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The development of the skull of the turtle with remarks on fossil reptile skulls.

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THE DEVELOPMENT O F THE SKULL OF T H E
TURTLE, WITH REMARKS ON FOSSIL
REPTILE SKULLS
RALPH F. SHANER
Department of Anntonzy, Universitil of Alberta, Edmonton, Alberta, Canada
SIXTEEN FIGURES
This paper is the report of a study undertaken at the
suggestion of a distinguished paleontologist, who lamented
the lack of knowledge of the development of the reptile skull.
There have been of course numerous studies on the reptile
skull, as the long bibliographies of Gaupp (’06) and others
show. Some of Rathke’s pioneer work in vertebrate embryology was done in this field. The renewed impetus to the
study of the skull that Huxley’s Croonian lecture gave moved
W. K. Parker to investigate the reptile as thoroughly as the
technical means of the time allowed. More recent studies,
however, have fallen into two rather narrow groups and have
concerned themselves either with the story of certain parts of
the skull or with detailed descriptions of single embryonic
stages. From neither group can one gather a very clear idea
of just how the adult reptile skull comes into existence. The
study here reported is an attempt to apply modern methods
to the older and broader problem, to give a straightforward
account of the development of a representative reptile skull
from the precartilaginous to the adult stage.
The interest of most recent writers on the development of
the reptile skull has lain in comparative embryology, and
interpretative discussions have been chiefly comparisons of
the form studied with other reptilian chondrocrania or with
those of amphibia. I n the study here presented, the author
343
THE ANATOXICAL RECORD, VOL. 32, NO. 4
Iias sought for any light tlie developmental story might throw
apoii the adnlt reptile skull of living a i d fossil forms. A t
f l i c k clnd of this paper Ihcrc is atltlcd a short discussion of the
Fossil reptile skull frwin the standpoint of embryology.
1’11(1 turtle, C,’hrysemys marginata, lias bcc.11 used for
material iii this work, partly because of its availability, partly
l ) ~ ( m i s cof tile writer’s previous esperieiice wit11 it, aiitl
1)ill.t ly l)ecaiis~of tlie possible value its e m b r p l o g y might
liavt~ f o r s t i i d ~ ~ of
t s fossil forms. Despite its spccializcd
~*i~l’>t~
tlic
) i itnrtlc
~,
still rclmaiiis our hest living example of a
loiig-departccl aiiimul world. It is much iieurer the gcncrali z d l’ermiaii vertebrates tliaii 2111)- living form c w i l F
;ivailable for embryological study.
Tlic s t o r - of tlic turtle skull falls naturally into two partst lie tle\vlopmerit of the clioiitli.ocraiii~lmmtl the rqjlacemeiit
of t l i c csartilagiiioiis skiill hy the 1)oiiy oiic.
THE CII0SI)KOC’RA~IUIL
In (’1irj-sem;vs the cartilaginous skull reaches its greatest
( l ~ v ~ l o j ~ min
( wRt l!)-mm. embryo (figs. 11 to 13). Tlic braiii
is then c ~ c l o s e din aii iricomplcte cartilaginous shell. Thc:,
pilrts of tlic hraiii hcliind tlie Iiypopliysis lie iii a Imx, tlic floor
of which is foi*metl of cartilage laid domi o i l either side of
the notocliorti and of remains of the hypoglossal vertehixie.
tlie sides by tlie otic capsules, a i d the roof 1);- an estciision
of tile last t o foi*ma tecaturn. Tlic parts of the 1)rain aiiterior
l o the hypophysis lie in a sczilepaii-sliapeti structure k i m w
;is tlic plarium supraseptale. T h e plaiium is supportetl 1))m i iiiterorhital septum. “lie septum is joiiied to the posterior
part of thc skull 11)- a l--shapecl bar, tlie trabecula craiiii.
A n t cbriorly, the interorbital septum contililies between tlicl
LN the nasal septum.
( ~ l t ’ i i ( ~ tcapsules
ol*~
T l i ~remaiiiing pai.ts of tlic! clioiiclrocranium arc not coiiwiwd with the hixiii. I,atei*d to tlie otic capsules alreacl!.
mentioiicd a r e foimd the quadrate cartilages. Each quadrate
cartilage is hollo~vf o r the reception of the midcllc~ear. 111
ntltlitioii, it bears aii aiiterior pterygoicl process and articu-
DEVELOPMENT OF THE SKULL OF THE TURTLE
345
lates belov- with lleckel’s cartilage of the lower jam-. The
rostra1 end of the skull is formed by the tm-o nasal capsules.
To follow the whole of such a complicated structure from
stage to stage is a hopeless task. It is better to divide the
skull up into convenient parts a i d to treat of each in turn.
Accordingly, 1 shall discuss tlic following : 1) Prechordal
region, i.e., the skull proper anterior to the hypophysis,
2 ) Parachordal aiid hypoglossal regions. 3 ) Otic capsules
and columella auris. 1) Quadrate a i d Meckel’s cartilage.
5 ) Xasal capsules.
P rec h ord nl
,regio n
The first clement of the chondroeranium anterior to the
hypophysis to appear is a pair of rod-like trabeculae craiiii
(figs, 1 to 3 ) . They lie close to the miclliiic and extend from
the hypophysis to the nasal sacs. I n the 6-mm. stage figured,
they are the only parts of the skull that are choiidrified.
The secoiid element, also present in the same stage, is an
ill-defined arch of mesenchyma attached at either root to the
caudal tip of a trabecula and springing across the space
filled with the hypophysis. In the 6-mm. stage the arch is
penetrated by the oculomotor nerve and deeply notched f o r
the trochlcar nerve. The best name for this element is ‘miclbrain arch’ (arcus mescnceplialicus). It is the ‘middle tra1)ccula’ of Ratlike, the ‘alisphenoid-platten7 of Sewertzoft’,
and thc ‘ splieriolateralknorpel’ of Gsupp. Ratlike’s name is
confusing, the others assume unjustifiable associations witli
adult bones.
The third clement has appeared in a slightly older embryo
of 5.75-mm. length (figs. 4 to 6). Here one finds two lateral
plates, one on either side of the forebrain, anterior to the
optic nerve, and at first loosely attached to the trabeculae
cranii. The two lateral plates can he called the laminae
proseiicephalicae.
It will be noticed, in passing, that the whole prechordal
part of the skull is at first quite unconnected to the notochord or to any other part of tlie skull (fig. 3 ) . I n addition,
346
RALPH F. SHANER
the long axis of the prechordal part makes a riglit angle with
that of the rest of the skull, in conformity to the general outline of the brain at that time (fig. 2).
Each forebrain plate is at first attached to an independent
trahecula cranii, of the sort found in the 6-mm. embryo
(fig. 1). The loose connection of the plate to the trabecula
becomes a more intimate one, and at the same time a center
of chondrification appears between the trabeculae cranii. A
general fusion of all structures ensues, and the scalepan-like
support for the forebrain comes into being (fig. 4).
ABBREVIATIONS
A.m., niidbrain a i eh
~J.C., Sleekel's cartilage
A?&.,angular bone
A.op.. ophthalmic a i t e i y
Boc., basioccipital bone
Bsp., hasisphenoid bone
P a , columella auris
Coin., complementary bone
C . ~ . H , .lateral
,
iiasal cartilage
C.p..n., paranasal cartilage
C T . ~ . ,crista parotica
C.S., crista sellaris
C . I , 2 , 3 , cervical vertebrae
D., dienceplialon
D m t . , dental bone
Bnc., exoccipital bone
Rpo., epiotie bone
B p t . , epipterygoid
P.b., forelmtin
F.b.p., posterior basicrauial fe1iesti;i
Pxntl., foramen f o r endo1yrnpli:itic duct
Fh., fenestrz for liypopliysis
F.m.-x., nietotir fissure, foramen of
vogus nerve
I?., frontal lione
E'.ve. fenestra 1 estibuli
h'.tt-m, foiamen f o r tlie cereljral nerves
G o . , gonial hone
TI.b., hindbrain
H I / . , lryoid cartilage
I€.Z,2,5,hypoglossal I ertebtae
L p . , lamina prosrncephalica
M.b., midblain
Mx., maxillary bone
N.c., nasal capsule
A 7 4 nasal sac
O.C., otic capsule
Opn., opisthotir bone
P.,palatine lmie
P.u., abducens process
Par., parietal bone
P.et., epipterygoid process
P.t., iiiterhyial process
PZ.9., planurn supraseptale
Pof., postfrontal bone
P.pr., pila prootica
P.pt., pterygoid process
Prf., prefiontal bone
Pr m., premaxillary bone
Pro., prootic bone
Pt., pterygoid bone
Q., quadrate cartilage and bone
Q..?., quadratojugal bone
Su., surangular h i e
S.L., iuterorbital septum
S.n., iiasal septum
Noc., supra-occipital bone
Sq., squamosal bone
T o . , vomer
Z.C., trabecula craiiii
T . m , taenia mxrginalis
Z'.p., tectum posterior
%., zygoma
it-mt.,
cerebral iicrres
DETELOPMENT O F THE SKULL O F THE: TURTLE
347
Rleaiiwliile the ends of the two trabeculae craiiii grow
forward between the nasal sacs. Beyond t h e cerebrum they
form a single vertical plate (fig. 4) wliicli becomes a part of
the nasal septum.
c
/-\
Pigs. 1 t o (i W a s models of the clionilrocrania of embryos of Clirysemys
marginata. I a n d 2 , riglit side; 3, dorsal side from a 6-mm. embryo, Alberta
Ernbryo1ogic;il Collection, series 110; 4 aiiil 3 , riglit side; 6, dorsal side from a
3.75-mm. eml)rTo. A.E.C. 107. X 15.
348
R A L P H I?.
SHANER
The two forebrain laminae are next bent toward each other
and partly fused together. The wide-open V is converted
into a U with flaring limbs above. The fused ventral parts
of the laminae together with one underlying fused trabecula
make the interorbital septum (figs. 7, 9, Il), while the upper
flaring limbs of the laminae form the planum supraseptale
of the completed chondrocranium.
While the above changes are taking place, the midbrain
arch is also growing. I n the first stage modeled (fig. 1) it
encloses only the oculomotor nerve. I n the next model
(figs. 4, 5) the arch surrounds the trochlear nerve and the
ophthalmic artery, and extends in two flanges, one on either
side, along the midbrain and diencephalon toward the optic
nerve. The nerve then lies in a notch.
The optic notch is converted into an optic foramen by the
fusion of the flange of the midbrain arch with the forebrain
lamina (figs. 7,s). A process of the forebrain lamina pushes
backward beneath the nerve at the same time, between it and
the trabeculae, and forms the floor of the optic foramina.
While the midbrain arch grows forward, it also extends
backward and joins the tip of the notochord (fig. 4 ) , thus
forming the first connection of the prechordal region with
the rest of the skull. At the same time two slender mesenchymatous processes push forward from the otic capsules.
Each process is penetrated by the abducens nerve, and on
that account may be called the abducens process. I n the
5.75-mm. embryo modeled (fig. 6), each process is still free
from the midbrain arch; shortly afterward, fusion with it
takes place, and the union of the prechordal region with the
rest of the skull is accomplished (compare figs. 6 and 9).
The subsequent history of the midbrair, arch is one of differentiation and reduction. The sharp bend in the skull is
reduced (compare figs. 4 and i), the flange-like extensions
of the arch (fig. 4) tear away from it, but remain attached
to the forebrain lamina and form the posterior boundary of
the optic foramina (figs. 7, 9). A persisting remnant of
the connection of the flange with the parent arch forms the
DEVELOPMENT O F THE SKULL O F THE TURTLE
349
taenia marginalis of other reptiles. The midbrain arch itself
is reduced, the oculomotor and trochlear nerves and the ophthalmic artery regain their freedom. The arch then flattens
down into a bar behind the hypophysis, the crista sellaris of
Figs. 7 to 10 Wax model of the chondrocranium and membrane bones of an
8-mm. embryo of Chrysemys marginata, A.E.C. 104. x 15. 7 and 8, right side;
9, dorsal side; 10, ventral side of nasal capsule.
350
RALPH F. SHANER
Kunkel (figs. 11, 13), which continues to divide the fenestra
basicraiiialis posterior from the foramen hypophyseos.
The early midbrain arch bears two pointed processes (fig.
6, P.pr.). They persist and are molded into the pilae
prooticae of the mature chondrocranium (figs. 7, 9, 11).
Behind the pila prootica the trigemiiial nerve leaves the brain
case.
Parachordal a i d hypoglossal regions
I n the youngest stage modeled (6 mm., fig. 3 ) , the notochord
extends backward beneath the hindbrain without any special
covering of precartilaginous tissue. This area bet~veeiithc
otic capsules is gradually filled in from behind forward with
unsegmented mesoderm (figs. 6, 9). The notochord lies at
first above the floor plate, and tlien is embedded into it.
Chondrification follows from no specially defined centers.
When this part of the skull floor is finished, a small fenestra
basicranialis remains, behind the crista sellaris (fig. 13).
The extreme posterior part of the slrull floor, the l-lypoglossal region, has a more interesting history. Three
precartilaginous hypoglossal vertebrae are formed, corresponding to the roots of the hypoglossal nerve (figs. 1 to 3 ) .
The first pair of hypoglossal arches are short and stubby,
the rest differ in no wise from the cervical vertebrae that
follow. The neural arches of the hypoglossal vertebrae at
first lag behind those of the cervical vertebrae (fig. 6 ) , and
their bodies are fused into a common mass which joins the
floor of the skull. The first hypoglossal foramen seems t o
be obliterated. Later, the hypoglossal arches grow rapidly
and form a single big process which pushes up heliind the
otic capsule (figs. 7, 9 ) and fuses with it. A large cleft
always remains between the common hypoglossal process and
the otic capsule for the passage of the vagus nerve-the fissura metotica of the mature chondrocranium (figs. 9 , l l ) .
The entire hypoglossal regioii is chondrified in an 8-mm.
embryo. No distinct centers could he found in the bodies of
the vertebrae. An ill-defined center can be distinguished in
each neural arch.
I ~ E V E I J O I ’ J I E S T O F T H E SKTJLL O F T H E TCRTLE
331
O t i c capsule and colunzella atiris
The otic capsule is partly sketcl~erlin precartilage iii tlic
(i-mm. stage (figs. 1, 3). Tlie basal and lateral portions between the facial aiid glossopliar!-ngeal nerves a r e definite
enough to be modeled. The rest of the capsule is outliiiecl
iii precartilage in the next stage modeled (figs. 4, 6 ) , and is
well clionclrified a t 8 mm. (figs. 7, 9). No definite centers of
cdiondrifieation could he made out.
I n the turtle tlie glossopharyngeal nerve lies very close
heliind the otocyst, and the facial nerve similarly skirts
around its anterior margin. When the prccartilaginous otic
capsule is laid down, it surrounds the first p a r t s of both
nerves. The glossopliarpngeal runs into the large hole 011
the median side of tlie otic capsule together with the acousticofacial complex. The upper p a r t of the I-acnitj- is filled with
the endolymphatic duct (fig. 6 ) .
A bar of cartilage then separates tlie ninth from the otlier
nerves, so that the former enters the otic capsule through
a distinct foramen (fig. 9 ) , passes through the cavity of the
capsule, and emerges from a special foramen behind (fig. 7)an arrangement that is permaiient.
The intracapsular course of the facial nerve is shorter arid
has been questioned lo>- Terry (’19). I n the 3.75-mm. embryo
(fig. 6 ) the combined acousticofacial trunk enters the otic
capsule, aiid the iiidepeiiclent course of tlie facial nerve does
not begin until the acoustic nerve is spread out over the otocyst. Tlie little bar of cartilage anterior to the nerve exit,
tlie prefaciai commissure, seems as much a p a r t of the otic
capsule a s any otlier part. It seems correct, therefore, to
speak of a n intracapsular course f o r the facial nerve in
turtles. The intracapsular path of the facial nerve is eventually partitioned off from the rest of the capsular cavity.
The large vacuity in the median wall of the otic capsule is
gradually subdivided into several openings, one each f o r the
glossopharyngeal nerve, endolymphatic duct, a i d facial nerve,
and two f o r the acoustic nerve. One or more foramina for
hlood vessels also remain.
352
R A L P H F. SHANER
The dorsal crests of the otic capsules extend upward and
form the tectum, the roof of the completed chondrocranium.
The columella auris of the turtle is simpler than in some
other reptiles. When fully laid down in cartilage, it is a
dumb-bell-shaped structure. The long curved shaft is divided
in the middle by a constriction. The inner head o r operculum
fits into the foramen vestibuli, and together with its part of
the shaft constitutes the columella proper. The rest of the
shaft and the outer head make up what is known a s the extracolumella. The outer head or insertion piece of the extracolumella bears a tapering interhyal process (fig. 11)’which
in a 19-mm. embryo is attached by a non-chondrified shred
to the tip of Meckel’s cartilage.
Much interest has been lavished on the stages leading up
to the cartilaginous columella auris. The evidence of my
material confirms the work of Miss L. S. Smith (’14) on the
same species and harmonizes with the results of Shiino (’14)
and Golby (’25) 011 the crocodile and alligator.
I n the 6-mm. stage (fig. l ) , the turtle columella, extracolumella, and interliyal process are all laid down as one
piece of precartilage. The extra-cdumella and the interhyal
process show the most advanced precartilage. The precartilage of the shaft and operculum fades out into the younger
sort of which the otic capsule is made. The operculum is
distinct, however, from the more or less nebulous otic capsule.
The precartilage of the extracolumella is in the same stage
of development as is that which forms the hyoid apparatus,
a sort considerably adraiiced over the precartilage of the
otic capsule aiid Meekel’s cartilage.
It seems very likely that, as Miss Smith states, the interhyal
process at a slightly earlier stage joined the hyoid arch. The
union must have been very transient; the interliyal process
of the stage modeled (fig. 4) is already turning toward
Meekel’s cartilage. I n two other embryos of nearly the same
age (A.E.C. 108, 6 mm., A.E.C. 109, 7 mm.) the interhyal process definitely joins the tip of Meckel’s cartilage.
DEVELOPMENT O F THE SKULL O F THE TURTLE
353
In a 7-mm. embryo a constriction appears in the shaft where
it passes over the first pharyngeal pouch. The extracolumella is then marked off from the columella in the narrower sense. In an 8-mm. embryo centers of chondrification
appear in the extra-columella and columella. From this time
the columella auris is truly subdivided. A third center in
the interhyal process is doubtful; it is imperfectly chondrified.
In later stages the interhyal process dwindles (figs. 7, 11).
In the adult the extracolumella remains cartilaginous ; the
rest is replaced by bone, a trace of which can be found in a
28.5-mm. embryo.
The old question whether the columella auris is derived
from the hyoid or from the otic capsule, o r both, is an unreal
one. I n the first place, the division of the columella is a
secondary one that appears only with chondrification. The
simple precartilaginous columella, like any other piece of
precartilage, is laid down in situ. It is not budded off from
surrounding structures. After all, the columella simply develops out of the head mesoderm as a high light does in a
photographic plate, correctly fashioned and properly placed
from the start.
Quadrate and Meckel’s cartilage
A fragment of the quadrate and a small h-leckel’s cartilage
are sketched in prechondrial tissue in the first stage modeled
(fig. 1).
Meckel’s cartilage is temporarily joined to the growing
quadrate in a slightly older embryo (5.75 mm., fig. 4 ) . It
regains independence and shows traces of cartilaginous matrix in a 7-mm. embryo. At 8 mm. the right and left cartilages
fuse at their anterior tips without the aid of an intercalated
cartilage. The fused tips are fashioned to conform to the
peculiar shape of the lower jaw and the articular facet f o r
the quadrate is modeled out (figs. 11, 15).
The fragment of the quadrate present in the 6-mm. stage
(fig. 1) expands into a definite quadrate in the next stage
modeled (fig. 4). I t then consists of a dorsal and posterior
354
RALPH F. SHAXEIL
mastoid portion, a rod-like articular part temporaril;-- fused
with Meckel’s cartilage, and a pterygoid process. I n a 7-mm.
embryo cartilage matrix appears in the mastoid part aiid the
quadratomecltelian joint is laid out. I n an 8-mm. embryo
(fig. 7 ) the mastoid part is enlarged, aiid an ascending epipterygoid process, homologous with the ‘columella ’ of ltiiiocraniate lizards, is added t o the pterygoid process. Tlie
whole is now in cartilage. While the chondrocranium grows
to its maximum in the 19-mm. embryo (fig. ll), the mastoid
part of the quadrate is hollowed out to accommodate the
middle-ear outgrowth from the first pharyngeal pouch.
The pterygoid process of the quadrate of embryos around
6 mm. in length (fig. 4) lies just above the ruclimciitary
dental ridge of the upper jaw. The pterygoid process thus
bears the same relation t o the upper jam that Rleckel’s cartilage does to the lower. The quadrate, its pterygoid process,
and Meckel’s cartilage form an oral visceral skeleton w r y
much like that found in salmon embryos (Gaupp, ’06).
Nasal capsule
The first part of the nasal skeletoii to appear is the septum,
the rostra1 part of which develops on tlie fused tips of tlic
trabeculae craiiii (fig. 4). Tl‘hen the nasal capsules appear
(8 mm., fig. 7 ) , they extend backward along the interorbital
septum for some distance. Tlie part of the interorbital septum
that lies between the capsules is added to the nasal septum
in the mature cartilaginous skull.
Each nasal capsule arises from two distinct cartilages
which appear in the 8-mm. stage (figs. 7, 10). Tlie smaller
medial paranasal cartilage lies along the ventral margiii of
tlie iiasal septum. The larger lateral cartilage forms tlie side
arid roof of the capsule. To form the roof, the lateral cartilages fuse with the dorsal margin of tlie nasal septum--a
process already begun at this stage aiid completed in the iiext
older one modeled. The kioor of the nasal capsule is completed by fusion of the paranasal with the lateral cartilage,
and with the ventral margiii of the septum. A persisting
DEVELOPNEXT O F T H E SKULL O F THE TTJRTLE
355
slit on either side of tlie \-eiitral margin of tlie septum forms
the prepalatiiie foramen. The tips of the two nasal cartilages are distinct at the posterior choaiiae long after the
capsule is complete.
The general contour of the nasal capsule is governed hy
the nasal sacs. In the completed cartilaginous capsule
(fig. 11) one caii distinguish hetweeii a ventral cylindrical
respiratory part, which forms a direct passage between thc
two choanae, and a dorsal dome-shaped olfactory portion.
The line of separation is marked by a slight fold on tlic
lateral wall of the capsule aiid by a parallel ridge on its iiirier
surface. A small ~ioclule,tlie pila supraglandularis of Kuiiltel,
which is attached to the nasal septum, may separate the two
parts medially.
In tlie mature cartilagiiious nasal capsule, tlie iipper lip of
each anterior clioaiia is deeply incised to accommodate a dorsal gland, which spreads out between the capsule and the
bones that form over it.
The fiiiished cartilaginous skull, the several parts of wliicli
have been followed in development, is found in a 19-mm.
embryo (figs. 11, 12, B ) . Icunltel’s ( ’12). admirable and exhaustive descriptioii of the mature chontlrocranium of Emys
is easily accessible, and 110 special discussioii of this stage
iii Chrysemys need be attempted here.
DEVELOPMEKT OF T I I E ADULT SKI‘LL
As the choiidrocraiiium approaches its maximum, the memhraiie hones appear around it, takiiig up at oiice their permaiieiit positions and relations. The chondrocranium is no
sooner finished than it degenerates. Much of it is replaced
1,y bone developed from centers located in the cartilage matrix. This second class of cartilage bones comes into correct
articulatioii with the membrane bones to finish off tlie adult
skull. The remaining portioiis of the chondrocraiiium, in the
turtle a t least, are largely resorbed. T’he three steps, then,
in the development of tlie adult skull, which caii now be followed in detail, are : 1) Ih-elopment of memhraiie bones.
356
RALPH F. SHAWER
2 ) 1)evclopmeiit of cartilage lioiies. 3 ) Ihgeiieratioii of t h e
c.11OII drocraiiiii ni.
*If? )>I 1) )'I2 It P
110 I ) V.S
'l'licl first memhraiie Imies are fouiicl in an 8-mm. emhrJ-o
which the squamosal, prefrontal, maxillar>-, ant1
dental boiies appear. In the 19-mm. stage (figs. 11, 12, 13)
all membrane bones are present but the parasphenoid and
the doubtful membrane element of the hasioccipital. The last
two are found in the oldest embryo modeled (figs. 14, 15, 16).
The memhrane bones of the turtle skull fall into six groups :
Group I. Dental, angular, suraiigular, gonial, and comj)lemeiitary h i e s . These form the greater part of thc lower
( fig. i ) ,in
J?I%-.
( t roup 1I . Parasplieiioid, palatine, ptcrygoid, vomei-, ant1
maxillary ?,ones. These form the roof of the month, supplemtwt the floor of the ctioric~rocl.aniumanterior to the Iiypophysia, aiid iii tlie adult form tlie h x c of the skull over the
samv area.
( i i*oup 111. Parietal arid frontal 1)oiitls. These two cornp l d c . the 1.0of of tlie brain casc.
( f r o ~ p11'. E'refroritnl, postfroiital, zygomatic, p;irts of the
~)alntiiiea i d of the maxillary 1,ones. This well-tlc.fiiied gi*oiip
malccs n p the orbit.
Group T.'. Premaxillary boiic. Tlic premaxil1ar~-is the
s o l t a ixyJresentatire iii turt1c.s of tlic group of memhraiie 1)oneh
that tlevclop around the iiasal capsule. In otlier reptiles tlic1
irasal and septomaxillary bones w ~ ~ i i lfall
d here.
(froup VI. Squamosd R I M I qnadratojugal hones. Both of
tliese are closely related to the quadrate cartilage a i d bone.
Wietlier or no thcsc g ~ o u p shave aiiy sigriificance outside
reptiles the writer leaves to others more skilled in following
the intricacies of skull development in other vertehrate
classes. Of the value of the groups in understanding thc
reptile skull more d l be said below.
DEVELOPMENT O F T H E SKVLL O F T H E TURTLE
357
Figs. 11 to 13 TVax rnodel of the clioritll.ocl.:rriiurri and niciii1)r:ciir lmies of
a 19-mm. eml)r>o of Cliryseniys rii:crgiiiat:i, A.E.C. 103. x 11. 11, lcft sitlc;
12, riglit side; 13, ieritral side.
338
IlALPH F. S H B S E R
(’artilnge hoizes
‘I’lie bones which arise in cartilagc arc all fouiicl I)eliiiitl
the hypophysis. They are s h o ~ v i i iii thc oltlcst embryo
modeled (28.5 mm., figs. 14, 15, 16).
The basispheiioid arises from two centers. The bone so
formed fuses with tlie membraiie-bone parasplieiioitl just
anterior t o it. The parasphenoid lies lieiieatli tlie li~-pophysis
;
it closes off tlie hypophyseal fenestra of the clioiiclrocratiiii~~.
Tlie lateral boiiiiclaries of the fencstra, i.e., the arms of the
Y-shaped trahecula craiiii (fig. 13), later ossify a s cartilagc
bone and fusc with tlie parasplicwoid beiic~~tli
to form tliv
sliallow pocket in which tlie Iiypophysis rests. ‘I’lie adult h s i sphenoid is theref ore formed of two cm+lage-hoiie clement s,
the basisphenoitl proper am1 the ossified p a r t s of the trnhecnla cranii, and the memhi*aiie-hoiie pai.asplieiioic1.
The basioccipital also arises from two centers. The hone
extends back into the occipital coiid~-le. Aiiteriorly, the h s i occipital aiiiiexes two delicate lamellae which lie heneath thr.
cartilage floor atid which are p~-obahlyof mcmbraiie hoitc.
The basioccipital in Cllirysemys is a l ~ a p sdistinct from tlic
exoccipitals. I n Chrysemps tlie extreme lateral p a r t of tlic1
cartilage floor, the crista substapedialis of Iiniiliel, seems t o
lie i q l a c e t l by R tiny ossicle that remains iiitiepeiitleiit of tlie
Iiasioccipital.
The exoccipital o r pleui.occipita1 hones prohahly ossify f rorn
several centers which could not be clearly distinguished. Tlic
bony matrix extends d o ~ winto the side of the occipital
coiitlyle and up into tlie hypoglossal or exoccipital process.
In C‘hrysemys the exocacipital does not fusc with the
opisthotic.
The epiotic is coiitiiinous in tlie stage modeled with tlic.
supra-occipital, the ossification in the tectum. Tlie two arc’
usually described as distinct lmies mcoiidarily fused. Yo
trace of secondarj- fusion appears in the 28.5-mm. emhryo.
The tecatum, it shoalcl he remembered, is a n exteiision of the
otic capsules atid has n o coiiiiectioii with the occipital cartilage. In the 28.5-mm. embryo the supr;i-occipital likewise
seems to lie a n extens;oti of the two elliotics.
DEVELOPMEST O F 'L'HE SIiPLL OF THE TT-HTLlC
359
menibraiic bones, and cartiFigs. 14 t o 16 Wax model of the elioiidroera~~iuiii,
lage bones of :I. 28.5-niui. embryo of ClirpemJ-s margiiint,a, 4.E.C.106. x 7.
14, left side; 1.7, riglit. side; 16, ventral side.
TIIE
:\XATOMICAL RXCORr). VOli. :12. NO. 4
360
RALPH F. S H A N E R
The quadrate, exclusive of the pter:-goid process, ossifies
as tlie quadrate bone. Before ossification sets in, the cartilage beneath the squamosal degenerates, and tlie large hole
left in the quadrate remains, although covered by the squamom1 bone.
The pterygoid process breaks away from the quadrate cartilage (fig. 14) and ossifies into the tiny epipterygoid hone,
which completes the lateral wall of the brain case.
‘Iko more cartilage bones, not directly connected with tlie
s k i i l l ai-c fourid in the 28.5-mm. embryo. The articular bone
appears beneath tlie quadratomeckelian joint in Meckel’s
cwtilagc (fig. 3 5 ) . The opercnlum of the columclla anris
sliows a trace of ossification. The extra-columella remains
cbartilaginous throughout life.
ljsgeneration of the chondvoct-aniwm
‘1’11~~chondrocranium behind tlie hypophpsis is replacecl by
cartilage bones. The extra-columella is the only pcrsisting
cltrtilagirious structure in this region.
The pilae prooticae are degeiieratiiig in the 19-mm. and
the 88-mm. embryo. They disappear witliout trace in the
;Id111
t.
The rest of tlie clioiidrocranium, the trabecula cranii (exwpt tlie parts incorporated into the basisphenoid) , the intcr( ~ r l ) i t dseptnm arid tlie planum mpraseptale, which together
made up the basket for the forebrain, are reduced to a set of
riwrnl)t*ane~.The membranes rctaiii the extent and shape of
thc cartilage, but are devoid of matrix and are made up of
c.oiinective tissue. No ossicles develop in the interorbital
Z;Cp t 1111.
‘I’lie nasal capsule is also reduced to a connective-tissue
rneml)raiie, which contains scattered groups of cartilage-like
cells without matrix. The nasal septum is also largely mcmhranons ; it does contain, however, :E delicate plate of hyalinc
vnrt ilagc.
DEVELOPMENT OF THE SKULL OF THE TURTLE
361
NOTE Oh- FOSSIL SKULLS
The turtle skull, because of its simplicity and massiveness
alike in the embryo and in the adult, lends itself very well
to an embryological interpretation of the reptile skull. With
its help, embryological criteria for many bones can be laid
down, which may help to clear up homologies in fossil forms,
and some of the more bizarre features of certain extinct
species can be understood and explained.
Cartilage bones
Of the occipital- and otic-bone groups nothing need be said,
for the criteria of these are obvious and homologies in this
part of the skull rarely cause difficulty.
On the sphenoid group, however, the data in this paper can
shed some light. ‘Basisphenoid, ’ ‘parasphenoid, ’ ‘presphenoid, y ‘orbitosphenoid, ‘alisphenoid,’ and ‘ethmoid’ are
terms applied by paleontologists to various bones that replace
the crista sellaris and the prechordal chondrocranium. The
terms, as used by many writers, are ill-defined and overlapping. The following criteria, some old, some new, may be
of use.
The basisphenoid, in the narrower sense, is an ossification
of the cartilage skull floor behind the hppophysis, in the crista
sellaris. I n many reptiles the cartilage floor and the basisphenoid bone have a lateral basipterygoid process on either
side. The process is absent in turtles generally. The parasphenoid is a membrane bone which closes off the hypophpseal fenestra and (especially in primitive reptiles) extends
forvi-ard beneath the trabecula cranii and the interorbital septum. The terms presphenoid and ethmoid should be applied
to ossifications in the interorbital septum, the former restricted to bone formed in the posterior part of the septum;
the latter, to bone laid down in that part of the septum adjacent to the nasal septum. The orbitosphenoid is an ossificatioii
of the planum supraseptale, above and behind the optic nerve
and anterior to the oculomotor and trochlear nerves. The true
iiIi~pIieiioi(1in wl)tilcs is ail ossification of the piln prootica,
w t l lieiicch lies hetween tlie oculomotor and troclil(~ar~ierves
i i i front a i d the trigeminal nerve behind.
In ~)~iitzc,iitologicalliteratnix? the I)asisplimioitl ttnd pai-ahplic~iioiclare seldom icleiit Xed incorrectly. The parasplieiioit I
s l ~ o its
~ ~fundamental
s
iiatnrc \'cry clearly in the cotylosaurs,
for example. Tlie presplienoid is typically clevelopecl in
I,;imhiosautw,-: (Uilmorc., '24) m t l in Ecimoiitosaums (Lambc,
'20). I11 ('oi.;\-tliosauriis l'arlis ( 7237pl. ITT) givtw the iiaino
~mrasplieiioid'to il large vertical blade \I-liich projects forward from the basisplienoitl lieileath tlie optic 17en-e. W l d c
t l i r 1)oncmay have R ~~araspliciic~icl
edge, most of it is almost
ccAi.tainly replacing tlic tlahecula c n i i i i ant1 the iiitcrorl~ital
scptum, ~ i t lshoiilcl he called a presphcnoid. The term
'c~thmoicl'lias been loosely applied to an ossification of the
w l i o l ~iiitomrbital septum iii Laccrta ( Parker and Haswell)
a i i t l iii 1)intlcctes (('asp). In siwli cases 'prespliciioitl' is prcfci.ahle; the term 'ethmoid' slioiiltl hc restricted to the rostra1
part of the interorbital septum, n-hich may hare some re1at'ion
t o t h e tltlimoicl of mammals, a s Sollas aiitl Sollas ('14) liave
lJoiiitcv1 out in their monograpli 011 I)icyiotloii.
X i 1 ossification of tlie part of the planum supraseptale Bchind the optic nerve-the metotic region--has been called the
6alisplienoid' b~ Parker ('79). Snch a bone lies iii the field
of tlic orbitospliciioicl. 'I'lie truc alisphenoitl, in all modern
forms in which its development can bc follomxl, arises as
an ossification of the pila prootica.
X more important source of confusion in tlie alisplienoid
~ ~ y i oisi i the qiiestion of tlie presence of mi epipterygoid iii
p I a ~ eof 811 alisphenoicl boiie. il true alispheiioid ossificatioii
of tlie pila prootica is fouiitl iii Tropidonotus (Parker, '78)
:\11d in the crocodile (Kesteveii, '18). In Lacerta the cartilaginous pila prootica persists. In the turtle tho pila disappears ant1 tlie gap in the brain case is filled 1))- an epip t el*ygoid os sificat ion of t lie epipt erygoid and p ter 5- goid
processes of the quadrate (figs. 11, 14). 111 fossil forms oiie
c i i i i sometimes determine wliicli hone is preseiit t)y iiotiiig
DETELOPLMENT O F T H E SKULL O F THE: TTTIITLI.:
363
the slight differences in relations to nerves and bones which
follow upon the differing developmental histories of tlie two
bones.
The alisplienoid is an ossification of tlie pila prootica (fig.
11). The trochlear and oculomotor nerves lie anterior and
the entire trigeminal nerve lies posterior to tlie pila. The
alisphenoid takes over the same relations. !Phe alisphenoid
develops in the plane of the otic capsule, and hence is not
apt to overlap the prootic bone and will not usually cover
the foramen of the facial nerve.
The epipterygoid hone is an ossification of the epipterygoid
and pterygoid processes of the quadrate cartilage. In the
chondrocraiiium the maxillary and mandibular nerves cross
the pterpgoitl process behind tlie epipterygoid process, but
the ophthalmic turns forward along the inner side of the
pterygoid process to reach the orbit. When the cartilage
structures are replaced by the epipterygoid bone, the first part
of the ophthalmic nerve is covered. Also, since the epipterygoici bone has a more lateral position, it tends to grov backward over the lateral surface of the prootic bone, and can
cover the facial foramen, as it actually does in the turtle.
I n Edmoiit osaurus (Lambe, '20) tlie alisphenoid clearly fits
into the space in front of the prootic and the exits of the
trigeminal a i d facial nerves are unohstructed. I n Lambeosaurus (Gilmore, '24) the bone marked ' alisphenoid' extends
back t o the paroccipital (opisthotic). No facial foramen
shows in the drawing. I n tlie text Gilmore quotes Lambe as
saying, " The ophthalmic branch of the trigeminal nerve is
enclosed in bone in its forward course . . . , " I n this illstance the presence of an epipterygoid" is very likely.
Nembrasze hones
The membrane bones of the higher vertebrate skull are
descendants of ossifications found beneath tlie skin of the
head and around the oral cavity of lower t-ertebrates, bones
which at first had no close relation to the skull proper. In
mammals this overskull has been intimately welded to the
364
RALPH F. SHAKER
caartilaginous bones. I n reptiles one finds an interesting halfwag stage in evolution, mliere the membrane bones retain
wnsiderahle freedom in tlie adult and betray their origin
rery clearly in the embryo. From the embryonic grouping
of the membrane bones some useful criteria for the adult
bones can be established and some of the extraordinary
developments of the reptile skull explained.
The group of hones laid down on the ventral aspect of the
c4iondrocranium (group 11) corresponds fairly well to the
' Zaliiiknoclien' of Hertwig and G egeiibaur (Oaupp, '06)a group thought to have arisen around the teeth. I n reptiles
their secondary relation to the brain case is more important.
The separate bones are usually easily identified from their
standard relation to one another and to the overlying brain
case. The pterygoid may have a constant relation t o the
pterygoid process of the quadrate ; in reptiles it generally
encloses the palatine branch of the facial nerve, as Gaupp
has pointed out.
Tlie parietal and Frontal bones (group 111) complete the
roof over the brain case. They can be identified by their
standard relation to the cranial cavity. The two bones seem
to he the most conservative in the reptile skull. Almost the
extreme of variation can be found in the turtle and tlie snake.
Ti1 the turtle the parietal seiids a long process ventrally to
lill in part of tlie vacant alisphenoid area. 111 the snake the
froiital extends ventrally and does duty for absent orbitosphenoid-a defect correlated with the slight development of
the orhitosphenoid (prechordal) region in snakes.
Group I V includes the prefrontal, postfrontal, zygomatic,
and in part the maxillary bones, to which may be added the
postorbital and lac~hrymalof other reptiles. All are subtlcrmal ossifications that have at first a very loose connection
with the skull. They are an early generation of sclerotic
bones which are later incorporated into the skull to form
;t socket for the eye. No matter what changes take place in
tlie skull, the members of this group retain their relation to
each other and to the eye-a characteristic which serves to
iclentify them in most diverse types of reptile skulls.
DE\'ELOPI\IEXT OF THE SKULL O F THE TURTLE
365
I n the nasal group (V) the turtle skull has but one bonethe premaxillary. I n other reptiles the septomaxillary and
nasal bones would be included. All three bones develop as
ossifications to cover the cartilaginous nasal capsule and hax7e
at first a very loose connection with the rest of the skull. The
premaxillary lies on the ventrolateral (respiratory) surface,
the nasal on the dorsal (olfactory) surface, and the septomaxillary lies beneath the ventromedial cartilage and tlie
organ of Jacobson. In the turtle a process of the prefrontal
takes the place of a nasal, and the absence of a septomaxillary
is perhaps correlated with the doubtful presence of an organ
of Jacobson.
The close relation of the t h e e bones to tlie cartilaginous
nasal capsule explains the formation by them of the
extraordinary crests of tlie helmet-crested Hadrosauridae,
e.g., Lambeosaurns and Hypacrosaurus (Gilmore, '20). The
helmet in the crested dinosaurs contains an hypertrophied
olfactory apparatus. The premaxillary and nasal bones have
only developed with the organ around which they are laid
clown in the first place.
The nasal capsule and its related bones are semi-independent of tlie rest of the embryo skull, and can hypertrophy
ivithout affecting the rest of the skull. It is unlikely that the
frontal bone, for example, would follow the nasal capsule and
participate in the formation of such a crest, as Parks ('22)
thinks the bone does in Parasaurolophus.
The last group of membrane bones (VI), the squamosal and
quadratojugal, are definitely associated with the quadrate
cartilage and bone. The squamosal appears on the posterior
and dorsal aspects of the quadrate cartilage and the quadratojagal develops along its anterior margin. I n later stages
(fig. 15) the squamosal overlaps the quadratojugal along the
dorsal margin of the quadrate. These are the embryonic
criteria f o r the bones tliat Thyiig ('06) has established f o r
vertebrates generally.
T ~ ipno ral a w h es and varwifiP-9
The grouping of the membrane bones in turtle embrpos suggests aii explaiiatioii for the origin of the temporal arches
a i d vacuities. Ti1 riearly cvery case the tcmporal arclies can
be thought of as an arrangement wliereb>- the quatlratc+sciuamosal-quadratojug.al group is fixed to tlie cwmium and
its roof bones on one hand ant1 to the orbital group of hones
oii the other. The object would seem to be tlie slioring of
the quadrate-mandibular joint. Roily tissue characteristically iiicreases along lines of stress aiid strain, and disappears
where these are absent. Tlie arclies seem to be placed 011
such lines of stress and strain which would appear d i e i i the
mandibular joint is l'mictioriiiig; the vacuities mark elements
of the stegocephalian memhraiie-bone orerskull which are not
needed in tlic more compact reptile skull. It is true tlie
turtle is ahcrrant iii this matter; its hoiiy arclies clo riot easily
lend themselves to comparisoii with those of other reptiles.
The turtle is an exception, ~ O T V C T ~ *wliicli
,
helps prove tlie
rnle. The turtle quadrate is unusually hroaci and flat, and is
wcll fixed to the otic bones. Heiicc the temporal arches are
less needed and are more variable.
Such is, of course, not the d o l e story of the temporal
arclies. The writer is in iio seiise of the word an expert on
fossil reptiles. It does seem to him, a student of the reptile
embryo, tliat the paleontologist lays too much stress on the
vacuities and the loss of such loosely articulated bones as the
intertemporal. Both of these are secondary to the arches
ilnd the reiiiforcement of the cluadrate-maiitlil)ulal. joint in a
type of skull that is chaugiiig from the loosely articulated
ampliibiaii sort to tlic compact unified sliull of higher
vertebrates.
L I T E R A T U R E CITED
1907 e b e r die Entwickeliing tlcs 01jcrculuiiis der L-rodelen und dcs
Distelidiuins (Coluriielln auris) einiger Ilcptilien. Anat. Anz., ErgSnzungslieft, Bd. 30.
GAUPP, E. 1906 Die Entwickeliuig tlrs Kopfskelcttcs. Hand. (1. rerg. u. e s p
F h t . (1. \Virb., Bd. 3, T. 2.
1900 D:IS Clioiidrocr:iiiiiiiri roil Lacerta agilis. Annt. Hefte, Bbt.
1, H. 49.
GILMORE,C. W. 1924 Contributions t o vertebrate Paleontology. Bull. 38,
Geological scrirs 43, Caiindinii Geological Survey.
GOLBY,F. 192.? Tlie development of tlic coluniel1:r anris in the Crocodilia. J o u r .
Anat., ~ o l 59.
.
KUNKEL,
B. 1912 Tlie developm~~iitof the skull of Emys lutnrin. Jonr.
Morph., 1-01. 23.
KESTEVEN,
€1. I,. 1918 The liomology of tlic m:immnalian alisphenoid and the
E:cliidti:i-pter?goid.
J o u r . Anat., vol. 32.
ILUIBE,
L. 111. 1920 The IIadrosaur Edinontosaurus from t h e upper Cretaceous
of A l l ~ ~ t a Memoir
.
120, gcw1ogic:il serirs 102, Canadian Geological
Surrey.
PARKER,
W. K. 1878 On the strneture and derclopment of the common biiake.
Phil. Trans. R.S., 169, pt. 2.
-___
1879 On the structure a n d development of the skull in the Laecrtilia. Pliil. Trans. R.S., 170, pt. 2.
~ ’ . ~ K K sW.
, A . 1922 1’ar:is:iurolopliiis wulkrri. Univ. Toronto Studies, geological series 13.
1923 Corytliosaurus intermedius, :I new species of Tracliodoiit
dinosaur. Univ. Toronto Studies, geological series l.?.
RICE, E. L. 1920 Tliu devplopmwt of the skull in t h e skink, Eumeces quinquclineatus. Joor. Rlorph., vol. 34.
SHIISO, I(. 1914 Das Clionrirocraniuiii voii Crocodilius mit Beriicksichtigung
tler Geliirnrierven und der Kopfgefiisse. Anat. Hefte, H. 30, AM. 1.
SNITH,L. W. 191.2 The origin :rnd de~elopirieiit of the coluniella auris in
(’hryseniys marginata. An at. Anz., Bd. 46.
SOLLAS,
I. €3. J., AND SOLLAS,
w. J. 1914 A study of the skull of a Dicyiiodon
hy means of serial sections. Trans. R.S., 204 B.
TERRY,R. J. 1919 The relation of the faci:rl nerre and otic capsule. Anat.
Rec., vol. 17.
TIIYNG,3’. W. 1906 Hquainosal bone in tetrapodnus vertebrata. Proc. Boston
Soc. Nnt. Hist., vol. 3 2 , no. 11.
FUCHS,
H.
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