JOURNAL OF MORPHOLOGY 188:315-326 (1986)
Ontogeny of Cranial Ossification in the Eastern Newt,
~ o ~ o p h ~ h aviridescens
/~us
(Caudata: Salamandridae), and Its
Relationship to Metamorphosis and Neoteny
STEPHEN M. REILLY
Department of Zoology, Southern Illinois University, Carbondale, Illinois
62901
ABSTRACT The ontogenetic sequence of cranial osteogenesis through
adulthood is described in samples of newts from completely metamorphosing
and partially neotenic populations. Cranial ossification proceeds in the same
sequence in both samples. Seven stages of cranial development are described
on the basis of conspicuous events that occur during ontogeny. These include
four larval stages, metamorphs, efts, and adults. Neotenic adults have skulls
that are metamorphosed completely and indistinguishable from the skulls of
non-neotenic adults. Neoteny in these newts does not involve the skull and is
limited to the postmetamorphic retention of some gill structures and, thus, is
termed "limited neoteny." The evolution of limited neoteny in newts as a
correlated response to the inhibition of land-drive behavior is discussed.
Adult cranial osteology has played an important role in the classification of salamanders (notably, Cope, 1889; Dunn, '26; Noble,
'31; Regal, '66; Tihen, '58; Wake, '66; Wake
and Ozeti, '69). Many previous studies have
detailed aspects of cranial structure and ontogeny, and related them to ecological specializations and metamorphosis (Fox, '54;
Monath, '65; Papendieck, '54; Parker and
Dunn, '64; Regal, '66; Srinivasachar, '62;
Worthington and Wake, '71; and references
therein). Because neoteny (Pierce and Smith,
'79) occurs in all families of urodeles (Porter,
'721, meaningful comparisons of adult cranial
structures are sometimes difficult to achieve.
Likewise, because of differences in larval ontogeny, comparisons of larval cranial structures are also difficult to use (Larsen, '63).
Comparisons of complete ontogenetic sequences can provide a better basis from
which to group salamander taxa and to interpret the ontogenetic details of neoteny and
metamorphosis that are needed to support
theoretic models relating ontogeny to ph;-Lgeny (Alberch et al., '79; Alberch, '85; Fink,
'82). Nevertheless, whole sequences of skull
development have been described for only
seven species of salamanders (Salamandra
salamandra, Stadtmuller, '24; Eurycea bislineata, Wilder, '25; Triturus vulgaris, Erdmann, '33; Ambystoma mexicanum, Keller,
'46; Ambystoma texanum, Bonebrake and
Brandon, '71; Rhyacotriton olympicus, Wor-
0 1986 ALAN R. LISS. INC.
thington and Wake, '71; and Aneides lugub
ris, Wake et al., '83).
A description is presented here of the ontogenetic sequence of cranial ossification,
through adulthood, in two populations of the
eastern newt, Notophthalmus viridescens,
one of which is neotenic.
The salamander genus Notophthalmus is
one of two genera of the family Salamandridae in the Nearctic Region. The eastern newt,
N. uiridescens, is the most widely distributed
of the three species in the genus. It occurs
throughout the eastern half of North America in a variety of habitats in which it displays alternative life history strategies
(Gage, 1891; Pope, '24, '28; Noble, '26, '29;
Bishop, '41; Healy, '70, '73, '74; Conant, '75).
The normal life cycle of N. viridescens involves aquatic eggs, aquatic larvae, a terrestrial juvenile (eft) stage of variable duration
and a largely aquatic adulthood. In some
areas the eft stage frequently is bypassed
through neoteny (Mecham, '67). Comparison
of the ontogenetic sequences of craniogenesis
in normal and neotenic populations will provide details on the relationship between neoteny and metamorphosis and on the
functional and adaptive significance of neoteny in newts.
MATERIALS AND METHODS
A total of 206 specimens of Notophthalmus
viridescens, representing two subspecies, was
316
S.M. REILLY
examined. A series of 137 N. v. louisianensis
at various developmental stages was collected during August 1983 to July 1984 from
McGuire's Pond, 9.7 km south of Carbondale,
Jackson Co., Illinois. Branchiate adults occur
in this population (Brandon and Bremer, '66;
Albert, '67) and comprised 68% of the adults
at the time of collection. Another 10 larvae
(September 1973), presumed to be neotenic
juveniles on the basis of size and degree of
branchiation, and an additional five branchiate adults (collected from November 1966
to July 1967) were examined from the same
locality. For comparison, a series of N. u.
viridescens containing 39 larvae (July 19661,
10 emergent efts (August 1975), and four
larger efts (June, 1983)was examined from a
population in which neoteny does not occur
(Chadwick, '44, '50) at Lake Ravenel and
vicinity, Highlands Biological Station, Macon Co., North Carolina. Numbers of specimens representing each stage of development
are indicated in Table 1.The ontogeny of the
hyobranchial apparatus will be described in
a separate paper.
All specimens were killed in 10% ethanol
or chloretone and fixed in 10%formalin. Sex
and snout-vent lengths were recorded before
the specimens were cleared and doublestained by the bone-cartilage staining procedure of Hanken and Wassersug ('81). Skulls
were examined under a binocular dissecting
microscope at a magnification of x 10 to x 25
and drawn with the aid of a camera lucida.
Voucher specimens are deposited in the Museum of Natural History, University of Ransas (KU 203905-203988).
RESULTS
Seven developmental stages are defined on
the basis of conspicuous developmental
events during cranial ontogeny (Table 1).All
cranial bones are paired except the parasphenoid and premaxilla, and are bilaterally
symmetrical until the Eft Stage. Slight
asymmetry in the paired bones and irregular
suture lines develops after metamorphosis.
Cranial ossification proceeds in the same sequence in newts from both geographic areas.
Teeth
The first ossification occurs in tooth-bearing elements early in Stage I when yolk is
depleted and the ability to capture food becomes important. Teeth form first on the coronoid. Premaxillary, vomerine, palatine,
and dentary teeth mineralize just before the
respective bones ossify, early in Stage I (Fig.
lA, B), when balancers are still present.
Teeth do not appear on the maxillary bone
until late in the Eft Stage, and then only on
the anterior portion and never on the jugal
extension. Through metamorphosis all teeth
are simple, pedicellate, and sharply pointed.
Late in the Eft Stage, bifid teeth begin to
appear medially on the premaxilla. By adult-
TABLE 1. Stages in cranial ontogeny in Notophthalmus viridescens and samples of specimens examined
N
Specimens examined
SVL' (mm)
(IL,NC)'
Mean
Range
I
14
(14,O)
7.0
5.5-9.0
11
42
(20,22)
12.9
9.0-16.0
Stage
Diagnostic feature of stage
Ossification of coronoids, dentaries, premaxillae,
squamosals, vomers, palatines, and prearticulars
Ossification of frontals, exoccipitals, parietals,
pterygoids, prootics, quadrates, orbitosphenoids,
parasphenoid, and opisthotics
I11
Ossification of opercula, prefrontals, maxillae,
otic capsule, and processes of frontosquamosal arch
Iv
Ossification of the nasals, and completion of the
frontosquamosal arch
MetaPalatine-pyterygoid disintegration; loss of
palatines and coronoids; new jugal process
morphs
on maxillae;
rearrangement of vomerine teeth
Efts
Appearance of bifid teeth, maxillary teeth, and
articular ossifies
Adults
Lengthening and solidification of skull; appearance
of coronoid process on mandible; completion of
'Snout-vent length.
'Specimens from Illinois ( I U and North Carolina (NO.
*Four efts (June 1983 sample) not included in calculation
15
(6,9)
16.5
13.0-20.0
48
(43,5)
22.7
15.0-30.0
8
63)
22.3
18.0-29.0
48
(38, lo)*
24.2
17.0-37.5
26
(26,O)
46.6
39.5-60.0
~
CRANIAL ONTOGENY IN NOTOPHTHALMUS VIRIDESCENS
317
Dentary
hood most teeth are bifid, slightly more expanded, and sharp, and resemble typical
At their appearance in Stage I the dentarhynobiid teeth (Tihen, ’58).
ies are long conspicuousbones with their anterior, terminal knobs approaching the
Coronoid
mental gap (Fig. 1A). No distinction could be
The first bones to stain strongly are the made between dentary and mentomeckelian
coronoids. They appear medial to the dentary elements as has been done in some ambystoand are heavily edentate (Fig. 1A). The CO- matids (Srinivasachar, ’62); thus, it is likely
ronoid remains centered on the dentary, ex- that the mentomeckelian portion is absent in
tending slightly dorsoposteriorly in Stage 11 Notophthalmus as it is in Salamandra (Par(Fig. 2C). Throughout Stages III and IV the ker, 1877). In Stages I1 through 111,the skull
coronoid becomes more elongate and proges- increases in length and the mental gap narsively more narrow, until it disintegrates rows until the dentaries articulate loosely
during metamorphosis (Figs. 3C, 4C).
with each other, and in Stage IV form a posterior mental projection. The posterior end of
the dentary in Stage IV is compressed laterally and bears a blunt terminus. Mediolaterally, the dentary articulates with the
needle-like prearticular for about half of the
length of the dentary. In the Eft Stage the
dentary is long and thick in lateral aspect
(Fig. 5C). In adults, its outer face continues
to thicken, especially posteriorly, forming a
“coronoid process’’ of varying height, and
-Pa more teeth appear (Fig. 6C).
I
A
t
1 mm
!
Fig. 1. Stage I larval skull of Notophthalmus viridescens. Ventral (A) and dorsal (B) aspects.
Vomer
The vomer is the major larval tooth-bearing bone. In Stage I, the vomer lies just anteromedial to the eye in the same plane with
the palatines (Fig. 1B). In Stages I1 through
I11 the vomer is elongated and lies posterior
to the premaxilla and ventrolateral to the
anterior end of the parasphenoid (Figs. 2B,
C, 3B, C). In Stage 11, the vomer is irregularly rectangular with rounded anterior ends
(Fig. 2B) that become more pointed in Stage
111 (Fig. 3B). Teeth cover the entire ventral
surface of the vomer and the posterior edge
of the bone loosely abuts the palatine. In
Stage IV,the posterior edge has an interdigitating articulation with the palatine (Fig.
4B). Elongation continues with an anterior
edentate portion lengthening toward the premaxilla and widening laterally toward the
maxilla. Widening continues through metamorphosis so that each vomer fuses with the
A bbreviatwns
C1, columella; Cp, coronoid process; Cr, coronoid; D, dentary, E, exoccipital; Fr, frontal; FSa, frontosquamosal
arch; M, maxilla; N, nasal; 0, opisthotic ossification;
Or, orbitosphenoid; P, parietal; Pa, prearticular; Pal,
palatine; Pf, prefrontal; Pm, premaxilla; Pm-de, premaxilla-dentigerous ramus; Pm-do, premaxilla-dorsal
ramus; Po, prootic; Ps, parasphenoid; Pt,pterygoid; Q,
quadrate; Sq, squamosal; V, vomer.
318
S.M. REILLY
A
1 mm
H
1 mrn
c------l
6
Pm-de
B
6
E
C
Fig. 2. Stage 11larval skull of Notophthalmus viridescens. Dorsal (A), ventral @), and lateral (C) aspects.
C
Fig. 3. Stage 111 larval skull of Notophthalmus viridescens. Dorsal (A), ventral (B), and lateral (C) aspects.
319
CRANIAL ONTOGENY IN NOTOPHTHALMUS VIRIDESCENS
A
-,
1 mm
Pm-de
--&p
A.
Q
Pal
B
B
tl
E'
1 mm
U
Pm-do
E
\
N,
Pm-de
C
Fig. 4. Stage IV larval skull of Notophthalmus uir6
descens. Dorsal (A), ventral (€9,and lateral (Cf aspects.
C
Pa
D
Fig. 5. Eft Stage skull of Notophthalmus viridescens.
Dorsal (A), ventral 031, and lateral (Cf aspects.
320
S.M. REILLY
Q
A
E
ipsilateral premaxilla and maxilla and forms
the entire medial and anterior rim of the
choanal notch in the Eft Stage (Fig. 5B). Posteriorly, the edentate portion narrows and
grows posteriorly under the parasphenoid.
The association of the posterior, tooth-bearing extension of the vomer with the parasphenoid is so close that the teeth appear to
be on the parasphenoid bone (Fig. 5B). In the
late Eft and Adult Stages, the vomers fuse
anteriorly, leaving a small median nasal passage, and form the roof of the mouth and the
choanal notch (Fig. 6B). Owing to progressive
posterior constriction of the vomers, two long
rows of vomerine teeth extend well back onto
the parasphenoid.
Palatopterygoid
The dual nature of the palatopterygoid,
representing the fusion of the palatine (anteriorly) and the pterygoid (posteriorly) is evident. The palatine appears in Stage I as an
irregular-shaped bone posterolateral to the
vomer (Fig. 1B). The dentigerous palatine
persists until metamorphosis as the only
tooth-bearing element of the palatopterygoid. In Stage 11, the pterygoid portion appears; it is somewhat constricted behind the
palatine, but expanded at the posterior end
Q
(Fig. 2B). By Stage 111, the palatopterygoid
still is constricted medially, but bears a wide
connection to the quadrate and prootic,
sq
whereas the palatine remains unchanged
(Fig. 3B, C). The palatine grows medially to
interdigitate with the vomer in Stage IV,and
fuses with the otic capsule and quadrate (Fig.
B
E
CI
4B, C). During metamorphosis, the narrow
strip of bone connecting the palatine and
pterygoid
disintegrates and the entire pala1 mm
tine is lost. The pterygoid, reduced in length
H
during metamorphosis, becomes fused more
solidly to the prootic and quadrate in the Eft
Pm-de Stage (Fig. 5B, C). In the Adult Stage, the
anterior spine of the pterygoid extends posteriorly and is attached to the maxilla by a
ligament to form the posterolateral edge of
0
the orbit (Fig. 6B, C).
Premmilla
The premaxilla of Stage I is a single bone
with wide, arcuate dentigerous processes that
extend laterally along the snout and with
D
C
two perpendicular dorsal rami (Fig. 1B). In
Stage I1 through I11 the dorsal rami overlap
Fig, 6. Adult Stage skull of Notophthalmus virides- the frontah (Figs. 2A, 3A). In Stage w, the
dentigerous rami extend laterally to touch
cens. Dorsal (A), ventral CB), and lateral (C)aspects.
CRANIAL ONTOGENY IN NOTOPHTHALMUS VIRIDESCENS
the maxillae and form a rostra1 notch (Fig.
4A). Dorsally, a palatal shelf extends posteriorly toward the vomers (Fig. 4A). The premaxilla changes little through metamorphosis, but by the Eft Stage, its fusion with
the nasal is complete, leaving a medial nasal
passage in the notch between the dorsal rami
(Fig. 5A). In the Eft and Adult stages the
premaxilla develops a large transverse shelf
that reaches to the palate in front (Figs. 5B,
6B).
Prearticular
The thin, pointed prearticular bone appears in Stage I medial to the distal half of
the dentary (Fig. lA), with the anterior point
wedged between the coronoid and the dentary. In Stages I1 through IV,the prearticular becomes trough-like as the lateral surface
curves dorsally. The posterior end of the
prearticular and its articulating surface enlarge and the anterior end expands to project
just beyond the coronoid (Figs. 2C, 3C, 4C).
By the Adult Stage, the high point of the
prearticular, in lateral aspect, culminates in
the “coronoid process” that is matched on the
outside by the dentary (Fig. 6C). The coronoid process varies in height but is always
the most dorsal point of the mandible in
adults.
Articular
The articulars seem to ossify after about a
year in the Eft Stage and are present in large
efts and all adults. Of four approximately
one-year-old efts examined, two still lacked
articulars. In another, the articular was cartilaginous and in the fourth it was ossified.
The articular ossifies as a small wedge posteriorly between the dentary and the prearticular, with its articulating surface facing
posterodorsally toward the quadrate.
Squamosal
The squamosal appears in Stage I as a thin
sliver of bone behind the eye (Fig. 1B). In
Stage 11,a thin otic process forms and curves
dorsomedially to a position at which it contracts the otic capsule in Stage I11 (Fig. 2A,
B). A frontal process projects forward as the
beginning of the frontosquamosal arch (Fig.
2C) that is unique to the salamandrids Wake
and Ozeti, ’69). The dorsal process is keeled
and extends obliquely downward to articulate with the forming quadrate bone. In
Stages I11 and IV,the hammer-shaped squa-
32 1
mosal increases in size and widens dorsolaterally (Figs. 3C, 4C). By Stage IV,the frontal
process expands to meet the frontal bone to
complete the frontosquamosal arch, and the
ventral process fuses solidly with the quadrate (Figs. 3C, 4C). In the Eft Stage, the
frontal process of the squamosal fuses with
the frontal bone to enclose the temporal fossa
and form the bony dorsum of the orbit (Fig.
5A, C). Owing to increased growth throughout the later eft period, the adult has a markedly larger and thicker squamosal which
dominates the skull laterally and marks the
widest part of the skull (Fig. 6A). Here, a
large scabrous keel demarcates the dorsolatera1 surface of the skull, and another large
keel runs down the lateral side of the squamosal to provide strength to the jaw articulation and more surface area for muscle
attachment (Fig. 6C). Parker’s (1877) illustration of the larval squamosal in no way
resembles the one described here.
Parasphenoid
The parasphenoid ossifies in Stage I1 and
extends from between the vomers to the foramen magnum in a parallel plane just dorsal
to the palatal bones (Fig. ZB, C). It has an
elongate pear shape with an anterior notch
and exhibits no major configurational change
through its ontogeny. It fuses with the surrounding bones and the otic capsule in the
Eft Stage. Parker (1877) described and illustrated a much longer anterior notch with the
rear portion of the parasphenoid pinched off
to form a posterior lobe and described this as
a rare condition for this bone. None of my
specimens approximates his description (see
Figs. 2B, 3B, 4B).
Orbitosphenoid
The side walls of the braincase begin to
ossify in Stage I1 when the orbitosphenoid
forms, medial to the eye, around the optic
foramen. The orbitosphenoid sometimes
touches the ventrolateral edge of the parietal
(Fig. 2C). In Stage 111, the orbitosphenoid is
free and irregularly shaped (Fig. 3C). By the
end of Stage IV,the entire bone is ossified
and fused to the prootic, parietal, frontal,
prefrontal, and parasphenoid (Fig. 4C). This
is in contrast to the condition in Ambystoma
texanum in which expansion and fusion of
the orbitosphenoid occurs after metamorphosis (Bonebrake and Brandon, ”71).No further
change occurs in the orbitosphenoid through
322
S.M. REILLY
metamorphosis, but its shape in Stage IV naris where the nasal, maxillary, and the
larvae, efts, and adults is highly variable (cf. premaxilla bones converged (Fig. 6A, C).
Figs. 4C, 5C, 6C).
There is no septomaxilla, contrary to Parker’s (1877) report.
Frontal
Parietal
Widely separated frontal bones appeared
in Stage II, each bone underlies the dorsal
The parietal bone begins to ossify in Stage
ramus of the premaxilla and bears a poste- 11, underlying the frontal, and has a midlatrior point that slightly overlaps the parietal era1 curve bending ventrally (Fig. 2A, C). By
(Fig. 2A, C). A small squamosal process pro- Stage 111, posterolateral expansion reaches
jects posterolaterally toward the squamosal. the otic capsule (Fig. 3A). In Stages I11 and
In Stage 111, each frontal widens and the IV, medial growth of each parietal closes the
squamosal process becomes its dominant fea- frontoparietal fenestra (Figs. 3A, 4A). By
ture (Fig. 3A, C). In Stage IV, the squamosal Stage IV, the parietal has grown laterally
process of the frontal establishes a wide artic- and ventrally to articulate with the frontal,
ulation with the frontal process of the squa- orbitosphenoid, and parasphenoid and
mosal, and solid contact is made with the thereby complete the braincase (Fig. 4C). In
orbitosphenoid, nasal, and prefrontal bones the Eft Stage, the parietals fuse medially
(Fig. 4A). From the frontosquamosal arch a (Fig. 5A) and cranial crests develop (Fig. 5C).
brow ridge runs across the frontal and con- Other than the enlargement of the crests
tinues onto the prefrontal to form the dorsal (Fig. 6 0 , little further change occurs.
aspect of the orbit (Fig. 4C). Another weak
Maxilla
ridge forms along the middle of each frontal
bone and continues onto each parietal. In the
The maxilla appears late in Stage 111as a
Eft and Adult Stages, this ridge becomes pro- small, toothless ossification posterolateral to
nounced and runs from the dorsal ramus of the premaxilla and anteroventral to the prethe premaxilla to curve convexly over the frontal (Fig. 3A, B, C). Through Stage IV the
maxilla grows anteriorly to articulate with
frontal, parietal, and opisthotic (Fig. 6C).
the premaxilla. A flattened facial process enQuadrate
larges dorsally into the cheek to meet the
The quadrate appears in Stage I1 anterior nasal and prefrontal (Fig. 4A, B, C). Later in
to the ventral process of the squamosal (Fig. Stage IV,a small jugal process appears (Fig.
2C). In Stage 111, the quadrate enlarges and 4A, C) and becomes greatly elongated in the
articulates with the pterygoids medially (Fig. Eft Stage (Fig. 5A, B, C). Then, in older efts,
3B, C). In Stage IV, the quadrate is pyrami- a few small teeth, in line with the premaxildal in shape, and touches the squamosal on lary teeth, begin to appear anteriorly on the
its lateral face, the pterygoid on its medial maxilla. In adults, the teeth are well develface, and the prearticular on its ventral face oped, but extend posteriorly only to the level
with its free face projecting ventromedially of the choanae (Fig. 6B). Teeth do not occur
(Fig. 4C). In the Eft Stage, the quadrate is on the long jugal extension of the maxilla.
slightly reduced in size, but fused more completely with the pterygoid and squamosal
Exoccipital
(Fig. 5B). By the Adult Stage, the articulatThis bone appears in Stage 11, with the
ing facets are greatly expanded laterally, and
bear a groove that receives the articular bone occipital condyle squared off posterornedially
to receive the cervical vertebra (Fig. 2B). Posof the mandible (Fig. 6B, C).
teriorly, the exoccipitals are rounded to form
Nasal
the rear of the skull (Fig. 2C) and a process
The appearance of the nasal marks the be- curves ventrally toward the parasphenoid
ginning of Stage IV. The pair of bones first (Fig. 2A). A pointed, curved sheet of bone
form as thin sheets of bone that gradually extends laterally over the dorsal otic surface
expand in the space between the prefrontal, (Fig. 2B) and although indistinguishable
maxilla, premaxilla, and frontal to overlap from the rest of the exoccipital, apparently
the dorsal ramus of the premaxilla (Fig. 4A, represents the opisthotic (see Otic Capsule).
C). In the Eft Stage, the nasals are not al- The sheet of bone continues to expand and
ways completely ossified, but by the Adult rapidly forms most of the otic capsule by
Stage, ossification is complete, leaving the Stage I11 (Fig. 3A, B, C). A small crescentic
CRANIAL ONTOGENY IN NOTOPHTHALMUS VIRIDESCENS
323
condyle remains, extending posteroventrally, (prefrontals and maxillae) appear and the
forming half of the round neural notch.
converging processes of the frontosquamosal
arches become evident.
Prefiontal
Stage IV
The prefrontal ossifies in Stage I11 as a
triangle of bone between the frontal and the
The nasals appear and the frontosquamosmall maxilla (Fig. 3A, C). In Stage IV, the sal arches are completed (Fig. 4). The otic
prefrontal spreads laterally and ventrally to- capsules are complete, but the nasal capsules
ward the maxilla, anteriorly toward the na- still are partially cartilaginous.
sal, medially toward the frontal, and
Metamorphosis to the Eft stage
posteroventrally to fill in the side wall of the
braincase along with the orbitosphenoid (Fig.
The onset of metamorphosis is signalled by
4A, B, C). Aside from the development of an the break of the palatine-pterygoid junction,
orbital rim, no further change occurs in the which is followed by the disintegration of the
prefrontal .
palatines and anterior portion of the pterygoids as the pterygoids realign in a more
Otic capsule
ventrolateral direction (Fig. 5). As metamorIn Stage 11, opisthotic and prootic ossifica- phosis continues, the coronoids are lost, the
tions appear medially to the otic capsule (Fig. lateral parts of the vomers expand anteriorly
2A, B, C). Formation of the double-walled to surround the choanal notches partially,
otic capsule progresses rapidly between while the posterior, edentate portions of the
Stages I1 and 111. The opisthotic ossification vomers elongate posteriorly and extend well
spreads dorsally and ventrally around the under the parasphenoid. The jugal processes
otic capsule from the rear and eventually of the maxillae become greatly elongated,
cuts under the squamosal and parietal. Si- and there is a complete ossification and
multaneously, the prootic expands posteri- thickening of the frontosquamosal arches.
orly and dorsally over the anterior part of The articular bones also appear in later eft
the capsule and fuses to the pterygoid. Before stages, first cartilaginous and then ossified.
the capsule ossifies fully, the oval operculum Bifid teeth eventually begin to appear and
forms within the much larger fenestra ovalis teeth form anteriorly on the maxillae in line
(Fig. 3A, B). Contrary to Wake and Ozeti (‘69) with the teeth on the premaxilla.
the columella is strongly ossified. In Stages
Adult stage
111 and IV, the foramen for the trigeminal
nerve is visible anteromedially in the prootic
In the adults, ossification and elongation
(Figs. 3B, 4B). In metamorphosis the ptery- completes the formation of the massive osteogoid rotates slightly laterally so that it has a cranium, but there is little difference bebroader articulation with the prootic dorso- tween larger efts and adults (Fig. 6). The
palate is complete, and a long, arcuate line
ventrally.
of teeth runs onto the maxilla from the preSUMMARY OF STAGES
maxilla. One distinctive character of the
Stage I
adult stage is the high point or “coronoid
The coronoids, premaxilla, vomers, and process” posterior to the teeth on the mandipalatines all appear bearing teeth (Fig. 1). ble. The skulls of branchiate adults are indisThe dentaries, prearticulars and squamosals tinguishable from those of normally
transformed adults.
appear as well.
One complete neotene was found in the
Stage II
Illinois population in 1976 by Ronald A.
Ossifications of the parasphenoid, frontals, Brandon. Externally, this gravid female (SVL
exoccipitals, parietals, and pterygoids mark = 48 mm) is like the other branchiate adults
the beginning of Stage II (Fig. 2). The squa- except that it has bushy gills, open gill slits
mosals thicken as the prootics, opisthotics, and gular fold, and a pointed snout. Examiquadrates, and orbitosphenoids begin to nation of the cleared and stained skull of this
individual shows that it is completely neoossify.
tenic, retaining all characters of a Stage IV
Stage III
larva (cf. Figs. 4, 7). None of the events of
Appearance of the opercula marks the be- metamorphosis has occurred and the only
ginning of this stage (Fig. 3). Cheek bones adult characteristic of the skull is the pres-
324
S.M. RlSILLY
ence of an ossified articular. The hyoid apparatus is completely larval in morphology as
well, although most of the elements have
ossified. This specimen is the only complete
neotene known from more than 1400 specimens examined from this population.
DISCUSSION
A
.
1 mm
,Pm-de
Pm-do
P
,
Ps
Pt,
C
Pa /
\
D
Fig. 7. Skull of a completely neotenic (nonmetamorphosed) adult Notophthalmus uiridescens.
Only one description of the skull of Note
phthalmus viridescens has appeared (Parker,
18771, based on two larvae and one adult;
however, it differs from the description presented here with respect to the parasphenoid
and squamosal bones, and also reports the
presence of septomaxillae (see Results). Life
history in the Notophthalmus viridescens viridescens population sampled is typical of the
species. Aquatic larvae become terrestial efts
for 1-8 years before returning to the water
to become permanently aquatic adults
(Chadwick, ’44, ’50). Along the Atlantic
Coastal Plain and in about a dozen inland
localities, where the terrestrial terrain provides a poor alternative to water, neoteny
has been reported Wecham, ’67). N. u. louisianensis of this study are from one of the
inland populations that exhibits both the
usual (completely transformed) and neotenic
strategies. Larvae either metamorphose into
efts, remaining on land for 1-2 years before
become aquatic adults, or they metamorphose directly into aquatic juveniles, and retain some gill apparatus (Brandon and
Bremer, ’66; Albert, ’67; Gates, ’78).
In this study, cranial metamorphosis was
well defined in neotenic newts and occurred
after the larval Stage IV.Changes in the
skull at metamorphosis (loss of coronoids and
palatines, new jugal processes of maxillaries)
seem to be adaptations for a change to terrestrial feeding. The minor changes (growth) in
the skull between efts and adults occurred
gradually and over a long period of time.
Changes known to occur in adults upon their
return to water (changes in skin texture, pigmentation, restoration of the lateral line,
keeled tail, aquatic retina, and increase in
ammonotelism; see Grant, ’61) seem to be
related more to the consequences of a return
to water and to sexual maturity (secondary
sex characters) than the result of a “second
metamorphosis” or the reversal of the first
metamorphosis of Grant (‘61).
All adults in this study, whether branchiate or not, had identically transformed
skulls. This confirms Brandon and Bremer’s
CRANIAL ONTOGENY IN NOTOPHTHALMUS VIRIDESCENS
report (‘661, based on two specimens, that
branchiate adults have fully transformed
skulls. Neoteny is limited to retention of
some hyobranchial and external gill structures. This represents a different and limited
type of neoteny, in which no delay in cranial
metamorphosis is involved and variable retention of some gill structures (limited neoteny) is essentially postmetamorphic. The
limited nature of neoteny in these newts also
is shown by (1)the gradual loss of gill structure in aquatic neotenes with age (Gates,
’781, (2) the rapid loss of gill structures in
neotenes removed from water (Noble, ’29;
Morgan and Sondheim, ’32;Healy, ’70; Gates,
’781, (3) the great annual fluctuation of the
percentage of branchiate adults in McGuire’s
pond (Gates, ’78, personal observation), and
(4)the great variability of retention of gill
structures (Reilly, personal observation).
The adaptive significance of limited neoteny in newts may be related more to behavioral than morphological selection as has
been proposed for Taricha granulosa Warangio, ’78). Because thyroxin controls both
metamorphosis and “land drive” in newts
(Grant et al., ’65),selection for decreased thyroxin secretion to inhibit “land drive” may
provide the hormonal basis for the limited
postmetamorphic retention of larval morphology (gill structures) as a “correlated response” (Mayr, ’63). The incomplete
metamorphosis of the gill apparatus and the
persistence of aquatic habitat preference in
newts with completely metamorphosed skulls
may result from the involvement of different
tissues having different response thresholds
to thyroxin. If this were true, then selection
to raise or lower the level of circulating thyroxin could result in the variation in metamorphic response observed in various
populations. For example, if circulating thyroxin exceeded the thresholds of all target
tissues, complete metamorphosis would result. If it did not reach the threshold of any
particular target tissue, complete neoteny
would result. Thus the branchiate adults
with transformed skulls in McGuire’s pond
might result if circulating thyroxin exceeded
the threshold needed for the cranium to
metamorphose but did not reach the threshold needed for the gill structures and habitat
preference to change. Whatever the mechanism, the significance of retaining larval behavior (aquatic habitat preference) and
thereby surviving in populations with hostile
325
terrestrial surroundings far outweighs the
value of limited retention of gill structures
that are not necessary for survival of aquatic
adult newts.
ACKNOWLEDGMENTS
I thank Ronald Brandon, Enoch Albert, and
Leslie Polgar for assistance in obtaining
specimens, and Linda Trueb for assistance in
preparation of the illustrations. Michael
Morris and Ronald Brandon provided invaluable discussions, and I thank them and an
anonymous reviewer for many useful comments which greatly improved the manuscript. This study was supported by the
Department of Zoology, Southern Illinois
University at Carbondale.
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