrids, they extend posteriorly, across the surface of the
parasphenoid to the level of the basicranial articulation (Regal, 1966).
The configuration of the skull seen in plethodontids (Fig. 7) is a further
extension of the specialization noted in ambystomatids. The other salamander
families (Figs 9, 10-12) depart to a greater degree from the configuration seen in
hynobiids, primitive salamandrids and ambystomatids, but all retain a broadly
similar suspensorium, formed by the squamosal and quadrate.
Considering all currently known living and fossil salamanders, hynobiids
appear to show almost entirely primitive character states for the characteristics
here emphasized. N o features have been recognized in hynobiids as a group that
16
K. L. CARROLL A N D R. HOLMES
0
A
Figure 11. Skulls of Sirenidae. A. Siren in dorsal, palatal, lateral and occipital views. The sirenids are
among the most specialized ofliving salamanders. The maxilla in the living genera is reduced to a tiny
remnant and the premaxilla has lost its teeth. B. The Late Cretaceous genus Habrosaurus, palatal view,
from Estes (1965), shows a much more normal arrangement of the marginal tooth-bearing elements.
The pterygoid is completely lost, but unlike other adult salamanders, there appears to be a discrete
palatine bone. The squamosal is firmly united with the otic capsule. The exoccipital appears as a
distinct ossification.
Figure 12. Skull ofAlbanel.peton,in dorsal and lateral view, from Estes & Hoffstetter (1976). The only
adequately known skull of the extinct family Prosirenidae, Miocene. The skull configuration is
advanced over that of the hynobiids in the fusion of the frontals and the great dorsal exposure of the
otic capsule. In contrast with most other salamanders, this family does not have pedicellate teeth.
ANCESTRY OF SALAMANDERS
17
would preclude salamanders with this morphological pattern having given rise to
all other living salamander families (Hecht 8c Edwards, 1977). Hynobiid cranial
structure seems to provide a valid basis for comparison with Paleozoic
amphibians.
The following cranial characteristics are considered of particular importance
in primitive salamanders, and would be expected in the immediate ancestors of
the group:
( 1 ) Emargination of the cheek
(2)Jaw suspensorium formed by quadrate, squamosal and pterygoid. Pterygoid
movable on the basicranial articulation and squamosal hinged to otic
capsule and parietal
(3) Otic capsule made up of distinct opisthotic and prootic
(4) Occipital condyle posterior to jaw articulation
(5)Double occipital condyle, loss of the basioccipital
(6)Absence ofa tympanum
(7)Stapes with a large foot-plate and forming a structural link between the
braincase and the cheek
Items 1, 2, 4, and 5 are definitely specializations over the condition in most
Paleozoic amphibians, although 4 is a common feature of larval labyrinthodonts.
Item 3 is a primitive character, but a more specialized condition occurs in some
Paleozoic amphibians. I t is not possible to ascertain with assurance what the
primitive character state was in regard to the stapes and the otic notch among
plausible lissamphibian ancestors. One of the most primitive adequately known
amphibians, the Lower Carboniferous labyrinthodont Greererpeton (Carroll,
1980) lacks an otic notch and has a large h omandibular supporting the
braincase against the cheek. This may represent Xe primitive character state for
amphibians as a group. The embryological association of the stapes and the
palatoquadrate in salamanders shown by Fox (1959) can be interpreted as a
direct inheritance from this condition in primitive amphibians.
Salamanders differ markedly from labyrinthodonts in the emargination of the
cheek. All labyrinthodonts maintain an unbroken palatal margin. Salamanders
differ from all but a few labyrinthodonts in lacking an otic notch. The
dissorophid labyrinthodonts, which most closely resemble frogs (Bolt, 197 7 ),
have a well developed notch that almost certainly supported a tympanum, and
have a small stapes that could have functioned like that of modern frogs. In
contrast to primitive salamanders, the otic capsule in dissorophids and their
close relatives (Olson, 1941; Sawin, 1941; Carroll, 1964) is formed primarily by a
single large ossification which, as in frogs, forms a stout lateral process of the
posterior portion of the braincase. It is conceivable that salamanders evolved
from such labyrinthodonts, but this derivation would require considerable
reorganization of the skull.
Much closer resemblances can be noted between primitive salamanders and
certain genera of lepospondyl amphibians included in the order Microsauria
(Carroll & Gaskill, 1978). Primitive microsaurs (Fig. 2) have a solidly roofed
skull, but members of two otherwise quite distinct families have evolved a deep
emargination of the cheek (Fig. 13). A condition most like that of salamanders is
seen in the family Hapsidopareiontidae. In the genus Liistro&s, the squamosal is
reduced to a narrow vertical rod that extended medially to the level of the otic
L
R. L. CARROLL AND R. HOLMES
I8
Figure 13. Skulls of rnicrosaurs. A. Mimuroter. B. Oslodolepis. As in urodeles, there is a large
ernbayment of the cheek and the occipital condyle is situated behind the level of the jaw articulation.
Members of this family have a large pleurosphenoid ossification that would not be expected in a
urodele ancestor. C. The gymnarthrid Curdzocephalus. The cheek shows little ernargination, but the
lateral surface of the dentary is excavated for the insertion of a large external adductor. The occipital
condyle is far posterior to the level of the jaw articulation, exposing the middle ear in a manner very
similar to that of urodeles. D. Lower jaw of Euryodu~,another gyrnnarthrid, showing a very strongly
developed area for insertion of the external adductor. E. Llzstrophus, family Hapsidopareiontidae. This
genus has a jaw suspensorium like that of primitive salamanders, with a narrow, upright squamosal
exteiiditigltnedially to the otic capsule and the parietal. It might have articulated with the braincase.
The quadratojugal is very small. Unlike the condition in most salamanders, the occipital condyle is
iiot known to extend behind the level of the jaw articulation in this family. Scale for each skull is
one inin.
capsule and parietal (Fig. 13C). A narrow postorbital bar is retained, but there is
a large gap between the maxilla and the jaw suspensorium. As in salamanders,
several families of microsaurs (although not known members of the
Hapsidopareiontidae) have the occipital condyle well behind the level of the jaw
articulation.
All microsaurs lack an otic notch. As in salamanders, the stapes (Figs 14, 15)
has a broad foot-plate, and a short stem, extending toward the squamosal or
quadrate. In so far as the braincase is known, the otic capsule is always ossified
from separate opisthotic and prootic elements and the exoccipital is not fused to
the opisthotic (Fig. 15).Microsaurs retain a basioccipital, but the exoccipitals are
clearly separated and form double condyles in Hupsidopureion.
A striking resemblance between a variety of microsaurs and primitive
salamanders is in the area of the otic capsule adjacent to the fenestra ovalis. In
B
Figure 14. Palates of microsaurs. A. Gornorhynchuj. B. Mitraroler. C. Cardzocephalus. These genera
Iiavr a staprs with a large footplate adjacent to an unossified area of the otir capsule that may have
Iwu~edail operr.uluin or connective tissue that was linked to the shoulder girdle by an1 opercularis
iiiuscle. The stein of the stapes is directed towards the quadrate and the occipital condyle is behind
tlir jaw articulation. As in larval and neotenic salamanders, a row of palatal teeth parallels the jaw
iiia~-gin.
Figure 15. A, B. Lateral views of the skulls of the microsaur Llislrophus and the hynobiid Batrachuperus
wmi) rlie postorbital bar of the rnicrosaur is represented by a dashed line. The braincase and
ptcrygoid havr been restored o n the basis of other members of the family Hapsidopareiontidae. The
r p i p t r r y g d is based on the structure common to other microsaur genera. C, D, E. Occiputs of.the
niici-osaurs Cardzocephalus (C) and Hapsidopareion (D)compared with the salamander Hynobius naevius
(El. Specializations of the salamander include the fusion of the exoccipitals and otic capsule and the
loss o t the derinal bones at the skull margin: the postparietals and the tabulars. The scale is 1 mm.
members of the families Ostodolepidae, Gymnarthridae and Goniorhynchidae
(Figs 14, 16) there is an unossified area medial to the base of the stapes.
Osteologically, the configuration is almost identical with that seen in
Batrachuperus sinensis and Hynobius naevius, in which there is a muscular connection between the otic capsule and the shoulder girdle, but in which the
operculum is not a distinct ossification.
Taken by themselves, these numerous points of resemblance between
salamanders and microsaurs might be considered to support close relationship.
20
R. L. CARROLL AND R. HOLMES
Figure 16. Palatal views of the skulls of A, the primitive salamander Hynobius naevius, showing the
relationship of the opercularis and adjacent hypaxial musculature; 8,the microsaur Mimaroter with
these muscles restored according to the pattern in Hynobiw.
Although no one microsaur that has so far been described has all the
characteristics expected in a salamander ancestor, such an animal would,
nevertheless, readily fit within the criteria established for the group as a whole,
and might be included within either the family Gymnarthridae or
Hapsidopareiontidae.
In conjunction with the differences in the bony anatomy of the skull of frogs
and salamanders, there is also a consistent difference in the pattern of the jaw
musculature. Although there is always some question of the validity of restoring
musculature in extinct forms, the configuration in living frogs and salamanders
is so consistent and so distinctive in each that it seems logical to assume the same
pattern in their immediate ancestors in the early Mesozoic in which an essentially
modern skull morphology had already evolved. The jaw musculature may
provide additional clues as to the significance of the differences in the
surrounding skull bones.
ADDUCTOR JAW MUSCLES
The terminology of the adductor jaw musculature developed by Luther (1914)
and Lakjer (19261, and used by Save-Soderbergh (1945), Haas (1973) and
Schumacher ( 197 31, together encompassing all the non-mammalian tetrapods,
allows simple and consistent comparisons throughout these groups. Three major
units of the adductor jaw musculature can be recognized by their position
relative to branches of the trigeminal nerve (Fig. 17). The adductor mandibulae
externus lies lateral to the maxillary (V,) and rostral to the mandibular (V,)
branches of trigeminal nerve. The adductor mandibulae internus lies medial
to the maxillary (V,) and rostral to the mandibular (V,) branches of trigeminal
nerve, and the adductor mandibulae posterior lies lateral to the maxillary (V,)
and posterior to the mandibular (V,) branches of trigeminal nerve. Each of these
three masses is variably subdivided in different tetrapod groups.
ANCESTRY OF SALAMANDERS
MAM E
MAMP
b igure 1 7 . Subdivision of the adductor jaw musculature giving the nomenclature of Save-Siiderbergh
(1945).
The jaw musculature of modern amphibians has been described systematically
and in detail by Lubosch (1914) and Luther (1914) and reviewed more recently by
Save-Soderbergh ( 1945). Additional dissection in the course of this study has
confirmed details and provided a tangible basis for comparison with Paleozoic
amphibians.
Fundamental differences in the anuran and urodele pattern can be seen from
the following descriptions (Figs 18-24).
The terms primitive and advanced or specialized are used in this description as
they apply to the pattern of the adductor jaw muscles and are not to be
considered as reflecting general taxonomic position of the genera. The term
primitive is used for the condition considered closest to that prevailing in small
Paleozoic amphibians in which the jaw musculature was entirely confined to the
inside of a continuous dermal skull roof. Fenestration of the skull roof was
certainly a fundamental feature of the origin of urodeles, whatever their
relationship to frogs. Hynobiids, ambystomatids and primitive salamandrids
retain a relatively primitive pattern of the adductor jaw muscles with a low degree
of differentiation of separate heads within each of three major muscle units.
Specialization or advancement in the adductor jaw musculature is measured by
the degree to which the muscles have extended beyond the confines of the
original dermal skull roof. The aquatic, and variably neotenic families,
Cryptobranchidae, Proteidae, Amphiumidae and Sirenidae have much modified
the general pattern of the skull roof and the adductor jaw muscles are much
specialized.
Adductor j a w muscles of urodeles
Adductor mandibulae externus
This muscle is always large in urodeles. It typically originates from the anterior
surfaces of the squamosal and quadrate (Hynobius, Ambystoma). In larger, aquatic
forms, its origin has migrated posteriorly and dorsally to attach to the dorsal
fascia of the depressor mandibulae (Cryptobranchus), the prootic and parietal
22
K. L. CARROLL AND R. HOLMES
Figure 18. Patterns ofjaw musculature of a representative salamander (A),Ambytoma muculdum, and a
trog (B) A J C U ~ ~Iruei.
U J These patterns are little modified in common representatives of major groups
within each order. Ranids have a small MAME originatingo n the squamosal and tympanic ring, but
this muscle is absent in most anurans.
(Necturus, Amphiuma) and even to the fascia of the epaxial trunk musculature
(Siren). The adductor mandibulae externus is a single muscle in Hynobius and
Ambystoma. In forms with more specialized skulls, it often forms two heads
(Cryptobranchus), or even three heads (Necturus), which have adjacent points of
origin. The adductor mandibulae externus inserts on the dorsal and/or lateral
surface of the lower jaw. In Hynobius and Ambystoma, the insertions are fleshy. This
may be a primitive feature, but could also be related to small size. In the more
derived (and larger) urodeles, the anterior part of the muscle usually inserts by a
tendon (Amphiuma. Necturus). The muscle is clearly pinnate in Siren.
Adductor mandibulae posterior
Unlike the condition in anurans (see below), the adductor mandibulae
posterior of urodeles is a relatively small, usually poorly differentiated muscle
ANCESTRY OF SALAMANDERS
23
........
..
,
Figure 19. Pattern of the adductor jaw muscles in Hynobius naeuius. The quadrato-maxillaly ligament
is a feature in common with other salamanders but is omitted trom the subsequent drawings to show
better the area of muscle insertions. Areas of muscle insertion on lower jaw shown in dorsal view.
MAMI
N A M E (Pro)
Figure 20. Adductor jaw musculature of Crypfobranchus aflegheniensis.All of the major muscles masses
are enlarged and subdivided relative to the primitive condition. The MAME is very large and
subdivided. The MAMI (sup post) attaches by a long tendon.
24
R. L. CARROLL A N D R. HOLMES
Figure 2 I . The adductor jaw musculature in the salamandrid Notophthalmus viridescms. Despite the
bony connection between the frontal and squamosal, the configuration of the muscles remains
siniilar to that of' the hynobiids. Two divisions of the MAMP can be recognized.
mass. Luther (1914) identified three heads in many urodeles and homologized
them with the subexternus, longus and articularis heads of the adductor
mandibulae posterior of anurans. Dissections suggest the existence of these three
heads in Cvptobranchus, Siren, Amphiuma and Necturus, although identification is
sometimes questionable. The adductor mandibulae posterior is not clearly
divided in Hynobius retardatus. In Hynobius naevius, there is a clearly defined head
inserting on the articular and more diffuse fibers inserting into the Meckelian
fossa. All heads originate from the squamosal and quadrate, medial to the origin
of the adductor mandibulae externus. Where it can be differentiated, the
subexternus head is the most lateral, and inserts on the coronoid process and/or
Figure 22. The adductor jaw musculature of Nectuuncr maculosur. This species shows extensive
development of tendons from the MAME and MAMI (sup).The MAME has several discrete heads.
ANCSI'KY OF SALAMANDERS
25
Figure 2% Adductor jaw musculature of Amphiurn tridactylurn. The MAMI is much specialized in its
posterior extent with only the long tendinous section within the area of the original adductor
chamber. The MAMI (pro) is far expanded posteriorly. The MAMP is readily divisible into three units.
articular bone. The longus head inserts on the tendon of the pseudotemporalis
except in Amphiuma, where it inserts directly on the jaw. This head appears to be
absent in Ambystoma. The articularis head is the most medial, usually inserting on
the medial surface of the articular, just anterior to the jaw joint. In Necturus, the
articularis head is either absent or has fused with the subexternus head.
Although these muscles are undoubtedly derived from the adductor
mandibulae posterior mass, their degree of differentiation and points of
attachment are obviously quite variable, and raise serious questions as to their
homologies not only between urodeles and anurans, but also among urodeles.
Save-Soderbergh (1945) believed that only the homology of the articularis head
was reasonably certain.
Adductor mandibulae internus
In urodeles, the massive adductor mandibulae internus is divided into
pseudotemporalis and pterygoideus portions. The pseudotemporalis is further
subdivided into a superficialis ( 'temporalis'), and a profundus head. The
superficialis head originates from the dorsal surface of the parietal and prootic
bones in Hynobius and Ambystoma. In Cryptobrunchw, the origin spreads farther
posteriorly to include the fascia of the epaxial muscles as well. In Amphiuma the
origin from the skull bones has been abandoned completely in favor of
attachment sites on the spines of the cervical vertebrae. In all forms, the muscle
passes anteroventrally and inserts by a tendon onto the dorsal rim of the
coronoid process.
The extent of the pseudotemporalis superficialis tendon is variable. In Hynobius
and Ambystoma, the tendon is very short in order to maintain sufficient muscle
tibre length. In Cryptobrunchus and Necturus, in which the bulk of the muscle
origin is posterior to the skull, the tendon is longer, and in Amphiuma the entire
muscle is located posterior to the skull. The tendon arises from the muscle at the
level of the occiput and passes over the top of the skull in pulley fashion to its
K. L. CARROLL AND R. HOLMES
26
MAMI
MAME
MAMP
(sub ex
Figure 24. Adductorjaw musculature of Siren lacertinu. This enus shows the least posterior expansion
of' the MAMI (sup), with the MAME occupying much of X e otic capsule. The MAMI (pt) IS much
elaborated, tunctionally approaching the condition seen in reptiles, in which it wraps around
the lowerjaw. .The MAMI extends far forward.
insertion on the coronoid. This posterior migration of the pseudotemporalis
superficialis and concurrent replacement by a tendon in the temporal region of
derived urodeles apparently provided extra room for the expansion of other jaw
muscles. In Amphiumu, this extra space is occupied by a large pseudotemporalis
profundus, whereas in Crypobrunchus an anterior head of the superficialis
division has developed to fill the space. One exception is Siren. Although this
animal is highly specialized in many ways, the pseudotemporalis superficialis is
small and takes its origin from the skull roof only. The small size of the
pseudotemporalis mass is probably correlated with the presence of a large
pterygoideus and the spread of the origin of the adductor mandibulae externus
onto the skull roof.
The seudotemporalis profundus of urodeles originates from the dorsolateral
edge o the frontals and parietals, anterior to the origin of the superficialis head.
In small forms with relatively large eyes (Hynobiw,Ambystoma and salamandrids),
f)
A N C t S I X Y OE SALAMANDERS
21
the origin does not extend farther anteriorly than the back of the eye capsule. In
larger urodeles, such as Cryptobranchus and Siren, the origin of the
pseudo temporalis profundus has extended anteriorly, medial to the relatively
small eye capsule. The muscle is large and is often subdivided (Amphiuma,
Necturus). The insertion of the pseudotemporalis profundus is variable. In
Ambystoma and Siren it is on the medial surface of the superficialis tendon, and in
Hynobius on the dorsomedial surface of the jaw. In Necturus, Crytobranchus and
Amphiuma the muscle extends into a tendon, which inserts independent of the
superficialis head on the medial surface of the jaw near the insertion of the
pterygoideus. In Necturus the muscle is divided into two heads. The posterior
head inserts on the medial surface of' the superficialis tendon. The anterior head
forms its own tendon, which passes ventrally to insert on the medial surface of
the jaw.
In Hynobius, a separate pterygoideus could not be identified. In Ambystoma it is
usually poorly differentiated from the pseudotemporalis profundus, originating
with it from the lateral exposure of the frontal and parietal. It inserts by a tendon
on the dorsomedial surface of the jaw ramus, posterior to the pseudotemporalis.
In urodeles with more specialized skulls, the separation of the pterygoideus is
accomplished by a ventral migration of the muscle origin away from the
pseudotemporalis profundus. In Amphiuma, the muscle has migrated ventrally,
but still originates from the frontal and parietal. In Cryptobranchus, internal fibres
have gained attachment to the pterygoid, although the bulk of the fibres still
attach to the frontal and parietal. In Siren and Necturus the transfer of attachment
to the pterygoid is complete. As the origin of the pterygoideus migrates ventrally,
the insertion also migrates ventrally from its primitive position on the
dorsomedial surface of the jaw to a position on the ventromedial surface of the
ramus. In Siren, the muscle has moved below the jaw and developed ventral and
lateral to the ramus in a manner analogous to that ofreptiles.
Adductorjaw muscles of anurans
Adductor mandibulae externus
The adductor mandibulae externus of anurans never attains the size or
importance that it has in urodeles, and it is usually absent. In Rana it is of
moderate size, taking its origin from the ventral surface of the tympanic ring and
from the zygomatic process of the squamosal. It passes medial to the maxilla and
inserts on the lateral surface of the jaw. In Ascaphus (Fig. 18) and Xenopus, as in most
anurans, the muscle is absent.
Adductor mandibulae posterior
The muscles belonging to the adductor mandibulae posterior group are the
most important jaw adductors of anurans. There are at least three heads: the
subexternus, longus and articularis. Save-Soderbergh ( 1945)recognized a fourth
head, the adductor mandibulae posterior lateralis, originating from the medial
and ventral surfaces of the quadratojugal and from the lateral surface of the
quadrate and squamosal, and inserting on the lateral surface of the jaw. The
subexternus head originates from the medial surface of the squamosal near the
base of the zygomatic process (Ascaphus, Xenopus), and from the ventral portion
o f the tympanic ring (Rana) where a tympanum is present. I t inserts on the lateral
28
K. L. CARROLL AND R. HOLMES
surface of the jaw medial to the lateralis head. The articularis head originates
from the ventral parts of the anterior surface of the squamosal and adjacent parts
of the quadrate. It passes ventromedially to insert on the inner surface of the jaw.
The longus head (temporalis) is the largest head of the adductor mandibulae
posterior and is analogous to the pseudotemporalis superficialis of urodeles. The
muscle has migrated onto the skull roof, where it takes its origin from the dorsal
surface of the otic capsule and passes anteroventrally to insert on the coronoid
process of the lower jaw.
Adductor mandibulae internus
The adductor mandibulae internus is much less well developed in anurans
than in urodeles. It is represented by a single, moderate-sized muscle originating
from the dorsolateral edge of the frontoparietal and passing ventrally and
slightly posteriorly to insert by a long tendon on the ventromedial surface of the
jaw (Rana, Ascaphus). In Xenophus, the muscle is larger than in most other
anurans, and inserts on the dorsomedial rim of the jaw rather than on its
ventromedial surface. Luther (1914) homologized this muscle with the
pterygoideus of urodeles. However, Save-Soderbergh ( 1945) suggested that it
would be more correctly homologized with the urodele pseudotemporalis. In all
anurans the ‘pterygoideus’ originates from the lateral edge of the frontoparietal,
much like the pseudotemporalis of urodeles, never from the pterygoid. In some
anurans, it inserts on the dorsomedial edge of the jaw, as does the
pseudotemporalis of urodeles. Although the ‘pterygoideus’ of anurans
sometimes inserts on the medial surface of the jaw (Rana), much like the urodele
pterygoideus, it must be remembered that in some urodeles (e.g., Necturus,
Cryptobranchus, Amphauma), slips of the pseudotemporalis profundus insert in
exactly the same manner. The ‘pterygoideus’ of anurans clearly cannot be
homologized specifically with either the pseudotemporalis or the pterygoideus of
urodeles.
Beyond the minor variations seen within both groups, there are consistent
major differences between the patterns of the adductor jaw musculature in frogs
and salamanders. The adductor mandibulae externus is one of the major jaw
muscles in salamanders, but is small or, more commonly, totally absent in frogs.
Both orders have a major muscle originating from the otic capsule. In frogs this
is the longus head of the adductor mandibulae posterior (a muscle only
questionably recognizable in salamanders), while in salamanders it is the
adductor mandibulae internus superficialis. The distinctive patterns of the jaw
musculature in frogs and salamanders could have evolved independently from a
more primitive condition, but neither specialized pattern is likely to have evolved
from the other.
Adductorjaw musculature in Paleozoic amphibians
It is important now to consider what atterns of jaw musculature might have
been present in the groups suggestecf to be ancestral to living frogs and
salamanders. Because of the extensive ossification of the skull and braincase, the
configuration of the adductor chamber in Paleozoic tetrapods is relatively
circumscribed. Together with the known position of the prootic foramen, the
epipterygoid and the configuration of the Meckelian fossa, one can make a
ANCESTRY OF SALAMANDERS
29
plausible reconstruction of a primitive condition, assuming that all three major
divisions had the same relative position as in living amphibians.
We will begin with the primitive labyrinthodont amphibian Dendrerpeton
(Carroll, 1967) because of its relatively small size and conservative proportions
from which one might derive the skull pattern of either frogs or salamanders
(Fig. 2 5 ) . The origin of the adductor mandibulae internus would have been
limited anteriorly by the margin of the orbit and the lateral extent of the
braincase, and posteriorly by the epipterygoid and prootic region of the
braincase. The insertion was limited by the area available for its passage through
the subtemporal fenestra, medial to the adductor mandibulae externus and the
lower jaw. Save-Soderbergh ( 1945) recognized both a superficial and a profundus
head in Triassic labyrinthodonts, but there is no evidence for this division in
Dendrerpeton. The fibres would have been inclined posteroventrally.
The adductor mandibulae externus is limited anteriorly by the margin of the
subtemporal fenestra and the posterior end of the tooth row, laterally by the
cheek and the limited space of insertion at the margin of the lower jaw. I t would
have originated on the upper cheek region between the orbit and the otic notch.
In Dendrerpeton, serrations on the coronoid suggest a posterodorsal orientation
of the deeper fibres and so a limit of their origin to the more posterior portion of
the cheek. More superficial fibres may have had an origin closer to the orbit.
Medially, the extent of the adductor mandibulae externus was limited by the size
of the adductor mandibulae posterior.
The adductor mandibulae posterior would have been limited posteriorly by
the slope of the otic notch, medially by the quadrate ramus of the pterygoid,
laterally by the extent of the adductor mandibulae externus and anteriorly by the
adductor mandibulae internus. It seems probable that its origin was primarily
determined by the dorsal extent of the quadrate ramus of the pterygoid.
Insertion would have been into the Meckelian fossa.
The relative importance of the three muscles cannot be exactly determined,
and they are restored on the basis of their typical areas of origin and insertion in
living lower tetrapods. It is expected that this general pattern could have been
ancestral to that of either frogs or salamanders, but we see little evidence of the
specific features of either. A Dendrerpeton-like animal has been considered in
recent years as an ultimate ancestor for both orders. This genus is certainly not a
lissamphibian, however, and in fact tells us little of the probable immediate
ancestor(s1 of living amphibians. From Dendrerpeton, we will shift to consideration of a suggested immediate lissamphibian ancestor, Doleserpeton (Bolt, 1969,
1977). In contrast to Dendrerpeton, the skull of Doleserpeton (Fig. 26) imposes much
tighter constraints on the muscle pattern. This is primarily because of its small size,
a factor that has been considered as basic to the origin of the lissamphibian skull
pattern. If we look to the area of the jaw musculature, it may be noted that the
cheek is much reduced by the large size of both the orbit and the otic notch,
allometrically adjusted to small skull size. The tooth row extends very far
posteriorly, and the subtemporal fenestra is correspondingly reduced. The lateral
extent of the braincase as a whole, and the anterior extent of the otic capsule is
greater, with the increase in brain size relative to that of the skull. The area
underneath the otic notch is a more or less confined chamber for the adductor
mandibulae posterior. To gain necessary length to allow a large gape, the
anterior fibres may have originated from the underside of the skull roof, passing
n. L.
30
CARROLL
Figure 25. Reconstruction of the adductor jaw musculature in the Carboniferous labyrinthodont
Uendrerpeton.
ANCESTKY OF’ SALAMANDERS
31
MAMP(lonpus1
UAUl I
MAMP
brgurc I b Reconstruction of the adductor law musculature in the Lower Permian labyrinthodont
UukJerpefeton Outline ot braincase, quadrate ramus of pterygoid and epipterygoid restored on the
bd\is ot renomius, allornetrically adjusted to the small skull size.
over the anterior margin of the quadrate ramus of the pterygoid. This suggests
initiation of the longus head of the muscle, typical of frogs. The adductor
rnandibulae internus would be reduced in size from the pattern seen in
Dendrerpeton and its origin restricted by the large size of the orbit. The adductor
mandibulae externus would certainly be restricted in anteroposterior extent by
the wide gape indicated by the great length of the tooth row. If the adductor
rnandibulae posterior occupied most of the area underneath the otic notch, the
adductor mandibulae externus would be limited to a very small cross-section.
The probable anterior extent of its origin cannot be determined. Doleserpeton has
been suggested as an ancestor to all Lissamphibia, but certainly the closest
resemblance of the skull and probable jaw musculature is to frogs.
The earliest known anuran, or anuran ancestor, Triudobatruchus (Fig. 271, has a
similarly small skull, with generally comparable proportions, extent of
subtemporal fenestra, size of otic notch, etc. The major contrast is in the extent of
the skull roof. Here the otic capsules are exposed, and the cheek is open in
typically anuran pattern. The skull roof is limited to a narrow bar above the
braincase. One can restore a typically anuran pattern of jaw musculature. The
adductor mandibulae externus was certainly small or absent, since it has almost
32
K. L. CARROLL A N D R. HOLMES
,*-7-r--._
,CO
'\
1
A
OIiC
notch
B
Figure 27. Skulls of A, Triudobatruchus, an ancestral anuran from the Lower Triassic, after Watson
(1940); B, hypothetical lissamphibian ancestor; left, from Parsons & Williams (1963); right, the
Parsons & Williams model modified to accord more closely with known amphibians from the Lower
Permian.
no place of origin. The longus head of the adductor mandibulae posterior can
now assume an area of origin on the otic capsule. As illustrated by Watson
( 19401, the shape of the pterygoid for accomodation of this muscle is exactly as in
living frogs. It may be assumed that posterior migration of this muscle was
selected to increase its fibre length. Such a movement would only have been
possible subsequent to loss of the bone at the posterodorsal margin of the orbit.
The probable pattern of jaw musculature in Triudobatruchw simply accentuates
that seen in labyrinthodonts with small skull dimensions and a large otic notch.
This reinforces earlier suggestions of the labyrinthodont origin of frogs.
The jaw muscles of urodeles differ consistently from those of anurans in the
large size of the adductor mandibulae externus and the spread of the superficialis
head of the adductor mandibulae internus onto the otic capsule. It seems very
unlikely that such a shift would have occurred from the well-defined anuran
condition, in which the longus head of the adductor mandibulae posterior
originates on the otic capsule.
As pointed out by Save-Soderbergh ( 19451, the spread of muscle origins onto
the otic capsule in frogs and salamanders could not have preceded fenestration
of the skull. Presumably this fenestration was associated with the spread of
muscles out of the previously restricted adductor chamber. The fact that the otic
33
ANCESI'KY OF SALAMANDERS
P
art
MAMI
MAMI
I
Figure 28. Reconstruction of the adductor jaw musculature in the Lower Permian microsaur Hapdopareton. Heavy dashed line indicates probable anterior margin of the quadrate ramus of the
p terygoid.
capsule is occupied by the longus head of the adductor mandibulae posterior in
frogs, and the superficialis head of the adductor mandibulae internus in
salamanders, suggests that fenestration occurred separately in the ancestors of
the two orders, each of which had previously developed a different distribution
of the adductor jaw muscles. At the initiation of fenestration, we can presume
that the longus head of the adductor mandibulae in frogs had already extended
dorsally to the skull roof, so that it could spread onto the otic capsule as the
dermal skull roof was reduced.
This reasoning makes the presence of a common lissamphibian ancestor with a
much reduced skull (Fig. 27B), as envisaged by Parsons & Williams (1963), very
unlikely.
On the basis of the jaw musculature, it is possible to conceive of a more
primitive labyrinthodont ancestor, such as Dendrerpeton, having given rise to
salamanders as well as frogs. One must then assume that the otic notch is lost in
the line leading to urodeles, and accentuated in the line leading to frogs. Subsequently, the urodele ancestor would have developed an emarginated cheek and
emphasized the adductor mandibulae externus, while the adductor mandibulae
posterior diminished in importance.
There is, however, no evidence among known labyrinthodonts of the initiation
of such salamander features as an emarginated cheek, or modification of the otic
capsule and middle ear region. All these features are encountered among the
microsaurs. Relationship to salamanders is also supported to some degree by the
probable distribution of the adductor jaw musculature in microsaurs. The
3
34
R. L. CARROLL AND R. HOLMES
emarginated cheek in modern salamanders can be associated with the large size
of the adductor mandibulae externus in all genera. A similar emargination of the
cheek in such microsaurs as the ostodolepids and Hapsidopareion and Llistrofus
also suggests a large adductor mandibulae externus. The supposition that this
muscle is large in microsaurs is supported by the condition in other genera in
which the cheek is not emarginated. The gymnarthrids (Fig. 13) have a solid
cheek, but the posterior lateral surface of the dentary is recessed, in a manner
resembling that of many mammals. In mammals, the recess is for the masseter
muscle, but in microsaurs the adductor mandibulae externus would have
inserted in this area. If we are to attempt to reconstruct the remainder of the jaw
musculature in the genus Hapsidopareion (Fig. 28) the absence of an otic notch
provides more room posteriorly than in labyrinthodonts for the origin of the
adductor mandibulae posterior, lateral to the otic capsule, where the muscle is
separated from the braincase by the quadrate ramus of the pterygoid. The muscle
fibres are shorter because of the low profile of the skull. The adductor
rnandibulae internus would have occupied essentially the same position as in
labyrinthodonts.
If salamanders did evolve from microsaurs such as Hapsidopareion or other
Paleozoic lepospondyls with a similar skull morphology, it would indicate that
fenestration of the cheek in the ancestry of salamanders occurred by embayment
of the lower margin. Such an emargination was presumably selected in
microsaurs to accommodate the large adductor mandibulae externus that came to’
insert on the lateral margin of the lower jaw. It may be assumed that fenestration
of the cheek in frogs occurred without interruption of the margin of the skull
since most genera retain the quadratojugal and the maxilla has a bony
attachment to the suspensorium.
One may suppose that the immediate ancestors of salamanders enlarged the
orbital openings to an extent equivalent to that seen in ancestral frogs.
Differences in skull configuration, particularly the lack of an otic notch and lesser
importance of the adductor mandibulae posterior, presumably account for the
dominance of different muscles that were to spread over the otic capsule. If the
orbit in microsaurs were to expand posteriorly and medially the first muscle to
be exposed would be the superficialis head of the adductor mandibulae internus.
This muscle could then take origin on the orbital margin, later extend onto the
skull roof, and subsequently migrate posteriorly with the receding margin until
the otic capsule was encountered. It would bypass the profundus head of the
internus and pass medial to the origin of the adductor mandibulae posterior.
Such a posterior migration of the adductor mandibulae internus is seen during
development in Hynobius (Fox, 1959) (Fig. 29).
On the basis of skull morphology of known Paleozoic amphibians one can
most simply envisage the specialized aspects of the skull and adductor jaw
musculature in frogs and salamanders as having evolved separately. That of frogs
evolved from labyrinthodonts, with an otic notch and an unbroken palatal
margin, and that of salamanders from microsaurs without a notch, but with a
gap in the cheek between the maxilla and squamosal.
PEDICELLATE TEETH
Parsons 8c Williams t 1963) cited the presence of pedicellate teeth in nearly all
living amphibians as strong evidence for a common ancestry for the three orders.
ANCES’I nY O F SALAMANDERS
35
Figure 29. Posterior shift of the origin of the superficial head of the adductor mandibular internus of
Hynobzus nebulosus during embryological development, from Fox (1959);A, 14 mm stage; B, 1 7 mm
stage; C, 3 2 mm stage. Skull drawn to aconsistent size to facilitatecomparison.
If salamanders evolved from microsaurs and frogs from temnospondyls, it must
be assumed that the character evolved separately in the ancestors of the modern
orders. Larsen & Guthrie (1975)provide a plausible explanation for the function
of pedicellate teeth in terrestrial salamanders that would also apply for frogs.
They point out a strong association between pedicellate teeth, bicuspid crowns
and manipulation of prey by the tongue. The biscuspid tip of the crown is to
prevent the prey being impaled by the tooth. If it is impaled, and so rendered less
capable of manipulation by the tongue, the crown can be readily broken off. The
teeth are intended to hold the prey while the tongue is manoeuvred, but not to
pierce or slash.
Regal & Gans (1976) have pointed out that tongue protrusion is based on an
entirely different mechanism in frogs and salamanders. Since the function of
pedicellate teeth in salamanders is apparently closely associated with tongue
manipulation, it would not be unreasonable for both features to have evolved independently in frogs and salamanders, as did tongue protrusion.
The fossil record of salamanders is very incomplete during the Mesozoic, and
only at the very end of the Cretaceous are any of the living families represented.
It may be significant, nevertheless, that few of the salamanders known from the
Mesozoic show pedicellate teeth, although the dentition is clearly evident in a
number of genera:
Prosirenidae
Prosiren elinorae (Estes, 1969b, fig. 2)
Prodesmodon copei (Estes, 1964, figs 43, 44)
Sirenidae
Habrosaurus dilatus (Estes, 1964, figs 35,361
Only non-pedicellate teeth are known in the two extinct salamander families
Prosirenidae (Estes & Hoffstetter, 1976 ; Estes, 1969a) and Batrachosauroididae
(Hinderstein & Boyce, 197 7). Within the family Sirenidae, only Pseudobranchus
striatus has any evidence of a zone of weakness, and Means (1972) questioned
whether it is homologous with that of other urodeles. A zone of weakness is also
poorly expressed in living proteids (Larsen & Guthrie, 1974). The teeth of the
Paleocene species of the proteoid Opisthotriton kuyi are described as pedicellate
(Estes, 1975: 369) but the Upper Cretaceous members of the same species (Estes,
1964) do not show a clearly defined division between the crown and base, but
have a weakly-developed “zone of weakness”.
The generally poor development of pedicelly in sirenids and proteids may be
attributed to their neotenic nature. The configuration of the skull of the Miocene
36
K. L. CARROLL AND R. HOLMES
prosirenid Albaner-eton (Fig. 12) is not at all what one would expect in a neotenic
form however, but resembles in its general appearance primitive terrestrial
salamanders. A further genus, from the Lower Cretaceous, Hylaeobatrachus, which
is neotenic but of uncertain taxonomic affinities, does exhibit pedicellate teeth
(Estes, pers. comm.).
The fossil record is very incomplete and biased toward the preservation of
aquatic salamanders, but does not contradict an interpretation that pedicellate
teeth evolved within the urodeles. The absence of pedicellate teeth in microsaurs
is not a sufficient reason, by itself, to rule out this group as possible urodele
ancestors.
CONCLUSIONS
Evidence of the skull and adductor jaw musculature indicates that the
ancestors of frogs and salamanders are probably represented by different groups
of Paleozoic amphibians. Many of the features expected in a frog ancestor are
initiated in the labyrinthodonts, and several significant features expected in
salamander ancestors are seen among the microsaurs. Although microsaurs as a
group exhibit features expected in salamander progenitors, no currently known
microsaur can be specifically cited as a plausible ancestor. Emargination of the
cheek and/or presence of a fossa o n the lateral surface of the dentary in three
families, and the absence of an otic notch in all genera, indicate the presence of
an essentially salamander-like distribution of the adductor jaw muscles
throughout the group. Skull proportions, dentition and configuration of the
braincase are variable among the microsaur families, and none have all of these
features in the combination expected in the ancestors of salamanders. An animal
with all these attributes could, however, be readily accommodated within the
concept of the order Microsauria. Of the known genera, members of the family
Hapsidopareiontidae exhibit the most salamander-like pattern of skull roof and
denti tion.
The origin of frogs from labyrinthodonts, and salamanders from microsaurs,
implies that most of the features that are used to characterize the modern groups
have risen independently. The general pattern of the cranial fenestration may be
presumed to have evolved in relationship to small size, achieved separately in the
ancestors of the two groups. The evolution of pedicellate teeth can be seen as
associated with tongue feeding out of the water. The strikingly different pattern of
tongue protrusion in the two groups raises questions as to the validity of the
assumption that pedicellate teeth were present in a common ancestor.
Unfortunately, the time of divergence of the ancestral groups is still difficult to
specify. Microsaurs are fully distinct from labyrinthodonts in the early
Pennsylvanian. 0ther lepospondyl amphibians are known in the Mississippian,
but there is no evidence that lepospondyls are a natural group. Microsaurs might
have differentiated from primitive labyrinthodonts any time from the Upper
Devonian to the earliest Pennsylvanian. This suggests a time of original
divergence of the ancestors of frogs and salamanders between 310 and 340
million years ago. Such a common ancestor would not be expected to have any of
the specific features we associate with Lissamphibia. Such evidence as the fossil
record provides suggests specialization toward the patterns recognized as typical
of small labyrinthodonts in the ancestors of frogs and toward microsaurs in the
ANCLS 1 KY Ob SALAMANDERS
37
ancestors of salamanders, followed by further size reduction, and specialization
toward feeding on small prey, such as insects, out of the water. Specifically
lissamphibian characteristics presumably began to evolve separately in both
lineages during the Permian.
ADDENDUM
Since this paper was accepted for ublication, descriptions of a complete
skeleton of an Upper Jurassic salaman er and a tiny larval salamander from the
Upper Triassic of Russia have appeared (Ivakhnenko, 1978).
The Triassic larva, Trium.~nw,shows little anatomical detail, but demonstrates the
presence of a typical urodele suspensorium consisting of the squamosal, quadrate
and pterygoid, a gap in the jaw margin between the maxilla and the quadrate and
an anterior position of the jaw articulation.
Karaurus is known from an almost complete, beautifully preserved skeleton. The
skull is iininediately recognizable as that of a urodele, with only a few primitive
features. Ivakhnenko recognizes it as a member of a new family within the
Cryptobranchoidei. It has a short trunk, moderately well developed limbs and a
transversely oriented vomerine tooth row comparable with that of some
hynobiids and most ambystomatids. Regal ( 1 966) associated this pattern of the
palatal dentition with terrestrial as opposed to aquatic feeding. The configuration
ot’ the pterygoid resembles much more closely that of hynobiids and
aiiibystomatids than that of known cryptobranchids. The articulation of the base
ot’ the pterygoid with the braincase appears to be somewhat more primitive than
that of other salamanders, and to resemble that of Paleozoic amphibians,
including inicrosaurs (Fig. 15). Other primitive features include the sculpturing
and great extent of the dermal bones of the skull roof.
rlie configuration of the dermal skull roof provides some indication of the
pattern of the jaw musculature. The remainder of the skull is so like that of
coiiservative living salamanders that there is no reason to deny a basically similar
distribution of the jaw musculature. The orbits are small, and behind them the
temporal opening extends medially toward the midline. The posterodorsal
iiiargin of the skull retains its dermal ornamentation, extending out over the top of
the squamosal in the area of the tabular bone in microsaurs. Clearly, the
superficialis head of the adductor mandibulae internus was already an important
muscle in Kuraurus, but its area oforigin had only begun its incursion onto the
surface of the braincase.
These specimens further demonstrate the early achievement of the typical
urodele cranial pattern and provide further evidence of the evolution of
salamanders from a group of Paleozoic amphibians distinct from the immediate
ancestors of‘frogs.
B
ACKNOWLEDGEMENTS
We thank the Reptile section, British Museum (Natural History) for the
opportunity to study skulls of a variety of salamanders which provided the
impetus for this work. Dr J.-P. Gasc, Laboratoire d’Anatomie comparke du
Muskum National d’Histoire Naturelle, Paris, made available hynobiid material
for dissection. Mr Franqois Gendron, then a student at McGill, collected
salamanders that were exchanged with Dr Erhard Paul, Berlin, for a hynobiid in
R. L. CARROLL AND R. HOLMES
38
the collection of the Humboldt University. Other hynobiid material was
borrowed from the California Academy of Sciences. Most of the drawings of
skulls and jaw musculature were made by Mrs Betsy Holland. We thank her for
this major contribution. Drs John Bolt, David Wake and Richard Estes read early
drafts of this paper. We thank them for their useful criticism. This work was
supported by grants from the National Research Council of Canada.
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K. L. CARROLL A N D R. HOLMES
40
ABBREVIATIONS USED I N FIGURES
a
ao
art
ba
bo
car 1.
co
d
ec1
eo
co-op
ePt
I'
lo
1-p
it
1
Id
111
11
01'
OP-CCJ
op-pro
oper
opis
ot-oc
P
pal
pal-pt
part
Po
PP
angular
accessory ear ossicle found in several
inicrosaurs
articular
basicranial articulation
basioccipital
carotid foramen
coronoid
dentary
ectopterygoid
exoccipital
fused exoccipital and opisthotic
epipterygoid
frontal
fenestra ovalis
frontoparietal
intertemporal
lacrimal
lacrimal duct
maxilla
nasal
opercular fenestra
fused opisthotic and exoccipital
fused opisthotic and prootic
operculuin
opisthotic
otic-occipital, representing fusion of
prootic, opisthotic and exoccipital
parietal
palatine
palatopterygoid
prearticular
postorbital
postparietal
'
tymi dii
V
IJLV,
VII, VIII,
Xand XI1
v,, v,, v,
pdlpebral cup
preinaxilla
prefiontal
prootic (in salamanders including
basisphenoid ossification of Paleozoic
amphibians)
parasp henoid
quadrate
quadrate ramus ofpterygoid
quadratojugal
quadrato-maxillary ligament
surangular
septoinaxilla
supraoccipital
sp henethmoid
squamosal
ligament connecting squamosal and
ceratoh yal
supratemporal
stapes
stapedial process ofsquamosal
ligament connectingstapesand
squamosal
ligament connecting stapes and
quadrate
ridge of bone presumed to have
supported margin 01 tympanum
tympanic annulus
voiner
foramina for cranial nerves
branches of the Vth nerve
ABBREVIATIONS USED FOR MUSCLES
DM
MAME
MAME 1,11.&111
MAME (pro)
MAME (sup)
MAM I
MAMI (pro)
MAMI (pro)I I,
deoressor mandibulae
adductor mandibulae externus
divisions of MAME
deep head of MAME
superficial head of MAME
adductor mandibulae internus
profundus head of MAMI
divisions of profundus head of
MAMI
MAMI (SUO)
MAMI (SU; ant)
MAMI (sup post)
MAMI ipt)
MAMP
MAMP (art)
MAMP (]at)
MAMP (longus)
MAMP(subex)
suoerticialis head of MAMI
aGerior head of superficialis
posterior head of superficialis
pterygoideus head of MAMI
adductor mandibulae posterior
articularis head o f M A M P
lateralis head of MAMP
longus head of MAMP
subexternushead of MAMP