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ILLINOIS BIOLOGICAL
MONOGRAPHS

Vol. VI January, 1920 No. 1

EDITORIAL COMMITTEE

STEPHEN ALFRED FORBES WILLIAM TRELEASE

Henry BALDWIN Warp

PUBLISHED UNDER THE
AUSPICES OF THE GRADUATE SCHOOL BY
THE UNIVERSITY OF ILLINOIS

.
Copyricnt, 1921 py THE UNIVERsITY oF ILLINOIS
DISTRIBUTED FEBRUARY 5, 1921

/ THE NASAL ORGAN IN
AMPHIBIA _

WITH TEN PLATES

BY
GEORGE MARSH HIGGINS

JUL 1 8 eu

Contributions from the
Zoological Laboratory of the University of Illinois
under the direction of Henry B. Ward No. 171

THESIS

SUBMITTEDIN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE
OF DOCTOR OF PHILOSOPHY IN ZOOLOGY IN THE GRADUATE
®
. SCHOOL OF THE UNIVERSITY OF ILLINOIS

1919

TABLE OF CONTENTS

Page

TTMTLOCUGLIOMG deta tA oe erect es attire re | otsratole, ofsten st ousy nto oten soy cxchonepeisyewe 7
M@he NasaleCapsulesyor ther Urodelamy arr sjaetre - crsieisi) sie leieteielereciedetel hate 8
Amb ly stoma pum Cla wane lye sesh chal ser sic) a ckenchs cieveleletevavelfench= 8
Salamandragmacwlata see wicieisctere Attar sic)eie,sicusl sciclol shotisue ae easton 14
TRTICONMETISCALUS eter eee eucrcls ciclere. «(cis nei sions @ siarsl ania) etaleh od seekerouerons 17
DiSmICeylUs pe viTIGeSCENS asia vers <velalct= haucrclane «1 sels <poleiete leone 19
Cryptobranchus alleghaniensis.............. Siohves ti AIR 21
Spelerpesmbilimeatusmrrs saya sertercer ie 8 veils siesta 25
Plethodonwenythronotust.- eerie - ltere ils eretolceleiral oes 27
INGERITIG, INERT Ce yng dan cocnoemobieobe ne bon cioscon co bour 28
Np, GNCENS. oben bdeacsdacqaneRsoocobboCoSUoohbooC 31
The Nasal Capsule of the Gymnophiona .....................---- 35
DGC oa doechoeSbonesbesGoabescoouumoouB Oo 35
Comparison of the Nasal Capsules in the Urodela and Gymnophiona. 40
MhesNasaliCapsulesron thevAMUrajy. sci c)-r-1-1tarjeretais ysis ore coker 49
Bipamamenrican deer. mcwane ier tecrcie verre eta ae sence epee 49
Bufo) americana)... . RAiave Ne aee ates RPO eR real oretescore 51
Eley Lava C ETI Lily for secyelcl ae exces ororsis ain eee AS Sle eye clin te sven 54
FRAN Ae VATIG ESCO epee ove epetcts oo ask chaps ceacper oi eect Pa oi omessie seers ones 55
Comparison of the Nasal Capsules in the Anura................... 58
Conclusions Based on this Study . Bears ste aay Sereree POO
Phylogeny of the Nasal Goosen on nAcaphibia stats fast avave aes sohie Const 60
Classification of the Amphibia; 44.42)... - 2 seo leet 63
Amphibian, Am Cestrysa actos ust eee is aieie = vers eran ciotap ale iaeyarneneT 65
Bibliopraphygaemr ye ye tee ie heirs pent ebeelt terete tele peeetats 68

Bxplanation of Plates, ao .c0c1. i's ona anaes alanine eeerae 71

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7) THE NASAL ORGAN IN AMPHIBIA—HIGGINS 7

INTRODUCTION

There is considerable literature upon the development of the chondro-
cranium of the Amphibia, but only a little of it gives adequate details of the
process of chondrification of the nasal capsule in this class of vertebrates.

Parker, in a long series of extensively illustrated papers, (1871, 1876,
1877, 1881) was the first to give any adequate account of the development
of the skull in the Amphibia; but his remarks, so far as the nasal capsules
are concerned, are general and no detailed description of the parts or pro-
cesses of chondrification are given. Born (1877) gives, in considerable
detail, the process of chondrification in Triton cristatus; while Stéhr (1879)
who also described the chondrocranium of Triton, paid but slight attention
to the ethmoidal region.

Gaupp (1893) in his well known work on the cranium of Rana fusca
discusses four stages in the development of the skull of the frog, treating all
parts with more detail than any other writer. According to Miss Platt
(1897) the nasal capsule in Necturus, to a great extent, chondrifies inde-
pendently of the trabeculae; but she gives but slight account of the develop-
ment of the fenestrated roof of the capsules. Winslow (1898) dealt with
the chondrocranium of several of the Ichthyopsida, but his account of the
development of the nasal capsules has but slight detail. Peter (1898) is
the only one who has described the skull of any Gymnophione; while
Terry (1906), who followed the history of the nasal capsule of Amblystoma
through five stages, states that the process of chondrification in Amblys-
toma agrees closely with that of Triton.

The work covered by this paper was undertaken with the idea of ascer-
taining what homologies, if any, could be drawn between the nasal capsules
of the various groups of Amphibia; and to determine in how far these
structures would substantiate or alter the different classifications proposed
for this vertebrate group.

The work was done in the Zoological laboratory of the University of
Illinois, almost entirely upon the departmental collection. It was carried
on under the supervision of Professor J. S. Kingsley to whom the writer
wishes to acknowledge his sincere appreciation for the many helpful sug-
gestions and his kindly attitude during the investigation and the prepara-
tion of this paper. I wish to acknowledge my best thanks to Professor
A. C. Eyclesheimer of the University of Illinois College of Medicine, for the
loan of several of his series of slides of Necturus.

8 ILLINOIS BIOLOGICAL MONOGRAPHS

THE NASAL CAPSULES OF THE URODELA
AMBLYSTOMA PUNCTATUM

Amblystoma was selected as the basis of these studies upon the nasal
organ of Amphibia, primarily because of the larger number of stages avail-
able, as well as on account of its intermediate position among the Urodeles.
I have studied and modelled seven stages of Amblystoma, which show the
successive steps, progressive and retrogressive, in the chondrification of the
nasal capsule of this Urodele. ;

A larva 11 mm. long (Fig.1) shows but few features of a nasal capsule.
The trabeculae (¢) extend forward along the ventral margin of the fore-
. brain and in the region of the eye, each has developed a small dorsal crest,
so that in cross section it appears triangular. At this stage the trabeculae
do not unite, but each expands distally into a small rhomboidal plate, the
cornu trabeculae (cé), which supports the anterior end of the nasal organ.
In a slightly older stage, a few cartilage cells appear above the medial mar-
gin of the cornu trabeculae of the left side only (Fig. 41). These cells are
the beginning of a bar of cartilage, which develops along the medial dorsal
margin of the nasal sac, and is known in the literature as the ethmoidal
column, a term used throughout this discussion.

In a larva 20 mm. long (Fig. 2), chondrification is much more advanced.
Slightly anterior to the internal nares, medial trabecular processes have
united in the middle line to form a broad planum basale (pb), which sup-
ports the anterior end of the telencephalon. This plate is broadly concave
dorsally, its lateral margins being elevated, the result of the trabecular
crests. Its posterior margin is straight and at right angles to the axis of the”
skull, but it meets the medial margin of the trabecula in an oblique angle,
because of the converging lines of the latter. The anterior margin of the
planum basale passes into the expanded cornua trabeculorum, which lie in
practically the same plane as do the trabeculae. The cornua extend
laterally and each is concave upon its dorsal surface (Fig. 42) and supports
the anterior part of the nasal organ and the organ of Jacobson; while poster-
iorly it reaches about the level of the middle of the planum basale where its
posterior lateral angle terminates in a short caudal process. The antero-
lateral margin of each cornu is at about an angle of forty-five degrees to the
median axis of the skull.

Dorsal and parallel to each trabecula and the median margin of the
cornu of either side is an elongate rod of cartilage, the further development

9) THE NASAL ORGAN IN AMPHIBIA—HIGGINS 9

of the cartilage cells above the cornu trabeculae in the earlier stage. This
columna ethmoidalis (ce) extends posteriorly to the level of the choana,
lying medial to the olfactory organ and separating it from the forebrain.
As yet it is distinct from all other cartilage structures, although Terry
(1906) in a similar stage has described a connection of this bar with the
crista trabeculae.

In this stage is the first appearance of a cartilage roof over the nasal
organ. From the posterior tip of each columna ethmoidalis, a small plate
has chondrified laterally which partially covers the olfactory sac above the
choana. This is the beginning of the planum tectale, which in the later
stages completely covers the posterior parts of the nasal organ. In this
connection it is of especial interest to note that although the columna
ethmoidalis chondrifies from in front backward, the planum tectale arises
at the caudal limit of the column and develops anteriorly.

In the next stage (Fig. 3), several features have been added to the cap-
sule. ‘The crista trabeculae (cr ¢) is well developed and has united to the
posterior end of the columna ethmoidalis (ce), thus forming a wide trough
or cavum cranii, which supports the anterior end of the telencephalon. In
front of the crista, each trabecula inclines slightly toward the median line
to pass into the planum basale (pb), which shows but slight modifications
from the earlier stage.

As yet the dorsal and ventral parts of the capsule are almost entirely
distinct from each other, the only connection being by the crests at the pos-
terior end (Fig. 4). On the other hand, the columnae of the two sides are
connected by a narrow ethmoidal bridge (pe), which lies directly above the
anterior margin of the planum basale and is formed by medial processes
from each ethmoidal column (Figs. 4, 44).

Between this bridge and the basal plate are procartilage cells, which in a
later stage are to form, with the pons ethmoidalis, a transverse wall of
cartilage (to be described later) bounding the cavum cranii in front. Up
to this stage there is no complete separation between the cavum cranii and
internasal space, a condition which is permanent in Urodeles like Triton.

Each columna ethmoidalis is now wider than before, except at its
extreme posterior end where it joins the crista. In front of the pons
ethmoidalis, each column bends obliquely outward and forward from the
axis of the skull and ends at the level of the tip of the cornu. A little in
front of the cristal connection of trabecula and column, each column bears
a lateral process which curves down over the choana. This is the beginning
of the planum tectale (pt) forming the posterior part of the more complete
roof of the capsule in the later stage. In the literature upon the amphibian
nasal capsule, this tectal plate has been called the lamina cribosa; but from
its relation to the olfactory nerve it is evident that it is totally different
from the cribiform plate of mammalian anatomy, hence the proposal of the
name used here.

10 ILLINOIS BIOLOGICAL MONOGRAPHS {10

Another cartilage arises from the lateral side of each trabecula, behind
the choana, and the anterior margin of the cristal connection of the trabec-
culaand column. This has been called by the German writers, the palatine
process; but it has no relation to the palate or the palatine bone, and is
better called by another name, frequently used for it, the processus antor-
bitalis (pa). It extends laterally about as far as the cornu, and is destined
to form a part of the posterior wall of the nasal capsule.

As yet there are no distinct olfactory foramina, but the olfactory nerve
leaves the forebrain at right angles to its median axis and passes into the
capsule through the large gap between the trabecula and the column, just
anterior to the crista trabeculae.

In a 34 mm. larva (Figs. 5, 6)the process of chondrification which formed
the pons ethmoidalis of the 25 mm. stage, has continued ventrally and
posteriorly, so that the bridge has joined the planum basale and has extend-
ed back to about the level of the planum tectale of the previous stage.
The result of this is the formation of a large median wall to the cavum
cranii, the only openings left being the olfactory foramina which pass into
the capsules at the lateral margins of this wall. From conditions which
occur in other Urodeles this median mass is best called the planum verticale,
although it is much thicker than in Amphiuma and the Caecilians. As will
be seen in the sequel, this planum verticale may be defined as the cartilage
connecting the nasal capsules of the two sides, beginning as a median dorsal
pons ethmoidalis from the two columnae and then extending down to join
the planum basale. The anterior margin of the planum verticale (pv) is
deeply excavate, and together with the medial walls of the nasal capsule, it
bounds the V-shaped internasal space in which the intermaxillary glands
lie. The lateral margins of the verticale slightly extend over the medial
margins of the nasal organs from the olfactory foramen to the tip of the
capsule, thus forming the anterior part of the planum tectale, which is
pierced by a small opening (fn) through which the ramus nasalis internus
of the fifth nerve passes into the internasal space. Thus the planum
verticale is a compound structure formed from the ethmoidal bridge and
the columnae ethmoidales, uniting ventrally with the planum basale.

The posterior parts of the planum tectale (f#), which began in the last
stage (25 mm.), now forms a broad curved plate which covers the caudal
half of the nasal organ, and extends forward from the crista trabeculae to the
level of the anterior margin of the foramen olfactorius. Laterally it extends
nearly to the level of the gap between the caudal extension of the cornu and
the antorbital process; the posterior margin of the tectale is oblique, its
antero-lateral margin is slightly arcuate, while in front it is produced into a
small conical process (Figs. 5, 6).

The expanded cornua trabeculorum (c?) do not differ greatly from those
of the preceding stage. The lateral margin of each cornu is slightly arcuate

11] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 11

and the posterior lateral angle nearly meets the lateral margin of the tec-
tale (Fig. 5). Medially and behind, the cornu is continuous with the
planum basale, which has now extended laterally so as to form a partial
floor beneath the medial side of the olfactory sac. In all Urodeles the
produced postero-lateral angle of the cornu supports the organ of Jacobson
(vomeronasalis). This relation and also that of the organ to the lateral
part of the tectale is of great aid in determining the homologies of the more
complex capsule of the adult.

The antorbital process (pa) is now larger, forming a plate rather than a
bar, and its antero-lateral angle is directed forward as a blunt process which
nearly meets the posterior process of the cornu and also the lateral margin
of the tectale.

In the nasal capsule of a 45 mm. larva, only a few modifications need
description. The capsule (Figs. 7, 8) has not increased in length, although
there has been an appreciable increase in width and depth. With the
greater development of the olfactory lobes there has been a corresponding
increase in the size of the cavum cranii (cc). The olfactory lobes extend
forward only as far as the caudal third of the nasal sac, so that the olfactory
foramina look obliquely forward from the antero-lateral angles of the brain
case. There is a gradual change during growth in the relative positions of
the nasal sac and the forebrain. In the earlier larva, brain and olfactory
organs overlap for about half the length of the nasal sac, while in the adult
the sensory structures are almost entirely in advance of the tip of the
olfactory lobes, approximating the anuran condition.

The planum verticale (fv) of this stage is shorter than before but its
height is almost twice that of the 34 mm. larva; so that this stage marks the
beginning of the reduction of the verticale which is so much smaller in the
last stage to be described.

The only other features to note in this stage are the broadening of the
tectale, which process has brought the foramen for a branch of the nasalis
internus on to the dorsal surface of the capsule and the extension of the
antero-lateral angle of the tectale, so that it now fuses with the postero-
lateral angle of the cornu, forming the first appearance of a lateral wall to
the capsule. The naso-lacrimal duct passes over this connection between
cornu and tectale, and empties into the olfactory sac just above the
anterior end of Jacobson’s organ.

Procartilage cells are abundantly distributed over the anterior end of
each olfactory sac, the anterior naris being terminal in all larval stages.
From these cells, the anterior cupola is formed; a process which involves
the shifting of the naris to its lateral position.

In a larva near the end of metamorphosis (Fig. 9) many changes of the
capsule of the early stage have occurred. The general proportions of the
capsule remain unchanged, although there has been a further reduction in

12 ILLINOIS BIOLOGICAL MONOGRAPHS 12

the length of the planum verticale, so that one-half of the entire capsule lies
anterior to this median vertical plate. The width of the verticale is also
reduced by one-half to accommodate the lateral development of the olfactory
organs which now lie much closer together. The anterior surface is widely
concave, its dorsal margin overhanging the ventral, thus forming a partial
roof over the intermaxillary glands.

The planum ‘ectale (pt) now covers the entire dorsal aspect of the nasal

ac and extends from the region of the choana to the tip of the capsule

where it has united to the anterior margin of the cornu trabeculae, forming
the cupola (Fig. 9). This area is pierced by five small foramina. Four of
these are in an oblique quadrilateral, the fifth, much larger, lying behind
the others. Of the four, the anterior three foramina are for the branches
of the nasalis internus which are distributed to the dorsal part of the snout;
while the lateral foramen passes a branch of the profundus from the capsule.
The larger posterior gap contains no nervous structures and apparently is
the beginning of the resorption of the cartilage roof of the capsule. The
medial surface of each capsule is marked distally by a small prenasal process
(pnp) at the base of which is the foramen nasalis internus (fii), above
described. On the dorsal surface of the capsule is a sixth small foramen for
a branch of the profundus of the fifth nerve, the result as before, of the
extension of the cartilage around the nerve.

The antorbital process (pa) has now united to the lateral posterior
margin of the tectale, a condition foreshadowed by the close association of
these parts in the earlier stages, thus inclosing a large foramen between the
posterior margin of the tectale and the basal part of the antorbital. This
is the foramen orbito-nasalis (fom) into which the caudal part of the nasal
sac extends, and through which the nasalis internus of the fifth nerve enters
the capsule. Lateral to this foramen, the united elements of the antorbital
and tectale are directed obliquely forward, covering the lateral aspect of the
olfactory organ. A branch of the profundus nerve and a blood vessel
pierce this plate by two foramina just posterior to its connection with the
caudal] extension of the cornu trabeculae (Fig. 9).

As in the earlier stages, the organ of Jacobson rests upon the caudal
extension of the cornu which extends more posteriorly, and has partially
united to the fused tectale and antorbital. This union of the cornu to the
posterior tectale has resulted in the formation of a new foramen, the infra-
conchalis of Gaupp (fez 7c), through which the anterior part of the organ of
Jacobson extends to the laterally enveloping tissue (Fig. 46, jo). Thus
this organ rests upon a shelf formed by the cornu trabeculae, while its
anterior end extends through the foramen. This infra-conchalis is separ-
ated from the large lateral narial opening by the bar, which in the 45 mm-
larva connects the cornu trabeculaeand the tectale. A deep groove occur-
in the lateral wall of the planum tectale which leads to the posterior bound-

13] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 13

ary of the external naris, along which the naso-lacrimal duct passes to the
olfactory organ (Fig. 45 /d).

This stage represents the highest development of the cartilaginous
capsule in Amblystoma. The nasal organs are completely encased in
cartilage, except for the external and internal narial openings. In the
later stages studied, and in the early adult capsule, conspicuous gaps have
formed through the process of resorption, giving way to the various mem-
brane bones that enclose these sensory structures in the adult. That the
completeness in the development of the capsule, which has been attained in
this stage, is in some way associated with metamorphosis, is very evident,
and it probably represents the end of the larval period.

The cartilaginous capsule of the adult Amblystoma (Fig. 10) results by
reduction and specialization of structures present in the stage just des-
cribed. Increase in the size of the sensory structures necessitates a capsule
of enlarged dimensions, although the proportions-are relatively the same.
The planum verticale is reduced to a narrow bar which is relatively more
posterior in respect to other capsular parts; its anterior ventral surface is
deeply excavate, the dorsal surface covering the intermaxillary gland to a
greater extent than before.

Strikingly characteristic of the adult cartilaginous capsule is the large
five-sided gap in the roof which completely exposes the dorsal surface of the
nasal organ. This gap is the result of the further resorption which just
began in the last larval stage described. From its point of origin oppo-
site the verticale in the planum tectale, resorption has extended anteriorly,
laterally and posteriorly, until all that now remains of the complete carti-
lage roof is a slender bar of cartilage, the dorsal process of Winslow, uniting
the anterior cupola with the lateral wall of the capsule. Posterior to the
verticale, a narrow bar, a remnant of the ethmoidal column, passes over the
foramen olfactorius and connects with the posterior tectale which now is
reduced to a narrow band of cartilage. Lateral to the foramen orbito-
nasalis (fon) the tectale broadens slightly, and curving obliquely forward
forms a partial roof over the choana and lateral parts of the nasal sac
(Figs. 47, 48). More laterally this roof, better known as the lamina
externa (/e), is pierced by three foramina, for a blood vessel and two branch-
es of the externus profundus nerves.

The caudal extension of the cornu trabeculae is more posterior than
before, and a transverse section through the planum verticale shows the
posterior end of the organ of Jacobson lying between the cornu and the
lateral part of the tectale (Fig. 47). The fenestra infra-conchalis (fem ic)
is more elongate and contains the anterior end of Jacobson’s organ (Fig. 48,
jo), which medially is partially covered by a part of the cartilage of the tectale
which supports the naso-lacrimal duct. From this, a cylindrical bar of
cartilage, the dorsal process, extends to the cupola, affording the only

14 ILLINOIS BIOLOGICAL MONOGRAPHS [14

covering to the nasal sac in this region, and which at the same time forms
the medial boundary to the external naris. The small band of cartilage,
which in the 45 mm. larva connected the tectale to the cornu trabeculae,
persists as a flat plate separating the narial opening from the fenestra infra-
conchalis, and is pierced by a small foramen for the externus branch of the
profundus nerve as it passes to the exterior.

Anterior to the planum verticale, a band-like cartilage, the lamina
medialis (/m) continues forward to the cupola. It is pierced by a single
large opening at the base of the prenasal process through which the nasalis
internus of the profundus passes to the internasal space.

In the larva of Amblystoma there is, first, a progressive development
which results in a well chondrified nasal capsule, reaching the extreme in the
oldest larval stage. With the assumption of adult conditions and the more
extensive development of bony structures, this capsule undergoes a marked
reduction, chiefly by the resorption of parts. Evidently there is some
relationship between the development of the cartilage capsule and the
period of metamorphosis, the significance of which will be discussed later.

SALAMANDRA MACULATA

In a larva of Salamandra maculata 25 mm. long (Fig. 11), the nasal
capsule has chondrified to a stage intermediate between that of the 25 mm.
and 34 mm. Amblystomal larvae. The cristae trabeculorum (cr ¢) termi-
nate abruptly just anterior to the region of the eye, from whence the
trabeculae pass forward a short distance and then unite to form a broad
trapezoidal planum basale (pb). The posterior margin of the planum is
parallel to and one-half longer than the anterior, and bears a strong caudal
process (cp), which Parker has called the hinder process, lacking in all other
stages and in all Urodeles which I have studied, with the exception of a
single stage of Cryptobranchus. The dorsal surface of the planum is more
concave than that of the corresponding stage of Amblystoma and the
ridges formed by the trabeculae are more prominent.

A broad trabecular cornu (ct) arises from the antero-lateral angle of the
planum basale as a thin triangular cartilage, which supports the anterior
part of the nasal sac. The lateral margin of each cornu is oblique to the
axis of the skull and meets the posterior margin at the level of the anterior
boundary of the planum basale; more medially the posterior margin curves
backward and fuses with the lateral margin of the planum basale near its
middle.

Parallel to each trabecula, and lying adjacent to the dorsal medial
margin of each nasal sac, is the columna ethmoidalis (ce). In this stage of
Salamandra, each ethmoidal column is united to the medial margin of the
cornu, before the pons ethmoidalis appears; and this fact suggests that the
columna does not arise independently here, but is a development back-

15] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 15

wards from the anterior cornu, just as in Spelerpes. At its posterior end a
small process, the beginning of the planum tectale, extends laterally and
then bends ventrally over the hinder end of the nasal sac at the level of the
choana; this planum tectale arising here as in Amblystoma from an out-
growth from the columna ethmoidalis. A small groove between the
anterior tip of the cornu trabeculae and the columna ethmoidalis allows for
the passage of the nasalis internus branch of the profundus nerve to the
internasal space (ims).

An antorbital process (pa) arises from the latero-ventral margin of each
trabecula and extends laterally a short distance and anteriorly to a point in
line with the caudal margin of the planum basale.

In a 38 mm. larva, the nasal capsule is similar in many ways to that of
the 45 mm. Amblystoma. The capsule has doubled in size and chondri-
fication has advanced in all parts, so that the olfactory organs are now
more completely protected. Each crista trabeculae has united to the
posterior end of the ethmoidal column, forming a lateral wall to the cavum
cranii, interrupted only by an oval foramen olfactorius (fo) for the olfactory
nerve.

The planum basale (pb) resembles that of the earlier stage, but has now
completely lost the hinder process, so that the posterior margin is semi-
circularly excavate as in the 45 mm. Amblystoma.

In a manner similar to that of the 25 mm. Amblystoma, an ethmoidal
bridge has formed uniting the columnae ethmoidales of the two sides.
This represents the beginning of the planum verticale which in the later
stage completely closes off the internasal space from the cavum cranii, now
in continuity by means of the circular fenestra ethmoidalis (Fig. 54, fen eth).
The dorsal surface of the rudimentary verticale is flat, continuous with the
dorsal margins of the ethmoidal columns; its anterior margin bears a
triangular cephalic process (ce p) projecting into the internasal space and
partially covering the intermaxillary gland, so that a sagittal section of the
verticale appears triangular.

A lateral chondrification from the entire length of the ethmoidal column
now forms a broad planum tectale (pt), which covers the nasal organ
throughout its entire length. Anteriorly the tectale has united with the
tip of the cornu trabeculae, forming a complete cupola (c), which is con-
tinuous with the verticale and is pierced only by a single foramen for the
nasalis internus of the profundus nerve. The lateral margin of the anterior
part of the tectale is separated from the lateral margin of the cornu by the
large oval narial opening, which lacks the deep fenestra narina of the
corresponding stage of Amblystoma; but similar to Amblystoma, the pos-
terior tectale unites by a small band of cartilage to the cornu, near its
posterior prolongation, which supports the organ of Jacobson. The naso-
lacrimal duct passes over this bar and is formed from two branches, which
come from the inner angle of the eye.

16 ILLINOIS BIOLOGICAL MONOGRAPHS [16

From the ventral surface of the anterior cupola (c), a small prenasal
process arises near the foramen nasalis internus and extends downward a
short distance into the enveloping tissue. The antorbital processes (pa)
are much as before, but as yet do not meet the anterior part of the floor of
the capsule.

There are some resemblances between the nasal capsules of the last
larval Amblystoma (Fig. 9), and the third stage of Salamandra (Fig. 13).
In both the planum basale and verticale are greatly reduced and the olfac-
tory organs lie well anterior to the forebrain. Complete chondrification of
the verticale in Salamandra has obliterated the fenestra ethmoidalis, so that
internasal space and cavum cranii are no longer continuous. The anterior
cephalic process (ce p) of the verticale is cylindrical and more elongate than
before and extends forward nearly to the level of the base of the prenasal
process. I have not observed this structure in any other Urodele.

Each antorbital process has grown forward beneath the lateral margin
of the tectale, and has united to the caudal extension of the cornu, thus
outlining two large fenestrae. Of these, the largest lies in the floor of the
capsule and surrounds the choana; while the orbito-nasal foramen (fom)
is posterior and lies between the posterior margin of the tectale and the
processus antorbitalis. In this stage the lateral margin of the tectale has
not united to the antorbital process, although they lie very close, so that no
fenestra infra-conchalis exists; but Jacobson’s organ lies between these
parts as in Amblystoma.

The anterior dorsal surface of the tectale is pierced by four foramina,
the medial three of which conduct rami of the nasalis internus of the pro-
fundus nerve from the capsule; its main branch passing to the foramen
nasalis internus at the base of the prenasal process. The lateral and larger
gap represents in Salamandra the beginning of resorption, which has been
described in a corresponding stage of Amblystoma. Posteriorly the tectale
is pierced by a small foramen for a branch of the profundus.

This stage of Salamandra is very similar to the last larval stage of
Amblystoma, and also represents the culmination of larval development.
Resorption has begun and the capsule of the adult would probably be
conspicuously reduced by the growth of the covering bones. Salamandra
differs from Amblystoma in the complete separation of the tectale from the
antorbital, and the consequent absence of the fenestra infra-conchalis;
however the approximation of these parts would suggest their connection
in the adult. The ethmo-palatine of Parker is the antorbital process, and
he says that in the adult it is very likely to fuse with the anterior parts of
the capsule. Furthermore Parker has described in the adult the persistence
of the prenasal processes and the median rostrum, and says that they seem
to be the non-segmented rudiments of the paired and unpaired elements of
the foremost visceral arch, whose splints are the premaxillaries. This

17] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 17

median rostrum is not present in any other Urodele, although prenasal
processes do exist in almost all types. Parker’s homologies are hardly
borne out by our present knowledge.

TRITON CRISTATUS

The nasal capsule of Triton cristatus differs in several points from that
of either Amblystoma or Salamandra. In the younger of the two larvae
accessible (28 mm.), the chondrification of the capsule is far advanced and
I know nothing, except by inference, of the earlier stages. At this stage
(Fig. 16) the capsule is somewhat rectangular in outline, gradually tapering
toward the anterior end. The cristae trabeculorum (cr t) are well developed
and form with the trabeculae, the walls of the cavum cranii, pierced only
at their anterior margins by the large circular olfactory foramina (fo).

Immediately in front of the crests, the trabeculae are united by a very
short planum basale (pb), which supports the olfactory lobes and the pos-
ior part of the intermaxillary glands; the latter, in this form, extending
backward beneath the anterior part of the brain. The planum basale in
Triton is very much smaller than that of Amblystoma, and lies more
posterior in respect to the other capsular parts. Dorsal to, and somewhat
anterior to the planum basale is a bar of cartilage which unites the capsules
of the two sides just in front of the olfactory foramina. This is the pons
ethmoidalis (pe), and is developed by medial growths from the dorsal part
of both capsules, much as in Amblystoma to which it bears a resemblance.
Unlike Amblystoma, however, the pons is never united to the basale by
the planum verticale; but throughout life it is separated from it by a large
circular fenestra ethmoidalis (fen eth) so that internasal space and cavum
cranii are separated from each other by membranous structures only.

In contrast to the larval stages of most other Urodeles, the nasal organs
of Triton are almost entirely anterior to the forebrain, so that planum
basale and pons ethmoidalis are close to the posterior parts of the capsule.
As a result of the relation of the central nervous system to the nasal struc-
tures, each capsule appears as a segment of an elongate cone, obliquely
truncate anteriorly, with the anterior half of its lateral wall interrupted by
a very large narial opening. As is true for all Urodeles, the cartilage
structures of each side, in front of the planum basale, are separated by an
internasal space (the intermaxillary room of Born, 1877). which in Triton
is more elongate and extends between the walls of the anterior two-thirds
of the capsule.

Anterior to its junction with the crista trabeculae, each planum tectale
(pt) curves outward and downward, completely covering the posterior
parts of the nasal sac and the choana; laterally it continues into the lamina
externa which covers the posterior part of the organ of Jacobson. More
posteriorly, each lamina externa has united to the anterior prolongation of

18 ILLINOIS BIOLOGICAL MONOGRAPHS {18

the antorbital process, thus completing the foramen orbito-nasalis (fom)
through which the nerves of the nasal region enter the capsule. A small
foramen in the tectale, just opposite the pons ethmoidalis conducts a
branch of the profundus nerve from the capsule; while the larger oval gap
in the anterior tectale, separated from the external naris by a narrow bar is
one of the gaps described by Born in the adult.

The lamina medialis (/m) forms the medial wall of the capsule, anterior
to the foramen olfactorius, and is continuous with the tectale and the cornu
trabeculae (Fig. 56),thus bounding the internasal space. The floor of the
capsule is formed by a large trapezoidal cornu trabeculae which extends
back to the level of the pons ethmoidalis where it forms the anterior margin
of the choana. Its lateral margin unites to the lamina externa, forming the
boundary to the naris, over which the naso-lacrimal duct passes to the nasal
sac, asin Amblystoma and Salamandra. Posterior to its junction with the
lamina externa, each cornu terminates in a small posteriorly-directed pro-
cess, which supports the organ of Jacobson; although, as in Salamandra, a
fenestra infra conchalis does not yet exist. At the anterior end, the floors
of the two capsules approach each other, and at the extreme medial tip of
each is a small prenasal process (pup), probably the homologue of that
structure in both Amblystoma and Salamandra. The nasalis internus of
the profundus nerve leaves the capsule through the foramen at the base of
the prenasal process.

The nasal capsule of the older larva of Triton cristatus (35 mm. long) is
intermediate between the 28 mm. stage and that described by Born (1877),
in which large gaps have developed. In this stage there has been a reduc-
tion in the length of the capsule, most of which occurs at the anterior end,
so that the width is greater in proportion to the length than in the earlier
larva. The relation of the forebrain to the nasal sac is much as before;
but in the adult, according to Born, all olfactory structures are entirely
anterior to the central nervous system. The planum basale and the pons
ethmoidalis are much as in the earlier stage, except that the pons is now
much farther anterior than is the basale, while the foramen olfactorius and
ethmoidalis are larger than before (Fig. 17).

Cartilage has formed around the branch of the profundus nerve which
supplies the organ of Jacobson, cutting off a smaller foramen adjacent to
the foramen orbito-nasalis (Fig. 17, 57). Just anterior, and slightly
lateral to this foramen, the lamina externa has united to the caudal exten-
sion of the cornu trabeculae thus outlining the foramen infra-conchalis, as
in Amblystoma, through which the organ of Jacobson protrudes from the
capsule.

Further description of this capsule is unnecessary, with the exception
of the cupola (c), which now encloses the anterior parts of the nasal sac, so
that now the external naris is entirely lateral. The lamina medialis (/m)

19] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 19

is pierced by a small foramen for a branch of the nasalis internus of the
profundus nerve, the main part of which leaves the capsule through the
foramen in front of, and at the base of the prenasal process. At the anter-
ior end of the floor of the capsule is a small gap which I believe to be the
beginning of the larger gap described by Born for the adult. @

It is impossible to be certain of all the homologies between the nasal
capsule of Triton and that of Amblystoma, without the early stages. Born
(1877) has described the process of chondrification, but has shown no figures
for his early stages. Terry (1906) says: “The development of the cartilag-
inous nasal skeleton of Amblystoma is comparable in many respects with
the processes in Triton as described by Born.” Born says nothing of an
ethmoidal column which chondrifies independently and then later becomes
associated with the trabecula; on the contrary he says: “Bei den Tritonen
die Knorpelkapseln der Nasenhéhlen durch directes auswachsen der
Trabecel gebildet werden.’’ The lamina medialis, planum tectale and
lamina externa would thus be formed by a continuous growth from the
trabecula; while the many gaps in the capsule would arise by interruptions
in the process.

_ Throughout its development, Amblystoma never has a fenestra eth-
moidalis completely outlined, and yet it is distinctly present in both stages
of Triton; and Born says: “Dieser Internasalraum ist bei Triton cristatus
und taeniatus, niemals durch eine knorpelige Wand von der Schidelhéhle
geschieden, sondern immer hautig gegen dieselbe abgeschlossen.”’

In larvae of Salamandra, Pelobates and Rana, the fenestra ethmoidalis
is complete, being bounded by cartilage upon all sides, but is closed in the
adult; while it persists throughout life in Triton and Diemictylus.

DIEMICTYLUS VIRIDESCENS

The nasal capsule of a 38 mm. larva of Diemictylus viridescens resembles
in many ways that of the 35 mm. Triton cristatus. In both, the two cap-
sules are united by a very small planum basale, the only connection between
them even in the adult Diemictylus, which lacks the pons ethmoidalis;
so that internasal space and cavum cranii are continuous cavities. The
small planum basale (pb) supports the anterior part of the telencephalon
which reaches forward into the internasal space; so that olfactory lobes and
intermaxillary glands overlap in this animal (Figs. 14, 53).

The antorbital process (pa) has united to the posterior margin of the
tectale at two places, thus outlining two small fenestrae the inner of which
is the foramen orbito-nasalis (fo 7) for the nasalis internus of the profundus
nerve; while the outer conducts the externus branch of the profundus,
which supplies Jacobson’s organ.

Anterior to these foramina, the united elements of the planum tectale
and the antorbital process completely cover the dorsal and lateral parts of

20 ILLINOIS BIOLOGICAL MONOGRAPHS (20

the olfactory organ; and together with the posterior prolongation of the
cornu form a shelf upon which the posterior parts of Jacobson’s organ rest.
Slightly anterior to its junction with the cornu, the tectalesis pierced by a
small circular foramen, which, like the infra-conchalis of Amblystoma and
Triton, contains the anterior end of the organ of Jacobson. The planum
tectale is interrupted on its anterior half by two oval openings, of which the
external naris is the larger, extending back nearly to the middle of the cap-
sule. The more medial gap is much smaller and marks the beginning of the
process of resorption, just as in the older Triton larva.

The lamina medialis (/m) is continuous with the tectale and forms the
medial wall of the capsule from the planum basale to the anterior cupola;
while ventrally, it curves into the floor of the capsule which is pierced by
two small foramina, through which rami of the nasalis internus nerve
leave the capsule. The main branch of this nerve passes to the internasal
space through the larger foramen just in front of the base of the pre-nasal
process.

The adult Diemictylus (Fig. 15) shows no further chondrification of
structures than those present in the larva. Ossification has taken place in
all parts and further resorption has increased the size of the gaps present
in the earlier stage. A single foramen exists above the antorbital process,
so that both nasalis internus and externus of the profundus nerve enter the
capsule through the foramen orbito-nasalis.

The planum tectale is more vaulted than before, and its posterior half
is pierced by two foramina; the medial of which is for a branch of the pro-
fundus nerve, while the lateral and larger one contains, as before, the
cephalic end of Jacobson’s organ. The anterior tectale has two large
openings, the external naris, lateral in position, and, medial to this, the
further development of the gap begun by resorptive processes of the larva.

The ventral surface of the adult capsule has a greatly enlarged choana,
which occupies the posterior two-thirds of the floor. It is bounded laterally
by the prolongation of the cornu, which in this stage extends beyond the
junction to the tectale, so that a short process, behind the shelf, supports
the posterior parts of the organ of Jacobson. The anterior part of the floor
and the cupola need no description, further than the mention of five small
foramina for branches of the nasalis internus nerve.

The nasal capsules of Triton and Diemictylus are very close. The
presence of the same large gaps, and the reduced planum basale, together
with the continuity of cavum cranii with the internasal space are strong
resemblances between the two. The fenestra ethmoidalis is not a perma-
nent character of any other adult, although it is temporary in some larvae
as Salamandra and certain Anura. There are some resemblances between
the capsules of the adult Amblystoma and Diemictylus. In both, the
anterior part of the organ of Jacobson extends through a foramen which in

21) THE NASAL ORGAN IN AMPHIBIA—HIGGINS 21

Amblystoma is called the infra-conchalis, separated from the naris by a
cartilage bar; while the posterior part of Jacobson’s organ rests upon a
shelf formed by the prolongation of the cornu. The orbito-nasal foramen,
the choanal opening, and the relation of the olfactory organ to the capsule,
are features common to both Amblystoma and Diemictylus; and yet the
absence of a planum verticale, the greatly reduced planum basale and the
complete continuity of internasal space with cavum cranii in the latter
form, preclude the determination of close relationships here.

CRYPTOBRANCHUS ALLEGHANIENSIS

Practically no work has been done upon the development of the skeleton
in the larval stages of Cryptobranchus, although the adult skull and nasal
structures have been described by Parker (1876), Wiedersheim (1877), and
Wilder (1892). I have studied four stages in the chondrification of the
nasal capsule, and although my material lacks some intermediate steps in
the process, yet I am able to recognize the method of development and to
note some features that may prove interesting from a phylogenetic point
of view.

The early process of chondrification in Cryptobranchus is similar to
that in Amblystoma, and my earliest stage suggests the eleven mm. larva
of that animal with certain additional features. In a larval Cryptobran-
chus two weeks after hatching (Fig. 22), a nasal capsule has not yet formed.
The cristae trabeculorum (cr ¢) are very strong and high, but terminate
abruptly near the anterior margin of the eye; while the trabeculae continue
anteriorly, turning slightly medially but not meeting to form the planum
basale. Each is curved upon its medial surface, which rests against the
olfactory lobe; while anteriorly a ventral lateral expansion of the trabecula
is the beginning of the cornu (ct), which resembles Amblystoma, and ends
in a blunt process in the surrounding tissue.

In contrast to the eleven mm. Amblystomal larva, trabecular crests
are well developed in this stage of Cryptobranchus; while on the other
hand, the cornua trabeculorum which are well developed in the young
Amblystoma are just beginning to chondrify in Cryptobranchus. Antor-
bital processes have not formed, nor is there any trace of an ethmoidal
column as in the youngest Amblystoma.

In a larva five weeks after hatching (Fig. 23), chondrification has ad-
vanced in all parts, but the absence of an intermediate stage prevents a
definite conclusion as to the origin of certain structures. In general the
capsule resembles in many respects that of the 25 mm. Salamandra.

From the anterior end of the crista, each trabecula inclines toward the
median line for a short distance, and then passes straight forward and is
united with its mate by a small planum basale (6) similar in size to that in
Triton cristatus. This planum basale differs from that of any Urodele thus

22 ILLINOIS BIOLOGICAL MONOGRAPHS [22

far described, in the fact that the dorsal surface is not concave but is convex
and bears upon its anterior half a distinct median swelling which probably
is the beginning of a planum verticale (Fig. 58). The anterior surface is
straight and at right angles to the median surface of the skull, while the
posterior possesses a short caudal process similar to that in the 25 mm.
Salamandra larva.

Anterior to the planum basale, each trabecula extends forward a short
distance and from its medial margin a columna ethmoidalis (ce) arises
dorsally as a broad band of cartilage, partially separating the anterior
part of the nasal sac from the internasal space. Passing backwards, up-
wards and outwards along the dorsal medial side of the olfactory organ,
each column becomes more rod-like; and at the level of the anterior margin
of the planum basale it expands into a large rhomboidal plate, the planum
tectale (pt) which extends forwards and outwards, covering the dorsal and
lateral parts of the nasal sac. Each tectale is pierced by a small foramen
through which a branch of the profundus nerve passes from the capsule.
Posterior to the tectale, each column continues backward and unites to the
crista trabeculae.

The cornu trabeculae (ct) of Cryptobranchus differs from that of any
other Urodele. In contrast to the board triangular plate of both Ambly-
stoma and Salamandra, it is reduced to a narrow bar, which curves back-
wards and upwards from the lateral anterior margin of the trabecula to a
point just below the tectale, to which it fuses in a later stage. A small
notch at the anterior end of the capsule, between the ethmoidal column
and the cornu allows for the passage of the nasalis internus nerve to the
internasal space.

From each trabecula, just posterior to the large foramen olfactorius, a
slender process passes laterally a distance equal to the width of the trabe-
cula, and then bends abruptly to pass backward to the pterygo-quadrate,
while it utterly lacks any anterior prolongation. The morphological
relations of this bar will be discussed in connection with a later stage.

In a larva two months after hatching, a more complete capsule has
formed. The planum basale has lost the hinder process and is now con-
tinuous with the planum verticale, which unites the two capsules just
anterior to the oval olfactory foramina and completely separates the
cavum cranii from the internasal space. Anterior to the verticale, the
columna ethmoidalis and cornu trabeculae have expanded to form the
lamina medialis covering the entire medial surface of the nasal organ. A
notch, marking the junction of column and cornu, allows for the passage of
a branch of the nasalis internus to the internasal space.

The planum tectale is considerably larger than before, reaching back to
the crista and extending forward over the posterior tip of the cornu trabe-
culae, with which it is not yet united. It is pierced by a small foramen as

23] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 23

in the earlier stage. A wide bay, the fenestra narina, marks the anterior
boundary of the tectale, and here, as in Amblystoma, is a larval character,
disappearing in the adult. The cornu trabeculae is somewhat wider than
before, although differing considerably from the broader cornua of other
Urodeles. A small notch at the anterior end of the cornu conducts a
second branch of the nasalis internus from the capsule.

In the last stage of Cryptobranchus studied, a larva three months old
(Fig. 24), chondrification has advanced in all parts, forming a well-defined
nasal capsule, resembling in some respects the 45 mm. Amblystoma. The
planum basale and verticale are much as before, supporting the olfactory
lobes, and uniting the capsules of the two sides just anterior to the olfactory
foramina. Anterior to the planum verticale, the lamina medialis (/m)
formed by both ethmoidal column and trabecula, together with the cornu
forms the anterior cupola of the capsule, which is pierced by two foramina,
one medial and the other ventral, through which the branches of the
nasalis internus nerve leave the capsule. The olfactory duct continues
forward beyond the lateral margin of the cupola and opens through the
external naris, anterior to all capsular structures.

The cornu trabeculae is much as in the earlier stage, except that it has
now united to the anterior extension of the planum tectale, just as in all
other Urodeles thus far described; and the organ of Jacobson rests upon the
caudal extension of the cornu behind this connection. The tectale itself
is larger than before, reaching forward a short distance beyond its junction
with the cornu, thus completely covering the choana and the dorsal parts
of the nasal sac. The fenestra narina is deeper than before, extending
back from the naris to the planum verticale. A branch of the superficialis
nerve enters and leaves the capsule through this bay; but in a later stage,
cartilage has chondrified around these nerves leaving two small foramina,
and completely obliterating the narina, as in the last larval stage of
Amblystoma.

In this stage, the bar of cartilage mentioned in connection wth the five
weeks larva as extending at right angles from the side of the trabecula, has
attained such relations as to throw light upon its morphology. At its tip
it is directly connected with the anterior end of the pterygoquadrate bar,
which extends back to the otic region where the relations are much the same
as in all Urodeles. This completeness of connection of the pterygoquad-
rate with the anterior parts of the trabecula is paralleled, so far as I know,
only in the Siberian genus Ranodon (Wiedersheim 1877, Fig. 69), and is
lost in the adult of Cryptobranchus, both our species and the Japanese
japonicus.

Some years ago, Gaupp questioned a statement by Kingsley (1892,
p. 672), who said: “the lower process may retain the name ‘antorbital’,
usually applied to it, for Amphiuma presents no evidence that it is the

24 ILLINOIS BIOLOGICAL MONOGRAPHS [24

palatine cartilage as Gaupp interprets it.”” Gaupp (1893, footnote p. 430)
says: “Hierzu méchte ich bemerken, dass ich die beiden Namen ‘Antor-
bital-fortsatz’ und ‘Cartilago palatina’ durchaus fiir dasselbe Gebilde
gebraucht habe (17, p. 115: ‘die Cartilago palatina’ oder wie die englischen
Autoren Huxley und Parker den Knorpel nennen, den ‘Processus antor-
bitalis’). Als ‘Processus palatinus’ wird der Knorpel aber z.B. von
Friedreich und Gegenbaur bezeichnet (14, p. 29), auch Hertwig (24) nennt
ihn auf den Figuren ‘Cartilago palatina’ (C.p.), und Wiedersheim (58, p.
483) spricht von einen Antorbitalfortsatz oder ‘Gaumenfortsatz’ der
deutschen Autoren. Da ich beide Bezeichnungen in der Literatur vorfand,
so erwihnte ich sie auch beide, habe aber nicht etwa einem bekannten
Gebilde eine neue Deutung geben wollen. Kingsley scheint unter ‘Palatine
cartilage’ hier etwas Besonderes zu verstehen; was das ist, kann ich aus
seinen Angaben nicht ersehen.”

Winslow (1898) discussed the question, and concluded that until it was
shown that the process in Urodeles arising from the trabecula in front of the
orbit was actually a part of the pterygoquadrate the name antorbital
should be retained. A further point is that the term palatine cartilage is
misleading, implying that it is the rudiment of the palatine bone, which is
not cartilaginous in origin.

With the evidence now presented by Cryptobranchus, it would seem as
if the basal part of the process here, and by implication in all Urodeles, is
really an anterior prolongation of the pterygoquadrate. But the anterior
portion of this process is something additional, and although possibly
pterygoidal in origin, may retain the name antorbital. Then in all other
groups, where the posterior connection to the quadrate is lost, the entire
outgrowth, although partly pterygoidal, is best known as the antorbital
process. Of course this retention of the anterior part of the pterygoid in
both Cryptobranchus and Ranodon larvae is an ancestral feature lost
elsewhere among the Urodeles. As stated in the above, the adults of both
species of Cryptobranchus have lost the connection of the pterygoid with
the side of the cranial wall, and in both the direction of the posterior
plainly pterygoidal part of the cartilage would not suggest that in the larva
there was any such connection with the trabecula or any relation with the
palatine bone.

Of the Urodeles thus far described, Cryptobranchus stands alone in the
origin of the planum verticale, which arises as a medial dorsal growth from
the planum basale, subsequently uniting to the medial margins of the
columnae ethmoidales and closing off the cavum cranii from the internasal
space. Thus at no time does a pons ethmoidalis or a fenestra ethmoidalis
exist in Cryptobranchus, like that in Amblystoma and Salamandra. On
the other hand the columna ethmoidalis in Cryptobranchus recalls that
structure in Salamandra which, arising in both from the medial margin of

25] THE NASAL ORGAN IN AMPHIEBIA—HIGGINS 25

the cornu, grows posteriorly along the nasalsac. Unlike Salamandra, how-
ever, the planum tectale does not develop from the posterior end of the
ethmoidal column, but rather chondrifies laterally from about its middle.

Although the planum tectale and the anterior cupola of my later stage
resembles in some ways those of both Salamandra and Amblystoma yet the
large planum basale and cornu trabeculae of the latter forms, do not exist
at any time in Cryptobranchus, both of these structures being greatly
reduced.

SPELERPES BILINEATUS

The nasal capsule of a Spelerpes larva 15 mm. long (Fig. 18) differs but
little from those of the early stages of all Urodeles. The trabeculae (¢) are
more cylindrical than in Amblystoma, however, and extend forward to the
tip of the forebrain, not meeting as yet to form the planum basale. At
their anterior ends, each trabecula expands into a triangular cornu, con-
siderably smaller than the cornua of corresponding stages of Amblystoma,
and, which only partially supports the anterior part of the nasal organ
(Fig. 59). Ethmoidal column nor crista trabeculae have not appeared in
this stage.

In a 37 mm. larva (Fig. 19) other parts of the capsule have chondrified,
but on the whole the capsule is far more simple than any other Urodele of
that age. The cristae trabeculorum (cr f) are well developed and together
with the trabeculae form the walls of the cavum cranii. Each crista
terminates at the level of the antorbital process, and from its dorsal margin
a short process extends anteriorly, which appears to be associated with the
development of the ethmoidal column, as described in the later stage.

From its junction with the crista, each trabecula inclines toward the
median line and is united with its mate by a small planum basale (9d),
convex upon its dorsal surface and resembling this structure in the second
stage of Cryptobranchus. Just anterior to the planum basale the trabe-
culae are strongly concave and a prominent ridge has developed along their
medial margins, forming a groove for the branches of the nasalis internus
of the profundus nerve (Fig. 60). The trabecular cornu is well developed
in this stage; its posterior margin extending backwards as a short process
to the level of the anterior margin of the planum basale.

The antorbital processes (pa) are much as in others of the order, arising
from the trabecula just beneath the crista, extending laterally a short
distance, and then bending anteriorly toward the capsule.

My oldest stage of Spelerpes is a larva 46 mm. long (Fig. 20). Some
additional structures are present, but the capsule is not completely developed
and satisfactory comparisons with the capsules of other Urodeles can
not be made.

Opposite the eye, the cristae trabeculorum (cr ¢) are low; but farther
forwards they are higher, their anterior ends being free from the lower

26 ILLINOIS BIOLOGICAL MONOGRAPHS [26

trabecula and reaching farther forward than before (Fig. 21). Anterior
to the crista, each trabecula turns more abruptly toward the median line for
a short distance, and then anteriorly; uniting by a very small planum bas-
ale, which in this stage is flat and level, with the dorsal surfaces of the
trabeculae.

Anterior to the planum basale, the trabeculae continue forward, sep-
arated from each other by a narrow internasal space; each expands distally
into a small cornu which supports the tip of the nasal organ. Arising from
the dorsal and medial margin of each trabecula, just anterior to the planum
basale, is a small process which extends backward a short distance along the
medial margin of the nasal sac. This process is the further development
of the medial ridge of the trabecula in the 37 mm. stage; and from its
relation to the nasal organ, it must be the beginning of the columna
ethmoidalis, whose further history is unknown (Fig. 61).

I regret that I have no older stages showing the farther chondrification
of the capsule; thus preventing a careful comparison with other Urodeles.
In general, however, Spelerpes seems to indicate a retarded growth in all
parts. In corresponding ages of other Urodeles, there is a much more
complete capsule than in Spelerpes.

I have not observed the free anterior extension of the crista in any
other Urodele, with the exception of Amphiuma; and judging from its
relation to the nasal organ and trabecula, it would appear as though this
process is the posterior beginning of the ethmoidal column. In other
words the columna ethmoidalis in Spelerpes may arise by the fusion of two
parts independent of each other; the anterior part from the medial margin
of the cornu, the posterior part from the anterior margin of the crista. In
no other Urodele, as far as I have seen, does the column arise in just this
way; however the early development of the crista trabeculae in Crypto-
branchus and the lateral development of the tectale from the middle of
the ethmoidal column, ledds me to conclude that in Cryptobranchus the
column arises, as in Spelerpes, from two distinct independent outgrowths.

The small planum basale is similar to that in Cryptobranchus, but the
larger cornu in the 37 mm. stage is more like that of Amblystoma. My
material does not show the formation of the planum verticale, but it
evidently does not arise as a dorsal growth from the planum basale, but
more probably by medial growths from the ethmoidal columns; thus in
this particular, approaching the condition in Salamandra.

The complete absence of intermaxillary glands, the close approxima-
tion of the capsules anterior to the planum basale, as well as the small size
of the latter, are points of similarity to Cryptobranchus, which, on the
evidence of larval characters alone, I believe Spelerpes more closely resem-
bles.

27) THE NASAL ORGAN IN AMPHIBIA—HIGGINS 27

PLETHODON ERYTHRONOTUS

Winslow (1898) has described the nasal capsule of a 20 mm. larva of
Plethodon glutinosus, and he compares it with a 45 mm. Amblystoma. I
have not studied any larval form of this genus, but have examined and
modelled the capsule of an adult, which is similar in many respects to my
last stage of Amblystoma. In the adult, ossification is extensive and in
some parts, all traces of a chondrocranium have disappeared. This is
especially true in the region of the eye, where the trabecular crests have
disappeared as far forward as the olfactory foramina, so that these open-
ings are confluent with the foramina orbito-nasales in this stage (Fig. 27).

' The dorsal surface of the nasal organ is exposed throughout its entire
length by a large gap in the capsule, similar to that of the adult Amblys-
toma; so that the planum tectale is reduced to a small cartilage plate
covering the posterior end of the nasal sac behind the choana. The lamina
externa (Je) formed by elements of the tectale and processus antorbitalis,
passes obliquely forward as a band of cartilage, protecting the lateral parts
of the nasal sac and the organ of Jacobson (Fig. 62). The nasalis externus
of the profundus nerve enters the capsule through a small foramen in this
plate, and is partly distributed to Jacobson’s organ; while the main branch
of the nerve leaves the capsule through the foramen in the more anterior
part of the capsule. Just lateral to the foramen nasalis externus (ne),
the lamina externa abruptly expands from its ventral margin into a horizon-
tal plate which partly covers Jacobson’s organ, its lateral angle terminating
in a small anterior process; while more anteriorly it narrows considerably
and lies directly above the posterior prolongation of the cornu (Fig. 63).
The anterior medial angle of the lamina externa is united by a cylindrical
bar to the anterior cupola, as in the adult Amblystoma (Fig. 10), which
separates the external naris from the large gap in the dorsal surface. The
naso-lacrimal duct passes to the nasal organ through the notch between
this bar and the anterior part of the externa, which is pierced by the fora-
men for the exit of the nasalis externus, as mentioned above.

The floor of the capsule is formed by the cornu trabeculae, which has
united to the lateral margin of the lamina externa, and continues poster-
iorly as a short process supporting the anterior end of the organ of Jacob-
son. The ventral gap in the capsule is very large and is similar to that in
Amblystoma.

The planum basale and verticale are united throughout their entire
length, forming a thick plate which unites the capsules just anterior to the
olfactory foramina and separates the internasal space from the cavum
cranii. Anterior to these parts, the lamina medialis (/m) forms the medial
wall of the capsule; narrower at its junction to the verticale, it becomes
wider more anteriorly and finally uniting with the cornu trabeculae, it forms
the anterior vault of the capsule. Midway between the tip of the capsule

28 ILLINOIS BIOLOGICAL MONOGRAPHS [28

and the verticale, the lamina medialis is pierced by two foramina, through
the dorsal of which, the nasalis internus of the profundus nerve passes to
the intermaxillary gland; while a blood vessel passes through the more
ventral one. A small prenasal process extends anteriorly a short distance
from the median ventral surface of the cupola. The internasal space is
deep and narrow, and it is filled with intermaxillary glands which extend
back beneath the planum basale, to its posterior margin. In the presence
of these glands, Plethodon differs from Cryptobranchus and Spelerpes
but resembles Amblystoma and Salamandra.

In all essentials Plethodon resembles very closely the adult Amblystoma
to which it is probably nearly related. The absence of earlier stages has
prevented a study of the development of the capsule; but comparing the
single larval stage of Winslow with my early stages of Amblystoma,
coupled with the many resemblances between the adults, I am inclined to
place Plethodon very near to Amblystoma. The absence of the fenestra
infra-conchalis in Plethodon is the primary difference between these cap-
sules; but the position and size of the planum verticale, the lamina externa
and medialis, the anterior cupola as well as the large dorsal and ventral
gaps are resemblances that suggest a very close relationship between these
animals.

NECTURUS MACULATUS

As in Spelerpes, the chondrification of the nasal capsule of Necturus
is greatly retarded; so that, except for the mere extension of the trabeculae
into the head region, there is no evidence of a nasal skeleton up to the 25
mm. stage. In higher Urodeles of this size, well developed capsules are
already chondrified.

In a 24 mm. larva, the trabecular crests are not developed, and the
cylindrical trabeculae incline toward each other, but do not unite to form
the planum basale. There is no evidence of a cornu at the anterior end,
nor has the antorbital process yet chondrified; but procartilage cells have
formed near the trabecula which indicate its later development. The
forebrain lies lateral to the nasal sac and extends slightly anterior to the
trabeculae.

In a slightly older stage (Fig. 25), the anterior ends of the trabeculae
more closely approach each other and near the tips they have expanded
dorso-laterally, so that a cross section of the trabecula in this region is
reniform. Miss Platt (1897) has described the independent chondrifica-
tion of the planum basale, and its subsequent connection to the trabecula;
although this stage does not show the chondrified basale, yet a few pro-
cartilage cells lying in the tissue between the anterior ends of the trabeculae
indicate its origin as independent of the trabeculae. In this stage also, a
small triangular antorbital process has chondrified from the trabecula.

29) THE NASAL ORGAN IN AMPHIBIA—HIGGINS 29

In a 30 mm. larva (Fig. 26), some additional structures are present,
although the capsule differs considerably from any other Urodele. The
trabeculae are now united near their anterior ends by a planum basale
(pb), trapezoidal in outline, its posterior margin being one and one-half
times the length of the anterior. A median swelling upon the dorsal
surface of the planum basale, together with the trabecular thickenings
give the plate a bi-concave appearance, the olfactory lobes resting in the
concavities. This median swelling, more evident over the anterior half of
the planum and which resembles a similar structure in Cryptobranchus,
must be regarded as a rudimentary planum verticale, although the later
stage shows no further development of it (Fig. 64). Anterior to the plan-
um basale, the trabeculae continue forward a short distance; and, without
expanding into cornua so typical of other Urodeles, each trabecula, sepa-
rated from its mate by a wide internasal space, ends bluntly in the surround-
ing tissue.

The beginning of the well-known fenestrated capsule of the adult
Necturus, covering the nasal organs, mentioned and figured by Wieder-
sheim (1877) and others, appears in this stage. Directly over the medial
margin of the nasal sac, and some distance from the trabecula is a small
bar of cartilage, the columna ethmoidalis (ce), which extends from a little
in front of the level of the anterior end of the trabecula back to the level
of the posterior margin of the planum basale. At no time is it united to
the trabeculae, and it recalls in origin and position this column in Amblys-
toma. A more posterior extension of this bar in the 33 mm. and 35 mm.
stages, in which it reaches nearly to the antorbital process, suggests that
here, as throughout the order, this bar chondrifies, first in the anterior
parts and then develops posteriorly; although here it never unites to a
crista trabecula, a structure entirely lacking in Necturus. Also in the 33
mm. and 35 mm. larvae I have observed cartilage cells along the lateral
margin of the nasal sac, some of which lie between the folds of the nasal
epithelium. These several areas do not seem to arise as a continuum,
but chondrify independently and later become connected to each other and
to the ethmoidal column to form the roof of the fenestrated capsule.

The antorbital processes are now more like those of other Urodeles,
reaching forward a short distance toward the other parts of the capsule.

In the last stage of Necturus studied, a larva 45 mm. long (Fig. 28),
the fenestrated nasal capsule (fez pr) has developed and resembles that of
the adult. The trabecula (¢), planum basale, and anterior extensions of
the trabeculae are much as before, differing only in size; while the planum
verticale, earlier prominent as the median ridge on the basale, is now
reduced to a small swelling on the anterior half of the basal plate. Accord-
ingly, the posterior half of the basale, which supports the olfactory lobes,
is slightly and broadly concave.

30 ILLINOIS BIOLOGICAL MONOGRAPHS {30

The entire dorsal surface of the simple nasal sac and part of the lateral
surface is covered by a curved and fenestrated cartilage, more extensive
posteriorly where it curves ventrally over the choana. This process is a
further development from the columna ethmoidalis with large additions
from the cartilage cells described in the earlier stage, which now have
united to each other in such a way that small gaps expose the dorsal sur-
face of the nasal sac (Fig. 65). In front, the lateral parts of the fenestrated
process are lacking, so that the ethmoidal column alone forms the roof in
this region; while the more extensive chondrification occurs in the posterior
parts. This more complete development posteriorly, and the gradual
reduction toward the anterior end culminating in the unspecialized eth-
moidal column, indicates a development from behind forwards, and recalls
the condition in both Sglamandra and Amblystoma in which the columna
ethmoidalis develops lateral processes, first from its posterior parts.
Although the fenestrated process of Necturus never unites to other capsular
parts, yet because of its relation to the ethmoidal column and the nasal
organ, it is the homologue of the planum tectale of other Urodeles.

The antorbital processes (pa) are larger than before, and although they
lie near the lateral parts of the fenestrated tectale, the two never unite, so
that a foramen orbito-nasalis is never completely enclosed; nor is there any
circumscribed olfactory foramen since the column is completely distinct
from the trabecula, and the olfactory nerve passes between column and
trabecula to the olfactory organ.

The early development of the nasal capsule of Necturus resembles that
of other Urodeles to this extent; the trabeculae with their antorbital
processes, the planum basale and the ethmoidal columns are common to all.
On the other hand, Necturus lacks the characteristic expanded cornua,
the trabeculae ending bluntly, as well as a planum verticale and lamina
medialis, which in all other Urodeles completely separates the nasal organs
from each other and closes the internasal space from the cavity of the
forebrain. The nasal organs of Necturus are exposed on their ventral,
medial and lateral surfaces, and are only incompletely covered on the dor-
sal by the fenestrated cartilage. In the origin of the columna ethmoidalis
and its subsequent direction of growth, together with the development of
the fenestrated roof, there is a similarity to Amblystoma; but the many
striking contrasts between the capsules of these two Urodeles must estab-
lish very remote relationships between them, or are possibly to be inter-
preted by the neotenic character of this animal.

The lack of skeletal protection for the nasal organs, the absence of
many parts of a typical urodelan capsule, as well as the very unspecialized
nasal sac itself, suggests for Necturus that it is to be regarded as either
ancestral, as a permanent larva or as indicating degeneracy of parts. To
regard Necturus with its fenestrated capsule, which has no counterpart

31] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 31

throughout the entire urodelan order, as primitive, would be unjustified;
but, the greatly retarded process of chondrification, the absence of cristae
and cornua trabeculorum, together with the entire separation of the roof
of the capsule from the other parts, may be explained in either of two
ways; Necturus has either descended from some more specialized Urodele,
or, as the retarded process of chondrification would suggest, it may repre-
sent a neotenic condition of some form, like Spelerpes.

AMPHIUMA MEANS

The first of the three capsules of Amphiuma studied, is that of a larva
still within the egg, in which the chondrocranium is very incomplete,
resembling in many ways the larva described by Kingsley (1892), and
figured by Winslow (Fig. 18, 1898).

Each trabecula, from the crista forwards, inclines, at first gradually,
and then somewhat more abrupt, toward the median line; the two uniting
to form a small rectangular planum basale (pd, Fig. 29), which supports
the olfactory lobes. Anterior to the planum, each trabecula’ continues
forward a short distance, and then expands into a triangular cornu, concave
upon its dorsal surface to support the anterior part of the olfactory sac.
The cornua are separated from each other by a deep and narrow inter-
nasal space, resembling that of Spelerpes, the Urodele, the larva of which
most resembles the early Amphiuma.

The cristae trabeculorum (cr f) are well developed and extend forward
to the base of the antorbital process (pa), which in Amphiuma is directed
obliquely forward from the trabecula, rather than at right angles to it as in
other Urodeles. The anterior margin of each crista trabeculae is con-
tinued forward as a cylindrical bar along the medial dorsal margin of the
nasal sac. At the level of the anterior end of the antorbital process, the
bar runs forward and outward and passes obliquely over the nasal organ,
giving rise to a short process just dorsal to the nasal sac, and continuing
outward and downward to the lateral surface of the sac where it turns
directly forward and runs along the lateral surface of the sac nearly to the
level of the planum basale. Hay (1890) speaks of this bar as the rudi-
mentary nasal capsule, while Winslow (1898) describes it as projecting
forward, outward and downward, but without the small dorsal processes
present in my stage, and which help to explain the later modifications of
the capsule. In its origin from the trabecular crest, this bar, which
probably contains elements of both ethmoidal column and tectal cartilage,
recalls the process in Spelerpes, extending forward from the anterior margin
of the crest, which was interpreted as the posterior end of a developing
columna ethmoidalis.

Olfactory foramina do not exist, but each olfactory nerve passes over
the trabecula just in front of the crista trabeculae, where the nasal organ
and the olfactory lobe are very close together.

32 ILLINOIS BIOLOGICAL MONOGRAPHS [32

In an older larva, a more complete nasal capsule (Fig. 30) has been
formed, which resembles in but few respects those of other Urodeles. It is
somewhat ovoid in outline, its greatest width being about one-fifth its
length. From the anterior end of the crista, each trabecula, relatively
more slender than before, inclines medially and passing along the lower
margin of the olfactory lobe, unites with its fellow at about the level of the
middle of the capsule, to form the planum basale (pb). This plate is
considerably larger than before, and together with the cornu of either
side, forms a plate roughly hexagonal in outline. Its posterior margin is
straight, while lateral to the line of the trabecula, its caudal margin is
directed antero-laterally to a point corresponding to the lateral angle of the
cornu of the early stage, where it fuses with another cartilage bar yet to be
described. Each lateral-cephalic margin is also curved and is produced
in front, in a line with the trabecula, into a process directed forward from
the planum, the anterior extension of the trabecula. These cornual tips
are separated by an internasal space somewhat wider although much
shorter than before.

The planum verticale (pv) arises from the anterior half of the basale,
just back of the internasal space, as a narrow band of cartilage, which
separates the nasal organs in this region (Fig. 69, pv). Dorsally the planum
verticale divides into two bars, the alary processes, which are inclined to
each other at about an angle of 60 degrees. Each alary process is con-
tinuous with the columna ethmoidalis, and partially covers the antero-
median surface of the olfactory sac.

The columna ethmoidalis is now complete, extending forward from the
crista to, and slightly beyond, the alary process. Apparently this cor-
responds to the bar arising from the superior margin of the crista of the
earlier stage, as far as and including the small process dorsal to the nasal
sac described above. The more lateral portion of the earlier bar is evi-
dently the lamina externa of this stage, which now extends forwards along
the lateral surface of the nasal organ. At about the level of the planum
verticale, the lamina externa (/e) sends a process downwards, which unites
with the lateral angle of the cornu. The lamina externa continues beyond
this junction as a broader plate, ending in an oblique circumnarial carti-
lage ring surrounding the narial aperture.

The antorbital process is much as before, being inclined at an angle of
about 30 degrees from the trabecula, rather than at right angles to it as in
most other Urodeles.

Many of the characters of the nasal capsule of the adult Amphiuma,
as described by Wilder (1892), appear in a larva 82 mm. long. The nasal
capsule (Fig. 31) has doubled in size, although the proportions are un-
changed; additional chondrification having occurred in the anterior parts.
The crista trabeculae, antorbital process, trabecula, planum basale, and

33] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 33

columna ethmoidalis are much as in the younger stage, and need no further
description. The dorsal surface of the capsule, however, has been changed
by the continuation forward of the ethmoidal column to a junction with
the circumnarial cartilage and a lateral extension of the cartilage from the
column to the lamina externa; so that the whole anterior end of the capsule
is roofed in as far back as the level of the verticale, this roof being perfor-
ated behind and near its median line for the passage of the nasalis internus
of the profundus. The lamina externa, behind its connection with the
cornu is wider than before, and close to the lower margin near its anterior
end is a smaller foramen for the nasalis externus of the profundus, where
it passes to the external nasal glands.

The chondrification of the anterior parts of the capsule has outlined a
large gap upon the dorsal surface, bounded by the columna ethmoidalis,
lamina externa and anterior tectale, resembling in shape the large dorsal
gap in Amblystoma. The floor of the capsule is represented by the cornu
trabeculae and the antorbital process; the latter has not united to any
more anterior capsular part, so that a foramen orbito-nasalis does not
exist, nor does Wilder describe one in the adult.

The nasal capsule of Amphiuma differs considerably from that of any
urodele thus far described. The large vacuities in the dorsal, lateral and
ventral surfaces and the consequent lack of skeletal protection of the nasal
epithelium is much in contrast to either Salamandra or Amblystoma and
may represent either a reduction in parts or a permanent larval condition.
So far as I know, a circumnarial ring does not exist in any other Urodele,
the anterior part of the capsule being vaulted in all others, with the excep-
tion of the Caecilians and Necturus. The fusion of the planum basale with
the cornua trabeculorum to form the hexagonal plate, is not common for
other capsules, where in the older stages these parts are considerably
removed from each other.

The narrow planum verticale develops dorsally from the median line of
the planum basale, somewhat as in Cryptobranchus, and then unites
laterally to the ethmoidal column which, as in Spelerpes, probably devel-
oped anteriorly from the cephalic margin of the trabecular crest. In no
other capsule, thus far described, with the exception of Necturus, is there a
complete absence of the lamina medialis. Anterior to the verticale the
nasal organs are separated by membrane only, a wide gap extending from
the medial margin of the cornu to the anterior tectale.

Amphiuma appears to be far removed from other Urodeles. It cannot
be regarded as ancestral, as it is difficult to homologize the capsule of this
animal, even in the early larval stages, with that of other genera; but it
probably is reduced from more typical conditions more closely related to
either Spelerpes or Cryptobranchus. In the origin of the verticale and in the
form of the cornu which unites to the anterior extension of the externa,

34 ILLINOIS BIOLOGICAL MONOGRAPHS [34

Amphiuma resembles Cryptobranchus; and furthermore, the expansion
of the ethmoidal column, at its middle to form the lateral parts of the capsule
is alike in both. On the other hand, Amphiuma resembles Spelerpes in the
size of the planum basale and the inter-nasal space, as well as in the pos-
terior development of the ethmoidal column, evidence being lacking on
this point in Cryptobranchus.

35] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 35

THE NASAL CAPSULE OF THE GYMNOPHIONA
EPICRIUM GLUTINOSUM

Considerable diversity of opinion has existed-in the past in regard to
the systematic position of the Caecilians. Cope (1889) classed them as a
family of the Urodeles, related to them through Amphiuma; while the
cousins Sarasin (1890), following Cope, also regarded them as Urodeles,
considering Amphiuma a neotenic Caecilian. Kingsley (1902) reviewed
the evidence as to the position of the group, showing that many points
supposed to indicate relationships, were based upon erroneous statements
or misconceptions and that the Gymnophiona are to be regarded as a
distinct group, without any close relations to any other existing Amphibia.

To determine to what extent, if any, the nasal capsules of this group
would shed light upon their relationships to the Urodeles, two larvae of
Epicrium glutinosum were studied,in which chondrification was well
advanced and the nasal capsules completely formed.

Peter (1898) has described the chondrocranium of a young Caecilian;
and Winslow (1898) a stage in which the embryo is still spirally coiled
within the egg, considerably younger than my earlier material. In con-
trast to all other Amphibia, the trabeculae of each side are double (Fig.
32), consisting of a dorsal and ventral bar in the position of trabecular
crest and trabecula, the dorsal doubtless being the homologue of what
Sewertzoff (1897) has called the alisphenoid cartilage of the Elasmobranchs.
On either side of the eye, the dorsal and ventral trabeculae are united by a
postorbital and preorbital band, the optic nerve passing through the
large gap between them. Anterior to the preorbital band, the lower or
true trabecula inclines toward the median line, and is united with its mate
by a slightly convex planum basale (pd), which lacks the trabecular
thickenings of the plana of Urodeles. The posterior and lateral margins
of the planum are straight, the latter more anteriorly curving outward
where it passes into the posterior margin of the cornu trabeculae, which
forms the floor of the capsule; while anterior to the cornu the planum
narrows considerably and is continuous in front into a pair of small proc-
esses, the tips of the trabeculae, separated from each other by a wide
internasal space.

The planum verticale (fv) is a narrow plate of cartilage, arising from
the ‘anterior half of the median line of the basale and extending dorsally

36 ILLINOIS BIOLOGICAL MONOGRAPHS [36

to the upper margin of the nasal organs, completely separating them in
this region from each other. The dorsal part of the verticale extends
backward a short distance over the planum basale; while anteriorly it
extends forward over the internasal space where it divides into three parts,
a short median rostrum continuous with the verticale, and a pair of alary
processes which extend ventrally and laterally, terminating near the tips
of the trabeculae. In a later stage these alary processes develop ante-
riorly and laterally to form the vault of the capsule.

Anterior to the preorbital band, a wide band of cartilage, the lamina
externa, forms the side wall of the capsule. It is pierced by two foramina,
the smaller more posterior one for a small branch of the fifth nerve, while
the profundus passes through the larger, more anterior one. Winslow
(1898), in his early stage, describes a small antorbital process which
extends outwards and forwards from the anterior margin of the preorbital
band, much as in the Urodeles. In this stage, the anterior part of this
process has united to the lateral parts of the capsule, enclosing the foramen
above described, which must be the orbito-nasalis of Urodeles; so that it
would seem that the lamina externa is formed of elements of an ethmoidal
column and an antorbital process, although complete evidence as to the
former is lacking.

Anterior to the foramen orbito-nasalis, the lamina externa widens
slightly, its dorsal margin extending more medially, reaches to the level
of the upper surface of the verticale, where a short process extends for-
ward, separated from the remaining externa by a deep notch through
which the superficialis passes to the nasal organ. Ventral to this notch
and in the same horizontal line with the foramen orbito-nasalis, is another
foramen through which a branch of the profundus nerve passes from the
capsule.

Beyond this latter foramen, the lamina externa, more narrow than
before, extends forward a short distance, ending in a blunt process in line
with the anterior margin of the planum basale; while ventral to the foramen
it is united to the cornu trabeculae, which supports the anterior end of the
nasal sac, forming the only floor of the capsule, and enclosing the large
ventral choanal gap.

! Winslow has described a small cartilage bar, lying near the trabecula,
ust beneath the preorbital band, which is unassociated with any other
part of the capsule. This he calls a palatine cartilage. In my material,
this small bar is directly in line with the anterior part of the pterygoid
process from which it is but slightly removed; and it would seem as though
it was a part of the pterygoid which may have chondrified independently,
or have separated from the more basal part of this process. Peter (p. 582,
1898) in his description of the pterygoid of Ichthyophis says: ‘‘Dagen
findet sich in seiner Verlingerung parallel der unteren Trabekelspange ein

37] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 37

Knorpelstab, der sich bis in die Mitte des Opticusfensters erstreckt und
seinerseits wieder in zwei Theile gespalten sein kann. Eine dichte Zellan-
hiufung verbindet die einzelnen Stiicke mit einander und mit dem Fort-
satze des Quadratum, so dass die betreffenden Elemente wohl als eines
Ursprungs aufgefasst werden kénnen.’’ The term palatal cartilage is a
misnomer at least, for it is evident that the palatine bone, which is mem-
brane in origin, could hardly be derived from this cartilage

The capsule of the older larva, 90 mm. long, (Fig. 33) differs consider-
ably from that just described; the greatest change taking place in the more
anterior parts. The ossification of many of the covering bones, and the
resorption of certain cartilage structures, as well as the chondrification of
others, has resulted in a capsule very different from that of any other
Amphibian.

The preorbital and postorbital bands are much as before and need no
further description, with the exception of the statement that they are
more oblique, from medial and dorsal to lateral and ventral, than before.
Through resorption, all connection between the preorbital band and the
planum basale has been lost, so that a short caudal process from the planum
on each side of the median line is a remnant of a trabecula, all intermediate
parts having become ossified. The planum basale is shorter than before
and the solum nasale or cornu trabeculae is now more posterior and in line
with the caudal margin of the basale, which it unites to the lamina externa
as in the early stage. The antero-lateral margin of the planum is more
semicircularly excavate than before, and the tips of the trabeculae, extend-
ing beyond the basale are more slender, the internasal space between them
being wider and deeper.

The planum verticale (fv), arising from the median line of the basale is
wider than before, although not relatively as high. It is continued
posteriorly into an elongate cylindrical process which extends backward
to the level of the posterior margin of the basale, the dorsal root of the
olfactory nerve lying lateral to it; while anteriorly it extends forward into
a similar process reaching nearly to the tip of the snout. The alary proc-
esses, flanking the median rostrum of the verticale, which were just
beginning to chondrify in the earlier stage, have now grown forwards and
outwards covering the more anterior parts of the nasal sac and uniting
with two lateral processes yet to be described, each forms a partial cupola,
incomplete ventrally which protects the anterior ends of the olfactory sac.
There is a small foramen near the lower margin of this cupola, through
which a branch of the profundus nerve leaves the capsule.

The lateral wall of the capsule of this older stage is considerably
different from that described above. The orbito-nasal foramen, the
medial process of the lamina externa and their nerve relations are as before;
but ventral to the foramen for the externus branch of the profundus, the

38 ILLINOIS BIOLOGICAL MONOGRAPHS [38

lamina externa bears a short posterior process from its ventral margin, a
remnant of resorption now going on, so that the choanal gap in this stage
is incomplete.

Just in front of the connection of the lower margin of the lamina externa
to the cornu trabeculae, the lamina continues forward as two cartilage
bars, the upper more cylindrical, the lower somewhat flattened, between
which the organ of Jacobson is included. By the fusion of these parallel
rods with the alary process above described, an elongate naris is formed
which extends over one-half the entire length of the capsule; and at the
same time these cartilages all unite to form the tip of the capsule, a flat-
tened plate which covers the end of the nasal sac (Figs. 67, 68).

The nasal capsule of Epicrium is considerably different from that of
any other Amphibian and can hardly be said to be Urodelan. In a very
few points, resemblances can be drawn between the Caecilian and Urodelan
structures; but these are so few, and the modification of the parts in the
Caecilian is so great, that few close relationships can be established. The
independence of alisphenoid cartilage and trabecula in Epicrium, find no
parallel among the Urodela where these parts are continuous and form the
wall of the cavum cranii; while in no other capsule do we find the deep
and narrow external naris, as is present in my older stage.

The floor of the capsule is formed by a cartilage called by Peter (1898)
the solum nasale, which can be none other than a modified cornu trabeculae
which has developed laterally and has united to the lamina externa, just
anterior to its fusion with the antorbital process. So that in this relation
of cornu trabeculae, lamina externa and processus antorbitalis, there is a
condition quite similar to the other capsules, such as Triton and Ambly-
stoma, although superficial resemblances are lost. That the solum nasale
was a cornu could not be derived from a study of the later stage where
the greater development has taken place anteriorly, placing the solum in
line with the planum basale; but the resemblance between the cornu
trabeculae of my two weeks Cryptobranchus larva and this structure in
my younger Epicrium seems to indicate the identity of these parts.

Superficially, the capsule of Epicrium resembles that of Amphiuma
more than any other Urodele. In both the sensory parts are but poorly
protected, wide gaps occurring in all sides of the skeleton. The presence
of a six-sided planum basale, with its anterior prolongations, the planum
verticale with its antero-lateral alary processes are structural resemblances
between these animals. On the other hand Epicrium lacks the circum-
narial ring of Amphiuma, and in its place has developed a partial cupola,
possibly in correlation with the burrowing habit of this Amphibian.

In the origin of the planum verticale from the basale, as well as in the
similarity of their cornua, Epicrium recalls Cryptobranchus; and it does
not violate probability to assume that the small process ‘developed

39] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 39

from the medial margin of the lamina externa is a remnant of an ancestral
ethmoidal column, which originally was united to the more medial parts
of the capsule.

Although some homologies may be drawn between the capsules of
Epicrium and the Urodeles, the divergence between the two is sufficient
to warrant the separation of the Caecilians and the maintenance of the
Gymnophiona, distinct from all other Amphibia. Although the greater
resemblance among the Urodeles is to Amphiuma, yet it is not sufficient to
warrant the position of either Cope or Sarasin in the relationship of these
groups.

40 ILLINOIS BIOLOGICAL MONOGRAPHS [40

COMPARISON OF THE NASAL CAPSULES IN THE
URODELA AND GYMNOPHIONA

The nasal capsules of several families of Urodeles afford a basis for
the division of this order of Amphibia into four groups, founded upon
similarity of larval structures and the method of chondrification. In
some forms, where larval characters were not at hand, adult characters
were employed in the classification; in others the early process of develop-
ment was the only criterion available. Of these groups, Spelerpes,
Plethodon and Amblystoma form one; Salamandra, Triton and Diemicty-
lus another; Amphiuma, although remote from Cryptobranchus in the
later stages, is included with it in the third; while Necturus remains alone
in the fourth group.

To recognize in the nasal capsules of the Urodela a complete phylo-
genetic development or gradual transition from one animal to another is
impossible, for many gaps exist, concerning which evidences of structural
relationships are wanting. On the other hand many resemblances in the
development of certain structures in the nasal capsule may throw some
light upon the inter-relationships of this Amphibian order.

Of the Urodeles included in this study, it would seem as if the capsule
of the American species of Cryptobranchus possesses characters most
ancestral and which show relationships to both Urodela and Anura. Re-
garding Cryptobranchus, then, as more primitive, Spelerpes, Plethodon
and Amblystoma appear in an ascending series from the primitive condi-
tion; while Salamandra, Triton and Diemictylus are separated from them,
but possibly related to them through some form like Spelerpes. Necturus
may be regarded as a neotenic condition of Spelerpes, while Amphiuma is
possibly reduced from the more primitive Cryptobranchus.

The two weeks larva of Cryptobranchus has a well-developed trabecular
crest which is not present in corresponding stages of Spelerpes or Ambly-
stoma; in the latter of which the development of the crest is apparently
correlated with the chondrification of the ethmoidal column. Thus it
would appear that in Cryptobranchus the dorsal crest is developed before
the column, while in Amblystoma the reverse is true. In this respect,
Spelerpes is intermediate between Cryptobranchus and Amblystoma,
although more like the former; for in the only available stage of the older
larva of Spelerpes, the crista is well developed, while the columna eth-
moidalis is but partly chondrified. My material does not show the origin

41] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 41

of the ethmoidal column in Cryptobranchus, for in the five weeks larva it
already unites the medial margin of the cornu to the crista; but judging
from its relation to the capsule, and in its complete separation from its
mate, these structures resemble those of Spelerpes in which the anterior
part of the columna arises from the medial margin of the cornu and grows
posteriorly along the nasal sac. Further, the anterior prolongation of the
dorsal crista in Spelerpes, interpreted as the posterior part of a developing
column, may also exist in Cryptobranchus, although conclusive evidence
on this point is lacking.

In the 25 mm. Salamandra larva, the anterior end of the column is
connected to the cornu trabeculae much as in Cryptobranchus; and yet
the expansion from its posterior end, forming a small tectale prior to any
connection with the crista, suggests an independence of the ethmoidal
column, like that of Amblystoma. Although the dorsal crests of Salaman-
dra develop along with the columna ethmoidalis, the two do not unite until
a later stage, thus the posterior part of a developing column is lost in all
Urodeles above Spelerpes. In Amblystoma, on the other hand, the eth-
moidal column and the cornu trabeculae are chondrified independently of
each other. Ina 13 mm. larva, I have described a few cartilage cells above
the medial margin of the cornu of the left trabecula only. This is the first
appearance of an ethmoidal column which subsequently grows posteriorly
along the median dorsal margin of the nasalsac. The fact that I observed
these cells as chondrifying, at first, upon one side only, has no especial
significance; but in the independent chondrification and the complete
development of the ethmoidal column from in front backwards, prior to
any association with the trabecula, Amblystoma differs from any other
Urodele, except Necturus in which the independently chondrified ethmoidal
column never unites to other parts of the capsule. Thus in the 20 mm.
stage of Amblystoma, completely developed columnae ethmoidales parallel
the trabeculae from their anterior tips to the choana; but do not unite to
any crista, which here is greatly retarded in its appearance, not developing
until the 25 mm. stage is reached.

The ethmoidal column in Amphiuma is more like that of Cryptobran-
chus and Spelerpes in the development of the posterior parts; there being
no evidence of an anterior part of a column in the youngest larva studied.
Somewhat as in Spelerpes, the anterior portion of the crista continues
forward into a cylindrical bar along the medial margin of the nasal sac, and
from its relation to other parts, as well as its position, it must be regarded
as a columna ethmoidalis. As in Cryptobranchus, it gives off laterally a
small process which may be homologized with the tectale, which then turns
anteriorly, forming the lateral wall of the capsule, the lamina externa.

In all Urodeles studied, the planum basale is formed by a fusion of the
trabeculae in the middle line of the skull; and in some forms, this plate,

42 ILLINOIS BIOLOGICAL MONOGRAPHS (42

which usually supports the anterior end of the telencephalon, is the only
connection between the two capsules. In Cryptobranchus, Amphiuma,
and Necturus, the planum basale of the larval stages is slightly convex,
due to the origin of the verticale from its median line; while on the other
hand the planum basale of Salamandra and Amblystoma are broadly
concave, being in no way associated with the development of the verticale.
The size of the basale is variable in the different groups; being very small
in Cryptobranchus, Spelerpes and the larval Amphiuma, it increases in
Plethodon and Salamandra, and reaches its greatest development in the
larvae of Amblystoma where the fused basale and verticale form a thick
anterior wall to the cavum cranii. Individuals approaching the end of
metamorphosis show a reduction in the size of the planum basale, and in
the adult stage it is greatly reduced, correlated with the development of
other parts of the capsule and the increase in size of the sensory parts. In
both larvae and adults of Triton and Diemictylus the planum basale is
very small, and in the latter, is the only connection between the two cap-
sules.

The planum verticale arises in different ways throughout the order.
In Cryptobranchus, it arises from the median line of the basale as a small
ridge, and later, uniting to the median margins of the ethmoidal columns,
it forms a complete wall separating the internasal space ‘from the cavity of
the forebrain. The same is true in Amphiuma, although evidence is lack-
ing as to the origin of the verticale, yet the later stages would suggest its
development from the planum basale as in Cryptobranchus. The early
larvae of Necturus have a small median ridge on the basale, probably a
vestigial verticale; but it never develops and is less prominent in the later
stage, a further evidence of the neotenic condition of this genus.

In the remaining groups, the verticale does not arise from the basal
plate, but is developed by medial growths from the columnae ethmoidales
which subsequently unite to the basale, so that the results are identical.
In my material of Spelerpes, evidence of the formation of the verticale is
lacking; but judging from the relation of the early columna to the cornu,
and by the flat dorsal surface of the basale, it would appear that here, as in
Amblystoma, the verticale arises from the medial growths of the ethmoidal
columns. Ina 25 mm. Salamandra larva, there is no evidence of a median
verticale plate. The cornua and columnae are united just anterior to the
planum basale, but internasal space and cavum cranii are continuous with
each other. In the later stage, medial growths from the anterior parts of
the columnae unite just above the anterior margin of the basale, and form
a pons ethmoidalis, separated from the ventral plate by a circular gap, the
fenestra ethmoidalis. This gap is only temporary in Salamandra, fortby
the more ventral chondrification of the pons, a complete verticale is formed
and the internasal space and cavum cranii are completely cut off from each

43] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 43

other. In Amblystoma, this process is.changed slightly, due to the
independence of the ethmoidal columns from the cornua. In the 25 mm.
larva, by medial growths of the columnae a pons has formed, so that in
this stage the capsule is divided into dorsal and ventral halves, the only
connection being the crista. By further chondrification of the region
between the pons and the planum basale, a verticale is formed, the process
continuing posteriorly, developing the solid thick cartilage of the 45 mm.
larva.

A planum verticale does not chondrify in Triton and Diemictylus, so
that internasal space and cavity of the forebrain are separated by mem-
branous structures only. The pons ethmoidalis develops in Triton, uniting
the dorsal medial margins of the capsules somewhat anterior to the planum
basale, but it is completely lost in Diemictylus. Evidence is lacking as to
the origin of the pons in Triton, but Born (1876) describes the process as a
continuous growth of cartilage from the trabeculae, and not as independent
parts; it would appear, then, that the pons has probably arisen by growths
from the medial surfaces of the capsules, similar to that of Salamandra.
In the absence of a pons, Diemictylus appears to be reduced from some
form like Triton; the nasal capsule of these two being very similar in other
details.

The antorbital process is present in all Urodeles, arising in all, except
Cryptobranchus, from the ventral margin of the trabecula just back of the
choana. It is directed laterally and anteriorly and in most Urodeles unites
to the lamina externa, or to the cornu trabeculae, outlining the foramen
orbito-nasalis, through which the nerves of the nasal region enter the
capsule. In Necturus and Amphiuma, on the other hand, this process
never unites to the more anterior parts of the capsule, so that a foramen
is never formed, nor is there any posterior wall to the capsule as in those
Urodeles where the antorbital unites to the tectale, as in Plethodon and
Amblystoma.

Gaupp (1893) held that the antorbital process of Urodeles is homologous
with the pterygo-quadrate arch of the Anura; and the terms palatine
cartilage or ethmo-palatine have been indiscriminately used when referring
to this structure. If we regard Cryptobranchus as ancestral, or at least
more primitive, a conclusion I believe both the nasal capsule and the
olfactory organs justify, then the relations and the development of the
antorbital process in this animal may throw some light upon the homology
of these structures. In the two weeks larva, in which the trabecular
crests are already well-developed, there is no evidence of an antorbital
process; but slightly posterior to its probable position, procartilage cells
lie near the lateral ventral margin of the trabecula, which continue pos-
teriorly into the pterygoid process of the quadrate. In the later stage,
these cells have chondrified and, uniting to the pterygoid, have reached

44 ILLINOIS BIOLOGICAL MONOGRAPHS [44

forward, and, bending at right angles the bar has joined to the ventral
margin of the trabecula in the region where the antorbital process occurs in
all Urodeles. In the five weeks larva, there is no extension forward of this
bar beyond its connection with the trabecula; but in the older larvae, a
small process extends forward toward the capsule, an apparent’ continua-
tion of the pterygoid; so that an antorbital process is formed which resem-
bles in detail those of most other Urodeles. Because of the lack of older
stages, I have no evidence as to the connection of the antorbital to the
capsule, nor can I say just when the resorptive processes take place which
establish the adult condition of the complete separation of the pterygoid
from the capsular region.

Regarding Cryptobranchus as primitive, then it would appear that the
Urodelan antorbital process is in reality composed of the anterior end of a
pterygoid plus an anterior extension which secondarily becomes associated
with the nasal region. In the Anura, both larva and adult, the pterygoid
unites with the anterior part of the trabecula, as in the larval Crypto-
branchus, suggesting here a common ancestry; and this relationship tends
to support the original conclusion of Gaupp that the antorbital process of
Urodeles, at least in its basal part, and the “palatine cartilage” of the
Anura are homologous structures. The anterior part of the antorbital,
however, is something else and may not be a part of the original pterygo-
quadrate arch; accordingly it would seem that in those Urodeles in which
the pterygoidal condition is lost, that the entire structure had best retain
the name antorbital process.

Winslow (1898) has described, in his second stage of Ichthyophis, an
isolated cartilage in front of the anterior end of the pterygoid, which he
calls the ‘‘palatine cartilage’’; and interprets it as being a part of an original
“palato-pterygoid-quadrate” arch. This cartilage can hardly be called a
palatine, and the triple term applied to the pterygo- quadrate is a misnomer
for the palatine bone is not cartilaginous in origin. It would appear,
however, as though this small cartilage is a part of the pterygoid which at
one time was connected to the antorbital process, and to the more proximal
pterygoid. In his earlier stage, Winslow describes a small antorbital
process which arises much as in the Urodeles ffom the trabecula. In my
material, this process has united to the more anterior parts of the capsule
outlining the foramen orbito-nasalis; and from its relation to the isolated
part of the pterygoid we are safe in assuming that these parts were at one
time in continuity, and in that sense the Caecilians are related to the
common ancestor, from which Cryptobranchus on the one hand, and the
Anura on the other, have arisen.

In the Siberian genus, Ranodon, Wiedersheim (1877, Fig. 69) has
figured the relation of the antorbital process to the pterygoid much as it
occurs in Cryptobranchus; which fact suggests that these genera may be

45] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 45

related, both having retained these ancestral characters. An older larva
of Spelerpes, also figured by Wiedersheim (Fig. 108), has a caudal extension
of the antorbital process, which he calls the maxillary cartilage, whose
relation to the pterygoid suggests an earlier relation between the two.

In several of the Urodeles, as shown by figures of Parker (1876), and
Wiedersheim (1877), a strong pterygoid reaches well forward from the
quadrate, absent in some of my larvae but present in the adult. In the
earlier larva of Amphiuma, a pterygoid process has not developed; but in
the later stage it has chondrified well forward, nearly to the base of the
antorbital. In all Urodeles, both processus antorbitalis and pterygoid are
developed, but the proximity of the two varies greatly throughout the
order, and I would hesitate to base any statement of relationships upon
the relative extent of development of these structures; but no where except
in Cryptobranchus and Ranodon is there any connection between them.

The openness of the nasal capsule of Amphiuma, together with the
somewhat specialized anterior part, renders it difficult of homology with the
more typical Urodele, and suggests that it is far removed from any other
Amphibian. However, in the early method of chondrification, and in the
development of some of the parts, Amphiuma appears to be more closely
allied to Cryptobranchus. In both, the cristae trabeculorum are formed
early, as well as the planum verticale, the latter arising from the median
line of the basale and later becoming associated with the columna eth-
moidalis. Further relationship is evidenced in the origin of the tectale as
a lateral growth from the columna, giving rise in Amphiuma to the elongate
lamina externa, along the lateral surface of the nasal sac. Meagre as
these relationships may seem, Amphiuma appears to be nearer Crypto-
branchus than any other Urodele, the anterior parts of its capsule having
become secondarily acquired.

Although Salamandra resembles Amblystoma in some ways, the many
differences between their capsules, such as the size of the planum verticale,
the persistence of the foramen ethmoidalis in the former, and the origin of
the ethmoidal columns, justifies their separation. In the persistence of
the caudal process of the planum basale in the 25 mm. Salamandra, there
is a resemblance to Cryptobranchus; but in the origin of the columnae
ethmoidales from the medial margins of the cornua, Salamandra is more
like Spelerpes.

Triton and Diemictylus are far removed from the group just described,
but are probably related to it through Salamandra. The complete
development of a lamina medialis, with the deep internasal space, and the
anterior position of the olfactory sac in respect to the forebrain, as well as
the persistence throughout life of the fenestra ethmoidalis, are characters
common to both Triton and Diemictylus. The complete loss of a pons
ethmoidalis in Diemictylus converts the fenestra into a gap, only a mem-

46 ILLINOIS BI OLOGI CAL MONOGRAPHS [46

branous partition separating the internasal space from the cavum cranii.
It would follow then, that Diemictylus is probably reduced from some
form like Triton, and both genera are related to Salamandra which has
developed along a line parallel to Amblystoma; and it is through some
Spelerpes-like larva, as far as the nasal capsules are concerned, that
Salamandra, Triton and Diemictylus are related to the group including
Plethodon and Amblystoma.

Necturus and Proteus have often been regarded as primitive and Cope
(1889) included them in a group, Proteida, apart from the Urodeles,
although ancestral to them. I have not examined Proteus, but upon the
basis of the nasal capsule of Necturus, which cannot be regarded as ances-
tral, Cope’s position can not be affirmed. Pinkus (1894) called attention
to the similarity of the nasal capsules of Necturus and Protopterus, a
similarity based wholly upon the fenestration of the capsules, and not upon
structural resemblances. The parts of the capsule of Necturus may be
homologized with those of other Urodeles, but many differences have arisen
in the appearance of these parts, so that relationships are very remote.
Many parts of the capsule chondrify independently, later uniting to each
other; the ethmoidal column, however, never unites to the other parts of
the capsule, but by lateral growths produces the fenestrated roof over the
nasal sac. Necturus is greatly retarded in the development of its nasal
structures. Ina 25 mm. larva only trabeculae are present, there being no
evidence of cornua or planum basale or columnae, as in corresponding ages
of Amblystoma and Salamandra. The earlier larvae of Spelerpes, Des-
mognathus, and Necturus seem to resemble each other very closely in their
cylindrical trabeculae, slight cornual expansions and absence of trabecular
crests. In the later stages, however, further resemblance is lost, for
Spelerpes has gained true Urodelan characters while Necturus still possesses
larval relationships; a fact, which, together with the retarded process of
chondrification, suggests for Necturus that it may be a persistent larva, as
has often been suggested.

As stated above, Cope placed Proteus with Necturus in the Proteida,
regarding them as primitive Amphibia, and related to the Stegocephala by
the presence of an intercalary bone. Kingsbury (1905) rejects Cope’s
thesis, affirming the absence of an os intercalare in Necturus, and suggested
that Cope had probably regarded the posterior process of the opisthotic
as an intercalary; furthermore he regards the intercalary of the Stegoce-
phala as a membrane bone.

Norris (1911) working on the cranial nerves of Necturus, concludes
that it cannot be regarded as primitive. The distribution of the cranial
nerves agrees in detail with that of the higher Urodeles, a condition which
would not be expected in a primitive form. Kingsbury, like others, has
regarded Necturus as a neotenic larva, and would place it near Spelerpes.

47] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 47

His conclusion is based largely upon the absence of certain cranial bones,
such as the nasals, prefrontals and maxillaries, which are present in other
Urodeles. Rudimentary nasal capsules exist in the larvae of both Speler-
pes and Necturus, and in the former a completely developed capsule is not
present until a relatively late period, correlated with its retarded metas
morphosis, the individual often not transforming until two or three years
after hatching. On the basis of the nasal capsule, I am inclined to regard
Necturus as a permanent larva, possibly related to the other Urodeles
through a Spelerpes-like ancestor. The retention of the larval characters
of the trabeculae and of the planum basale can certainly not be regarded
as ancestral, nor can degeneration alone explain the present structure of
the capsule of Necturus.

The phylogenetic position of the Gymnophiona has occasioned much
diversity of opinion. Huxley (1875) stated that there was not the slightest
indication of any approximation to either the Anura or the Urodeles. On
the other hand, Cope (1889) even placed the family Caecilidae among the
Urodeles, and regarded them as degenerate and related to the main line
through Amphiuma; while the Sarasin cousins (1890) took the position
that Amphiuma was a neotenic condition of the Caecilian. Kingsley
(1902) discussed the views of both Cope and the Sarasins and established
the conclusion, now generally accepted, that the Gymnophiona are to be
regarded as distinct from either Urodela or Anura and placed in a separate
order.

The nasal capsule of Epicrium presents little of classificatory value,
except that it presents only distant resemblances to the characteristic
Urodelan capsule. In the presence of dorsal and ventral trabeculae, Epicrium
differs from all other Urodeles where the alisphenoid and trabecula are
continuous and form the lateral wall of the cavum cranii. In the earlier
stage, which Winslow studied, the ventral trabeculae unite to form the
planum basale, but there is no extension forward of the trabeculae into
cornua as in Urodeles; although in my earlier stage, which is considerably
later than that of Winslow, small processes occur at the anterior margin of
the basale, the probable tips of the trabeculae. The solum nasale, how-
ever, or floor of the capsule which unites the lamina externa to the planum
basale, is a modified cornu, which in the older stage especially, is greatly
removed from the position of the cornu trabeculae in Urodeles. The
antorbital process, a lateral growth from the trabecula in the early stage of
Winslow, later unites to the other parts of the capsule, as in Urodeles,
bounding the orbito-nasal foramen. That the antorbital was at one time
related to the parts of the pterygoid just posterior to it, is suggested by a
sharp protuberance on its ventral margin toward the small independent
part of the pterygoid; so that it would appear as if the processus antor-
bitalis and pterygoid cartilage of Epicrium were at one time united as in

48 TLLINOIS BIOLOGICAL MONOGRAPHS {48

Cryptobranchus, but the now intimate association of the former with the
nasal capsule indicates that the Caecilian probably is far removed from
ancestral conditions.

Epicrium is more like Amphiuma, of all Urodeles, although differing
greatly from it. The greater similarity lies in the origin of the planum
verticale from the median line of the basale and in the subsequent develop-
ment of the alary processes which, in the later stages of both, partially
cover the dorsal surface of the nasal sac. Further similarity lies in the
modification of the cornu trabeculae which in both, forms the floor of the
capsule, uniting the planum basale to the lower margin of the lamina
externa, and partially supporting the nasal organ.

On the other hand, the parallel rods of cartilage which in Epicrium form
the lateral wall of the capsule anterior to the solum nasale, uniting anter-
iorly with the alary process to form a partial vault, do not exist in Amphi-
uma, where the united elements of cornu and lamina externa expand into
an oblique circumnarial ring. Further, the antorbital process of Amphiuma
never unites to the capsule as in Epicrium, nor at any stage does a complete
columna ethmoidalis exist in the latter form, so that there are many
contrasts between the capsules of the two. Thus upon the evidence
submitted by the nasal capsules, the position of Cope or Sarasin can not
be supported, all conditions pointing to the complete separation of the
Gymnophiona from the Anura or the Urodela.

49] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 49

THE NASAL CAPSULES OF THE ANURA

PIPA AMERICANA

The Surinam toad, a representative of the aglossate Anura, is unique
among the Amphibia in its quiescent larval period, during which, the entire
development takes place; so that the adult characters are formed before
the animal takes up its free existence.

Parker (1876) has described the chondrocranium of a Pipa larva,
considerably younger than my single stage, in which the complete fusion of
the trabecular plates has obliterated the large hypophysial fenestra, so
common to most amphibian skulls. In Parker’s larva, the coalesced
trabeculae form a broad, slightly emarginate internasal plate, which
extends forward to the tip of the skull, where from each lateral margin a
slender process bends posteriorly and, passing beneath the nasal organ,
terminates in a rounded projection near the middle line of the capsule.
Parker calls these processes the ‘recurrent trabeculae’, but it is easy to see
that they are modified cornua, which in Pipa are more cylindrical than in
most Urodeles, more like those in Cryptobranchus.

In my single stage, a Pipa larva two-thirds of an inch long, much of the
cartilage of Parker’s stage has been resorbed and the chondrocranium is
more like that of other Amphibia. The broad intertrabecular floor is now
reduced to a pair of trabeculae, which, with greatly reduced cristae, reach
forward to the level of the eye, where they are united by a planum basale
as in Urodeles (Figs. 34, 35, pb). This planum basale is broadly concave
dorsally (Fig. 73, pb), and supports the olfactory lobes which lie above the
posterior parts of the nasal organ; so that the olfactory nerve, which leaves
the olfactory lobe from its ventral margin, passes through a large median
foramen olfactorius (fo) in the basale, reaching the nasal sac at the choana.
More anteriorly the planum basale narrows considerably, covering only
the medial parts of the nasal sac and the nasal glands; at the same time
expanding ventrally into a prominent keel, which separates the choanae
of the two sides. Farther forward the planum basale is continuous with
the planum verticale, which reaches forward to the tip of the skull, there to
unite with other parts yet to be described thus completely separating the
nasal organs of the two sides.

From each lateral angle of the planum basale, a small planum tectale
(pt) passes obliquely outwards and forwards, covering the posterior part
of Jacobson’s organ where it empties into the nasal sac. At its lateral

50 ILLINOIS BIOLOGICAL MONOGRAPHS (50

posterior angle the tectale is continuous with the anterior portion of the
pterygoid process, the two uniting to form a large triangular plate, Parker’s
ethmo-palatine cartilage, which continues forward into his pre-palatine
spur; this process covering Jacobson’s organ and part of the nasal sac. It
is obvious that the terms ethmo-palatine and pre-palatal spur, used by
Parker, are misleading for reasons stated before in this paper; and it would
seem that the term planum tectale had best be used to designate this entire
process. The extension forward of the pterygoid is the normal condition
in the Anura, but among the Urodeles it is known to exist only in Crypto-
branchus and Ranodon, this ancestral character having been lost in other
Amphibia.

On the lower outer surface of the trabecula, at its junction with the
capsular parts, is the foramen for the nasalis nerve, hence this is the orbito-
nasalis of the Urodeles. It follows from this identification, that the bar
‘ventral to this is the greatly reduced antorbital while the roof of the foramen
is as plainly tectale. The main part of the nerve courses forward through
the cartilage, and the anterior end of the foramen lies on the ventral side
of the tectale (Fig. 35). Another branch of this nerve emerges on the
dorsal surface of the trabecula, turns medially and then ventrally and
passes through another foramen to the medial side of the nasal sac parallel
with the olfactorius. Just medial to this last foramen is the olfactory
foramen for the I nerve which passes downward to reach the olfactory
organ. From this it follows that the cartilage region anterior (and mor-
phologically dorsal) to these nerves and their foramina must be the columna
ethmoidalis.

At about its middle, the lower margin of the planum tectale gives rise
to a short bar, at first extending ventrally and then medially and a little
posteriorly, just above the anterior end of the organ of Jacobson. From
near its base this bar gives rise to a cylindrical rod, which runs obliquely
forward and inward to become continuous with the lower lateral surface of
the planum verticale near its anterior end. In this course it passes, first,
on the outer surface of the connection of the organ of Jacobson with the
olfactory sac, then along the ventral lateral margin of the sac itself. The
medial end of the ventral bar is connected with a second cylindrical
cartilage, passing obliquely forward and inward to join the dorsal lateral
side of the verticale at its tip, medial to the naris. Where the more ventral
of these two cylindrical bars unites to the verticale, it expands into an
alinasal cartilage, which supports the anterior part of the nasal organ, and
is separated at its anterior end from the distal margin of the verticale by
a crescentic groove, the external naris (Fig. 74).

The two cylindrical cartilages just described, have been known in the
literature as the dorsal and ventral bars or processes, terms that convey
nothing as to their homologies. From a study of Parker’s early larva, it is

51) THE NASAL ORGAN IN AMPHIBIA—HIGGINS 51

evident that the planum verticale is a reduced internasal plate, and that the
so-called ventral process is a modified cornu. In the early stage, according
to Parker, this cornu trabeculae is free from the tectale, ending near its
median margin in a blunt process; but in the stage that I have studied the
two are united, thus recalling the relation of these parts in the Urodeles.
The dorsal process is evidently something additional in Pipa and cannot
be compared to any Urodelan structure; although it exists in some form or
other in all Anura, where it has been called the oblique cartilage because of
its relation to the nasal organ. ‘This cartilage may be a part of the original
internasal plate of Parker’s stage, the intermediate part between it and
the verticale having been resorbed, leaving the elongate gap upon the dor-
sal surface of the capsule.

The capsule of Pipa is unlike any other Amphibian, differing markedly
from any Urodele or Phaneroglossa, although similar in many ways to the
other aglossal genus Dactylethra. The chondrocranium of Parker’s
younger larva is more complete and lacks the large gaps of the later stage,
in which the resorptive processes have so greatly changed the appearance
of the capsule. The planum tectale is evidently a growth from both the
columna ethmoidalis and the trabecula, and has subsequently become
united posteriorly to the pterygoid process, while anteriorly it has grown
forward into the triangular process which has erroneously been called the
ethmopalatine cartilage.

From the above identification of the ethmoidal column, it would
appear that the planum verticale has developed by a fusion, in the middle
line of the skull, of the trabeculae and the columnae ethmoidales; the
ventral part of the verticale being trabecular in origin, the dorsal half
derived from the united columnae ethmoidales. In this relationship, then,
we have a condition very largely Amblystomal; for in the 34 mm. larva,
the ethmoidal columns unite to the coalesced trabeculae to form the thick
planum verticale so characteristic of Amblystoma, but which in Pipa is so
greatly reduced in width.

BUFO AMERICANA

The nasal capsule of the Phaneroglossa is far more complex than that
of the Aglossa, and the olfactory organs which lie entirely anterior to the
forebrain are better protected by cartilage structures.

In a larva of Bufo vulgaris, one-third of an inch long (Parker, 1876),
the trabeculae have fused to form an internasal plate, smaller than in Pipa,
from which they diverge forward forming the cornua trabeculorum with
an internasal space between them. So that this early stage of Bufo is
similar to my 28 mm. Rana viridescens, yet to be described.

In my single stage of Bufo americana, whose body length is 9 mm., a
complex nasal capsule has been chondrified; and resembles in many ways

52 ILLINOIS BIOLOGICAL MONOGRAPHS [52

the chondrocranium described by Gaupp (1893) of a 13 mm. Rana fusca.
In this stage (Figs. 36, 37), a complete cavum cranii has been formed,
bounded upon each side by the high alisphenoid cartilage, the internasal
plate or planum basale forming the floor; while in front a perpendicular
ethmoidal wall, pierced by a pair of olfactory foramina, separate the olfac-
tory lobes from the nasalsac. Anterior to this ethmoidal wall, the planum
basale (pb) forms the floor of the capsule; extending forward as a thick
plate as far as the large naso-basales fenestrae, which open from the cavity
of the capsule to the internasal space. The planum basale supports the
medial parts of the nasal sac and its ventral diverticulum.

The planum tectale (pt) forms the roof of the capsule; reaching forward
from the cavum cranii, somewhat more narrow and thinner than the
basale, it covers the medial portions of the nasal sac to the external naris,
in front of which it bends abruptly downward to form with the solum
anterius, the anterior wall of the capsule. At its anterior end, the tectale
expands laterally into a pair of alinasal cartilages, which curve outward
and then upward, supporting the anterior end of the nasal sac and forming
the ventral margin of the external naris; while from the base of these a
pair of superior prenasal processes extend downward and somewhat me-
dially into the internasal space (Fig. 82). Just medial to the external
naris, the tectale is pierced by a small foramen on either side for the exit of
the internus branch of the fifth nerve.

The planum verticale (pv) completely separates the nasal organs from
each other. Arising from the median line of the perpendicular ethmoidal
wall, it chondrifies anteriorly uniting the plana basale et tectale by their
dorsal and ventral surfaces respectively. It extends forward to the tip
of the skull, and its anterior margin separates the two large circular naso-
basales fenestrae, which perforate the forward wall of the capsule (Fig. 80).
These fenestrae surround the medial portion of the ventral nasal diverticu-
lum together with the frontalis nerve, which passes to the intermaxillary
gland in the internasal space.

In contrast to Pipa, a posterior wall is formed in the capsule of Bufo,
by a lateral extension of the posterior part of the planum tectale, which
curves outward and downward beyond the alisphenoid, uniting to the
anterior prolongation of the pterygoid, which has already fused with the
lower parts of the cranial wall. In the angle formed by the fusion of the
pterygoid, tectale and alisphenoid, a small orbito-nasalis foramen conducts
rami of the fifth nerve into the capsule; so that here, as in Pipa, there is a
resemblance to the Urodeles, which furnishes a clue to the homologies of
these parts (fom).

The united elements of lateral tectale and anterior pterygoid form a
small rectangular cartilage which lies against the lateral surface of the
nasal sac. This cartilage has been variously named the pars plana (Parker

53] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 53

1876) or planum terminale (Gaupp 1893); but from its relation to the
tectale and the pterygoid, and from its position in respect to the nasal sac,
the term lamina externa is best used here. Furthermore, it is apparently,
at least in part, the homologue of the antorbital process of the Urodeles.
Parker has also used the term prepalatine for this cartilage, which appeared
to him to be in some way segmented from the more posterior parts; but
I have no evidence that the lamina externa in Bufo is distinct from the other
parts, for it appears to develop as a continuum, subsequently uniting to
the more anterior parts of the capsule.

From the dorsal margin of the lamina externa, a narrow bar of cartilage
passes upward, forward and medially over the lateral surface of the nasal
sac to unite to the lateral margin of the planum tectale, slightly posterior
to the external naris. This is clearly homologous with the dorsal process
of Pipa, better known in both groups as the oblique cartilage (Fig. 81).
The facrimal duct, arising from the eye by two branches, passes forward
over this oblique cartilage and down through a groove in the lamina
externa to empty into a lateral diverticulum of the main nasal sac (Fig. 80).

Anterior to its connection with the oblique cartilage, the lamina externa
continues forward into the lateral margin of the solum anterius, which
forms the anterior wall of the cavum inferius, and is evidently developed
from the cornu trabeculae, together with a dorsal extension of it. It isa
thin plate of cartilage, bent upon itself, so that it includes in the angle the
anterior part of the cavum inferius, which contains the more lateral parts
of the ventral pouch of the nasal sac. More dorsally the solum anterius
unites to the anterior margin of the planum tectale, its lateral margin
expanding into the alinasal cartilage, already described. More posteriorly
and within the capsule itself, is a short cylindrical bar of cartilage which
extends from the lower margin of the alinasal cartilage to the anterior
margin of the planum basale, thus separating the main nasal sac from the
organ of Jacobson.

A small cylindrical inferior prenasal process, larger than the superior,
extends forwards and slightly upwards into the intermaxillary glands.
Below and behind, from the lateral angle of the solum anterius, a short
process is directed posteriorly which rests beneath the diverticulum of the
nasal sac, where it receives the lacrimal duct. This process may possibly
be the tip of the cornu.

In contrast to Pipa, the capsule of Bufo much more adequately protects
the olfactory organs; the gaps in its wall being smaller than in that genus.
In Bufo the choanal fenestra is small and is distinctly bounded by cartilage,
while in Pipa its boundaries are decidedly indefinite. Again Pipa has no
circumscribed fenestra naso-basalis. Further differences between the cap-
sules of the two genera are the greater depth of that of Bufo, correlated
with a reduction in length, the result being an apparently more complicated
condition of the anterior parts.

54 ILLINOIS BIOLOGICAL MONOGRAPHS (54

HYLA PICKERINGII

My work on Hyla has been restricted to a study of the adult, in which
the development of membrane bones over the anterior end of the forebrain
has been accompanied by a partial resorption of the posterior parts of the
capsule, so that homologies are not always certain. Still Hyla in general
has a somewhat close resemblance to its arciferan relative, Bufo.

Behind the planum verticale (fv), the planum basale (pb) has under-
gone resorbtion in the middle line, so that it is represented by a pair of
narrow plates (Fig. 38). In front, however, the continuity of the two
sides persists to the anterior end of the capsule, where the planum basale
passes into the solum anterius. The perpendicular ethmoidal wall is
lacking, as well as the posterior part of the planum tectale, so that the
latter, posteriorly is reduced to an oblique bar on either side, the tectale
being complete only in its anterior third, where it is expanded in front to
twice its width. At the tip of the cranium, the tectale bends downward to
pass into the vertical solum anterius.

All that remains of the planum verticale (pv) is a median septum, with-
out a gap, uniting the anterior parts of plana basale et tectale. In front,
where it joins the solum anterius, the tectale separates the two basal fenes-
trae, which are very much smaller than in Bufo. Dorsal and slightly
lateral to these openings, is a small foramen for the exit of the nasalis
internus nerve from the capsule.

The lamina externa (Je), developed partly from the lateral part of the
planum tectale, and partly from the anterior prolongation of the pterygoid
process, forms the side wall of the capsule in the choanal region. Anterior
to its connection with the tectale, this plate narrows considerably, and is
interrupted by an oval gap, apparently a further evidence of resorbtion, as
no sensory or nervous structures were found to pass through it. Just
anterior to this opening the oblique cartilage (oc) passes upward and for-
ward from the lamina externa over the nasal sac, to unite to the planum
tectale at its widest part, its ventral side being expanded to form the pos-
terior boundary of the naris (Fig. 77).

Just ventral to the origin of the oblique cartilage from the lamina
externa, the lower margin of the latter expands outward into a small
process which separates the cavum inferius from the more ventral cavum
medium. More anteriorly, this part of the lamina externa unites with the
lateral parts of the planum basale to form the solum anterius, which
constitutes the anterior wall of both cavum inferius and c. medium, and the
more medial parts of the capsule.

As in Bufo, the solum anterius is a thin plate of cartilage which curves
upward and continues into the anterior margin of the planum tectale.
Near its junction to the latter, a small alinasal cartilage extends laterally,
forming the anterior boundary of the external naris; it is continuous med-

55] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 55

jally into a small superior prenasal process which extends ventrally and
medially from the capsule. The inferior prenasal process is considerably
longer than the superior; it arises from the planum basale just in front of
the choanal gap and extends forwards and downwards into the internasal
space (Fig. 78). Forming the floor of the c. medium, and extending back-
ward beneath and slightly lateral to the lamina externa is a conical process
considerably larger than that in Bufo; the possible remrfant of the original
cornu trabeculae.

Two small foramina pierce the solum anterius; the smaller and more
dorsal conducts the nasalis internus from the capsule, while the larger more
medial one is the fenestra naso-basalis, considerably smaller than that
described for Bufo.

RANA VIRIDESCENS

The nasal capsules of the Arcifera and the Firmisternia are essentially
alike, and, although I lack a series of stages showing the chondrification of
the nasal capsule in Rana, the work of Gaupp (1893) has made it possible
to compare the growth of the nasal capsule of the frog in connection with
my own two stages.

In a larva 28 mm. long (entire length), in which the characteristic
Anuran chondrocranium is beginning to develop, the nasal capsule (Fig. 40)
consists of an elongate planum basale (pb), with the anterior extension of
the trabeculae to the labial cartilages. The muscularis process of the
quadrate (mpq) has fused with the lateral wall of the planum basale, and
just above the junction of the two a dorsal process has arisen from the
basale, which is to become the side wall of the capsule (Fig. 83). Gaupp
(1893) has referred to this cartilage as the ‘“‘Ethmoidal-pfeiler,” but it
differs from the ethmoidal column of Amblystoma in which chondrification
of this bar is independent of the planum basale.

Medial processes from the dorsal margin of each columna ethmoidalis
fuse in the middle line and form a pons (fe), recalling this same structure
in Amblystoma and in Salamandra (Fig. 84). In all three genera the
cavum cranii and the nasal cavity are continuous during a part of the
larval development by means of the fenestra ethmoidalis (fen eth) ventral
to the pons. Unlike Triton and Diemictylus however, chondrification
from the pons to the planum basale soon develops the ethmoidal wall which
separates these cavities.

Upon a level with the pons ethmoidalis, and arising from the dorsal
part of the ethmoidal column, a small process extends laterally toward the
muscularis process of the quadrate. A small opening, which must be
regarded as the foramen orbito-nasalis for the nasalis internus nerve,
pierces this process near its base; and from this identification, it follows
that this process must contain parts of both planum tectale and processus
antorbitalis, the latter being beneath the foramen. The more dorsal posi-

56 ILLINOIS BIOLOGICAL MONOGRAPHS [56

tion of the antorbital in this stage, may be explained by the presence of the
muscularis process of the quadrate, and its attachment to the planum bas-
ale just ventral to the antorbital (Fig. 83).

Just in front of the choana, which opens into the mouth slightly anterior
to the ethmoidal column, a longitudinal constriction of the nasal sac
partially divides it into two chambers; one medial and dorsal, lying upon
the lateral part of the trabecula, the other lateral and more ventral (it is the
beginning of Jacobson’s organ), which lies to the side of and to some extent
beneath the trabecula.

The olfactory nerves of the two sides now pass from the forebrain for-
ward and beneath the pons ethmoidalis to the nasal sac. Later, a chon-
drification ventral from the pons completely obliterates the fenestra
ethmoidalis and, forming the ethmoidal wall, it outlines the two olfactory
foramina in the anterior lateral angles of the cavum cranii.

Anterior to the planum basale, the trabeculae diverge, enclosing a
wedge-shaped internasal space between them. At first more narrow, each
trabecula widens nearer its tip; and, just in front of the level of the naris,
bends abruptly downward to end near the inferior labial cartilage. This
vertical portion of the trabecula is apparently what Gaupp calls the super-
ior labial cartilage, and which he figures as a discrete element in both his
earlier and later stages. Ido not find in my material any line of demarca-
tion between the trabeculae and the superior labial cartilages.

I have had no material intermediate between the larval stage just
described and a young frog soon after metamorphosis. But it is easy to
see, however, that the changes undergone are about as follows; this account
agreeing substantially with that of Gaupp.

As in a larva of Bufo, a tadpole of Rana approaching the end of meta-
morphosis, according to Gaupp, shows a decided reduction in the sagittal
plane of the anterior part of the nasal capsule. This reduction is caused
by a partial resorption of the earlier larval trabeculae, so that the definite
nasal capsule is formed by a development of the posterior parts of the
trabeculae, together with certain independently chondrified parts.

Subsequent to the closure of the fenestra ethmoidalis, by the develop-
ment of a perpendicular ethmoidal wall, the planum verticale chondrifies
anteriorly, separating the nasal organs of the two sides and uniting the
planum basale in its median line to the planum tectale, which has grown
forward from the dorsal margin of the pons and the ethmoidal column.
The lamina externa forms the side wall of the capsule, and develops from
the lateral part of the tectale; it unites to the oblique cartilage, which chon-
drifies independently and lies diagonally across the nasal sac from the
lamina externa to the more anterior tectale.

In the anterior part of the capsule, the greatest modification takes place.
The loss of the labial cartilages and the anterior parts of the trabeculae

57] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 57

causes a shortening of the capsule, which is accompanied by an increase in
its depth. In front, each trabecula gives rise to a solum anterius which
forms the anterior wall of the capsule; and at its junction to the tectale
each solum gives rise to an alinasal cartilage, which supports the anterior
end of the nasal sac and forms the posterior boundary to the external naris.
The large naso-basal fenestrae between the medial margins of the anterior
walls of the capsule and the planum verticale open from the nasal cavity
to the internasal space much as in Bufo.

In this stage, the articulation of the lower jaw has moved backward, so
that the deeply curved muscularis process of the quadrate is more poster-
ior; and, as a result, the pterygoid has united to the capsule at the point of
origin of the tectale from the ethmoidal column, the anterior maxillary
process reaching forward from the junction of the two.

In a young adult of Rana viridescens (Figs. 85, 86) there has been a
relative reduction in the height of the verticale, although the proportion
of breadth to length is approximately unchanged. Anterior to the cavum
cranii, planum tectale, basale and verticale have fused into a thick plate,
recalling the association of these same structures in Amblystoma. The
olfactory foramen (fo) opens obliquely forward from the antero-lateral
angle of the cavum cranii to the nasal cavity just beneath the foramen
orbito-nasalis the posterior opening of which lies adjacent to the lateral
margin of the cranial wall. Lateral to the foramen orbito-nasalis, the
fused tectale and antorbital curve outward and downward over the choana
and continue posteriorly into the pterygoid, while anteriorly a small maxil-
lary process reaches forward midway to the tip of the capsule.

The nasal sac is completely covered dorsally by the lateral parts of the
planum tectale which reaches forward to the tip of the cranium, and is
considerably narrower at the anterior end. At about the middle of the
tectale, an oblique cartilage bar (oc) extends backward and slightly out-
ward, ending bluntly near the anterior end of the maxillary process (amp).
Although unconnected in this stage, these two structures are probably
the homologue of the lamina externa and the oblique cartilage of the larva.

The nasal sac opens to the exterior just anterior to the oblique cartilage,
where the alinasal cartilage, continuous anteriorly into a superior prenasal,
forms the floor of the naris. Beneath the alinasal, but connected to it, is
a thick cartilage, the crista subnasalis (cr s) possibly a remnant of the
earlier solum anterius, although evidence is lacking here. Anterior to the
crista sub-nasalis is the inferior prenasal process, which extends ventrally
from the capsule; while directly above it is the fenestra naso-basalis,
greatly reduced here, and more like that in Hyla.

58 ILLINOIS BIOLOGICAL MONOGRAPHS [58

COMPARISON OF THE NASAL CAPSULES IN THE ANURA

The division of the Anura into the suborders Aglossa and Phaneroglossa
is borne out by this study of the nasal capsules; for Pipa would appear to
be far removed from the other Anura, and because of the large vacuities
in the chondrocranium it may be said to be more like the Urodeles.

In all of the Anura, the extension of the pterygoid process to the nasal
capsule is the normal condition, and recalls this relationship in Crypto-
branchus Furthermore, the planum tectale, apparently a lateral growth
from the. columna ethmoidalis, unites to the pterygoid, the two forming
in Bufo the lamina externa, which forms the side wall of the capsule; while
in the adult Rana, the anterior connection of the lamina externa is lost, the
united pterygoid and tectale forming the anterior maxillary process.

The cavum cranii of Pipa is not as well developed as in other Anura,
the alisphenoids being but little higher than the planum basale, and less
crest-like in their appearance. The forebrain in Pipa lies dorsal to the
posterior part of the nasal sac, rather than posterior to it as in Bufo; and,
if the olfactory nerve may be regarded as sufficient evidence for the deter-
mination of homologies, then that part of the basale in Pipa, anterior to
the foramen olfactorius, must be the perpendicular ethmoidal wall in Bufo
and other Phaneroglossa. This change in the relative position of these
parts may be explained by the statement of Gaupp that the chondrocrania
of larvae of Rana fusca suffer a reduction in the sagittal plane during
metamorphosis.

In both groups, the roof of the capsule, anterior to the region just
described is formed by a fusion in the middle line of the ethmoidal columns,
which also unite to the planum verticale. In Bufo, the extent of the tectale
lateral to the verticale is considerably more than in Pipa, where the medial
parts of each nasal sac are but slightly covered and suggest for Pipa a more
complete fusion of the ethmoidal columns. There is no floor of the nasal
capsule in Pipa, while in all the Phaneroglossa the planum basale extends
forward from the cavum cranii to the tip of the capsule, where each lateral
angle expands into the alinasal cartilage. The presence of these alinasals
in Pipa would suggest that the ventral half of the planum verticale must be
a fused and greatly reduced trabecular plate, homologous to the anterior
planum basale in the Phaneroglossa.

The lateral wing of the capsule, the so-called ethmo-palatine of Parker
or planum terminale of Gaupp, but more properly designated the lamina
externa in Bufo, is formed, partly from the pterygoid and partly from the
columna ethmoidalis. In both groups two cartilage bars unite the lamina

59] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 59

externa to other parts of the capsule; although differing in their relations
to each other, and in their position.in the capsule, their homology is very
evident. The ventral of these two bars is the cornu trabecula, more slender
and cylindrical in Pipa; while in Bufo it is greatly reduced in length, con-
siderably broader and has been designated in this paper as the solum
anterius. The junction in both groups of this cartilage with the alinasal
cartilage is a further,evidence of their homology. The dorsal of the two
bars, above mentioned, is apparently an additional structure in the Anura,
for I do not recognize it in any Urodele. The term oblique cartilage seems
to best designate this bar, extending, as it does, obliquely forwards and
upwards from the lamina externa to the planum tectale, or as in Pipa to
the tip of the planum verticale.

60 ILLINOIS BIOLOGICAL MONOGRAPHS {60

CONCLUSIONS BASED ON THIS STUDY

PHYLOGENY OF THE NASAL CAPSULE IN AMPHIBIA

The cartilaginous nasal capsule of Amphibia must have been derived
from that of some lower vertebrate, be it Dipnoan or be it Crossopterygian,
and that in turn from the Elasmobranch. So far as our knowledge goes,
the Elasmobranch capsule is a continuous cartilaginous structure with no
gaps or openings except that for the naris and the small foramina for the
passage of nerves. The amphibian capsule, on the other hand, has inter-
ruptions in its walls; some of which are due to the fact that in the adult,
bones appear in the nasal region and thus do away with the necessity of
the persistence of protecting cartilages in certain places. Some are caused
by the development of a complete olfactory duct with its choana, in addi-
tion to the naris.

Within the class of Amphibia there are many differences between the
various capsules, caused by differences in the size and shape of the cover-
ing bones, by the changes in the development and shape of the organ of
Jacobson, the modifications of the lacrimal duct, as well as by the difference
in the size and shape of the olfactory sac. It follows, therefore, that in the
history of the amphibian capsule, two stages should be recognized; one a
progressive process in which the capsule is built up, a repetition of the
ancestral (piscine) history, and the other in which this capsule is reduced
and changed into the definitive form.

In following these two stages, we are hampered in our conclusions by
the fact that we have no accurate and detailed account of the develop-
ment of the capsule of any fish, and expecially in those groups universally
recognized as ancestral. Neither Parker nor Sewertzow give any details
of the development of the Elasmobranch capsule which can be used in this
connection. The studies made in this laboratory of the development of
the capsule in Acanthais only go far enough to show that it consists, when
it first is recognizable, of a rudimentary floor, and an even more incomplete
roof, and that these arise independently of the trabeculae or other cranial
elements.

The foregoing studies show, that in those forms where the develop-
ment has been followed with any detail from one stage to another, that
there is first a progressive development, apparently tending toward the
formation of a complete capsule like that of the adult Elasmobranch.
Then alterations occur, largely degenerative in character, which result in
the partial reduction of the floor and roof. These progressive changes

61) THE NASAL ORGAN IN AMPHIBIA—HIGGINS 61

are well exemplified in Necturus where, even in the adult, the capsule is
more nearly entire than in any other genus; a condition which may be
explained on the supposition that Necturus is to be regarded, not as more
primitive than other Urodelan genera, but as a permanent larva, a view
which has been advocated by many in recent years.

In Amblystoma, as detailed in the foregoing pages, this history is
carried farther. There is first a progressive development tending toward
a complete capsule, but never approaching completeness as nearly as does
the adult Necturus. Then, in conjunction with the process of meta-
morphosis, there comes a resorption of parts and a modification of those
that persist, resulting in large vacuities in both floor and roof of the cap-
sule. These steps are detailed above, and the final result is an envelope
for the olfactory organ in which parts are recognizable as homologous
with those of the capsules of the adult Anura.

In the history of the capsules in all Amphibia the following parts are
concerned. The two trabeculae are united in the ‘ethmoid’ region by what
Gaupp and others have called an internasal plate. This lies below the
tip of the brain and is the ‘ethmoid plate’ of Winslow or the ‘planum
basale’ of the foregoing description. In front of this planum basale, the
trabeculae continue as the cornua trabeculorum to the tip of the skull,
supporting the anterior part of the nasal organ. In several Urodeles,
where I have studied the early larval stages (this history has not been
followed in the Anura with sufficient detail to say whether it holds for them)
a bar of cartilage, the columna ethmoidalis, arises on the upper medial side
of the olfactory organ (either independently or as an outgrowth from the
cornu) and lies parallel to the lower trabecula. By a lateral growth from
this ethmoidal column, the planum tectale extends over the dorsal surface
of the nasal sac, uniting in the later stages to the cornu trabeculae. The
term lamina cribosa, used by Winslow (1898) and Terry (1906) to designate
this cartilage is a misnomer, for it is hardly necessary to say that it cannot
be homologous with the structure bearing the same name in the mammals,
as it lies wholly dorsal to the olfactory nerve.

In the larvae of several Urodeles, and in my single larva of Rana, the
ethmoidal columns of the two sides are connected by a pons ethmoidalis
which roofs the fenestra ethmoidalis leading from the cavum cranii to the
ethmoid region. This is only a temporary condition in most amphibia
where the chondrification of the planum verticale closes the fenestra and
unites the floor and roof of the capsule. In Triton and Diemictylus, on
the other hand, the planum verticale never develops; so that cavum cranii
and internasal space are separated by membranous structures only.

The last special element entering into the formation of the capsule is
the antorbital process, which needs a somewhat longer discussion. In
the Urodeles, a process arises from the side of the trabecula just back of

62 ILLINOIS BIOLOGICAL MONOGRAPHS [62

the choanal region; it extends laterally a short distance, then turns forward
and later uniting to the planum tectale forms a part of the lateral wall and
floor of the capsule. This has almost universally been called the antor-
bital process; but the larva of Cryptobranchus shows what it really is.
In my second larva of this animal the pterygo-quadrate bar extends for-
ward from the hinge of the lower jaw and joins the trabecula at the same
point from which the antorbital projects in other Urodeles. In Ranodon
judging from Wiedersheim’s figure (1877, Fig. 69), there is a similar con-
nection of the pterygoquadrate with the anterior part of the skull. Else-
where in all described Urodeles, as far as I have been able to discover,
there is only an extension of the pterygoid process forward from the quad-
rate towards the capsular region; and even in the adult Cryptobranchus
(and this holds also for the Japanese species, as figured by Parker) the
connection between the pterygoid and the structures farther forward is lost.

In all the Anura, on the other hand, the pterygoid cartilage is connected
throughout life with the nasal capsules. In this respect Ranodon, and to
a less degree Cryptobranchus, approach the Anura more closely than any
of the other Urodeles. It is usual to regard this arch as the homologue of
the upper jaw of the Elasmobranch, which, with the development of the
osseous upper jaw of the Teleostomes and higher groups, has lost its original
function as a part of the feeding apparatus, and has fused with the side of
the cranium, its middle portion dropping out in the process. It may be
remarked parenthetically, that the name palato-quadrate commonly
given this arch is incorrect, as it contains no palatal element and no part of
the palatine bone is developed from it.

In no Elasmobranch is there any extension of the pterygoid as a distinct
process beyond the curve of the arch of the upper jaw. On the other hand,
in all of the Amphibia there is such a forwardly directed process, the
antorbital, already referred to. It would then apparently follow that the
antorbital process of the Urodele, is in its basal part, the anterior end of the
pterygoquadrate, while its anterior portion is a new formation. That this
interpretation is correct, is supported by all of the Anura that I have
studied.

In my earlier stages of Salamandra (in which there is no connection at
any stage between the pterygoid process and the structures farther for-
ward) the antorbital process is developed and extends forward beneath the
nasal capsule; but as yet it is unconnected distally with any other cartilage.
Just dorsal to the base of this process, both the ophthalmic and super-
ficialis branches of the fifth nerve pass into the capsular region. Thus
the antorbital process is ventral to these nerves. In the oldest larva
that I have of this genus, the roof of the capsule (planum tectale) has
extended back so that its posterior margin overlies the base of the antor-
bital, while between the tectale and the antorbital there is a very large gap.

63) THE NASAL ORGAN IN AMPHIBIA—HIGGINS 63

In other genera, both Urodele and Anuran, these same nerves pass through
a small foramen in the region corresponding to that in Salamandra; and
since nerves and their distribution may be regarded as sufficient criteria,
it follows that this part of the capsule is a composite of a ventral antorbital
and a dorsal tectale.

In Pipa, Bufo and Rana, the pterygoid joins the side of the anterior
part of the cranium, this distal portion being nearly at right angles with
the axis of the skull. At the anterior side, a process extends forward from
the bend in the pterygoid, forming the postero-lateral wall of the capsule.
This is the lamina externa in Bufo and Hyla; and in the adult Rana, where
its anterior connection with the capsule has been lost, the lamina externa
becomes the anterior maxillary process. This anterior process, then,
reaching forward from the pterygoid, be it ethmo-palatine (Parker 1881)
or planum terminale (Gaupp, 1893) can be none other than the antorbital
process of the Urodeles; and it is joined either in front (Bufo and Rana) or
upon its ventral surface (Pipa) by two cartilages, the oblique cartilage bar
and the cornu trabeculae, the latter being designated the solum anterius in
the Phaneroglossa.

On the basis of the nasal capsule, Epicrium is far removed from either
the Urodeles or the Anura; and it would appear that the grouping of the
recent Amphibia into three orders by Miiller (1832) is borne out by this
study. Anterior parts of a pterygoid reach well forward into the nasal
region, and although there is no continuity between the pterygoid and the
antorbital (which in my material has united to the more anterior parts of
the capsule); yet a sharp process extending from the latter toward the
pterygoid leads to the assumption that at one time these parts were con-
tinuous and that the antorbital process in Epicrium has had a pterygoidal
ancestry.

CLASSIFICATION OF THE AMPHIBIA

The earliest classification of the Amphibia did not include the extinct
with recent forms, largely because of the uncertainty of the systematic
position of the fossil forms, which were regarded by some as reptiles. It
was not until 1854 that Vogt stated that Archeosaurus and all the Laby-
rinthodontia are amphibians and not reptiles. Owen (1866) was among
the first to propose a classification to include both extinct and recent forms.

Since these earlier days most Zoologists divide the class into four
orders: namely; the Anura, Urodela, Gymnophiona and Stegocephala.
There have been few variations in the subdivisions in the Anura and the
Gymnophiona, but with regard to the Urodeles ideas have differed greatly.
Some would recognize only Salamandrina and Ichthyoidea; while more
commonly the tendency has been to subdivide the group into Perenni-

64 ILLINOIS BIOLOGICAL MONOGRAPHS (64

branchs, Derotremes and Salamandroidia,! according as external gills
persist through life, as gill clefts remain permanently open or, in the latter,
as the animals undergo a complete metamorphosis, losing their external
gills and gill-clefts.

Strauch (1870) divided the Urodeles into two sub-orders, the Salaman-
drida and the Ichthyoidea. The basis of his classification was the presence
or the absence of eyelids, the arrangement of the palatal teeth, and the
permanence of gills and gill clefts. The Salamandrida were subdivided
into two groups according to the arrangement of the palatal teeth. Those
Urodeles in which these teeth formed diverging rows upon the inner margin
of the palatine were grouped as the Mecodonta; while the Lechriodonta
included those animals in which the palatal teeth form converging rows
along the posterior margin of the palatine. The Mecodonta embrace six
genera of which Salamandra, Triton and Diemictylus are represented in
this paper; while of the thirteen genera included in Strauch’s Lechriodonta,
I have studied Amblystoma, Plethodon and Spelerpes.

The Ichthyoidea are divided into two groups, the Cryptobranchiata
and the Phanerobranchiata, according to the persistence of gill clefts only
or of both gills and gill clefts. Cryptobranchus, Menopoma and Amphiuma
belong to the former group; while Necturus, Proteus and Siren are included
in the latter.

The nasal capsules would support a classification of the Urodeles
similar to that of Strauch. Im the fore-going pages, I have included
Spelerpes, Plethodon and Amblystoma (part of the Lechriodonta of
Strauch) in a group descended from the more primitive Cryptobranchus;
while Salamandra, Triton and Diemictylus (the Mecodonta of Strauch)
are included in a group connected with the other group through some form
like Spelerpes. I have regarded Cryptobranchus as more primitive, and
Amphiuma as closely related to it, although not in the main line of descent.
Strauch has grouped Necturus and Proteus into the Phanerobranchiata
more distantly related to Cryptobranchus, while I have regarded Necturus
as a permanent larva of some Spelerpes-like animal. I have not studied
Proteus, but have placed Necturus in a separate group in keeping with
the later Perennibranchiate classification.

Accordingly on the basis of the nasal capsules, I would adhere to the
classification of the Urodeles into three suborders, the Perennibranchi-
ata [Phanerobranchiata (Strauch)], the Derotrema [Cryptobranchiata
(Strauch)] and the Salamandroidia. The latter may be divided into two
groups, and, following Strauch, the terms Mecodonta and Lechriodonta
may be retained.

‘In many text books, this is given as Salamandrina, but the group was called Salaman-
droidia by Fitzinger (1826) who in the same place describes a genus Salamandrina. Con-
fusion is therefore avoided by restricting the latter name to the genus while Salamandroidia
with its ordinal termination may be retained for the larger group.

65] THE NASAL ORGAN IN AMPHIBIA—HIGGINS 65

Cope (1889) misled by a supposed ethmoid bone in Amphiuma placed
the Caecilians with the Urodeles, in which view he was later supported by
the Sarasins (1890). Kingsley (1902) definitely determined the position
of the Caecilians and maintained Huxley’s conclusion that the Gymno-
phiona have probably separated from the ancestral Amphibia back in the
early Carboniferous period. The nasal capsule of Epicrium is further
evidence of the wide divergence of this group from all other Amphibia.

The Anura are readily separated into two groups, on the basis of the
nasal skeletons, and these agree with the extablished classification into the
Aglossa and the Phaneroglossa. Cope’s subdivision of the latter into
Arcifera and Firmisternia is not so readily recognized in the nasal capsules
of my material, although there are more resemblances between the cap-
sules of Bufo and Hyla, than of either with that of Rana.

AMPHIBIAN ANCESTRY

The Amphibians appear, as Stegocephals, in the Carboniferous period,
and although from the first they are considerably diversified, there is not
known a single trace of any tetrapodous vertebrate in the Devonian with
the sole exception of a single footprint from the Pennsylvanian. In the
Devonian and somewhat earlier, fishes belonging both to the Dipnoi and to
the Crossopterygian ganoids occur, and both of these piscine groups have
been invoked by various zoologists as the ancestors of the Amphibia,
possibly the tendency of the evidence at present favoring the Crossoptery-
gians.

All of the amphibians of the Carboniferous, with the possible exception
of Pelion, were caudate. Moodie (1916), the latest to study these ancient
forms, is inclined to regard Micrerpeton, a small Salamandra-like form, as
representing the ancestors of the modern groups, with Necturus as an
annectant genus. He bases this conclusion upon the resemblances of the
skull, the form of vertebrae and ribs, the peculiarities of the lateral line
system, and the presence in both of ‘ventral scutellations,’ a view which
closely resembles the earlier ideas of Cope.

But it would seem as if Moodie was leaning upon a weak reed in invok-
- ing ventral scutellations as an argument, no matter what view one may
take with regard to the other points of resemblance. It is well known
that many of the Stegocephals had ventral scutes, plates or bars upon the
ventral surface of the body, but the universal view is, that these structures
were purely dermal, belonging like scales of fishes to the skin. Moodie
cites Wilder as stating that Necturus had small cartilages in the ventral
region, and apparently he regards these as the homologue of the ventral
armor of Stegocephals. But there are very important differences between
the two.

66 ILLINOIS BIOLOGICAL MONOGRAPHS : [66

Most students have regarded the gastralia of Sphenodon and the Croc-
odilia as derivatives from the plates and bars of the Stegocephals. These
latter are also suggested as forming the elements from which the clavicles
and episterna of the higher vertebrates are derived. In Sphenodon, ac-
cording to Osawa (1896) and Howes and Swinnerton (1901), the gastralia
develop without any cartilage basis, and, with the single exception of
Schneider, no one has ascribed any cartilage stage for the gastralia of the
alligators and crocodiles; while Voeltzkow and Déderlein (1901) shows
that in Crocodiles there is no cartilage stage in these structures. In short,
the great bulk of the evidence goes to show that these so-called abdominal
ribs are derma] elements without any cartilage stage.

Wilder explicitly states that the cartilages he describes in the ventral
surface of Necturus lie in the myocommata; that is, entirely deeper than
the skin. He compares them to sternal elements. Hence it would appear
that other evidence than these intermuscular cartilages must be brought
forward to support his thesis.

According to Moodie, Micrerpeton has well developed nasals, pre-
frontals and elongate maxillaries, all of which are lacking in Necturus.
Now if Necturus is to represent the ancestors of the modern Urodeles in
which these same elements are present, we have the difficulty of explaining
how these bones disappeared from the line of descent and then were re-
formed in the later generations.

Cope regarded Necturus as primitive because it possessed what he
called an intercalary bone in the skull, an element which he also recognized
in the Stegocephals. But Kingsbury (1905) says, that, at least in Necturus,
Cope’s intercalary was the caudal extension of the opisthotic.

Nothing is known of the cartilaginous nasal capsules of the Stego-
cephala, so that no comparison can be made between those of Necturus,
and Micrerpeton. However, the complete isolation of the Necturan cap-
sule and its wide separation from that of the other Urodeles, is certainly
one argument against the ancestral position of this animal. Furthermore,
the absence of maxillaries, nasals, and prefrontals in Necturus is one of the
arguments of Kingsbury (1905) in regarding Necturus as a permanent
larva, a conclusion which a study of the nasal capsule suggests.

Moodie (1916, p. 24) says: “The condition found in the skull of Crypto-
branchus alleghaniensis will represent pretty accurately the condition of
most of the coal measures Amphibia.”’ Farther than this no emphasis is
laid upon the primitive condition of Cryptobranchus. However, because
of the simplicity of the nasal capsule, the persistence of the pterygo-
quadrate arch, and also because of the time and manner of the ossification
of the skull, I am inclined to regard Cryptobranchus as more primitive.

As a study of the nasal capsules suggests, the Urodeles are widely
separated from the Anura. Fossil Anura occur in an excellent state of

67) THE NASAL ORGAN IN AMPHIBIA—HIGGINS 67

preservation as far back as the Tertiary. Earlier than this all known fossil
forms are caudate, with the exception of a single specimen, Pelion lyelli,
found in the Carboniferous, which closely resembles recent Salientia.
Should Pelion prove to be a primitive Anuran, then the Urodeles and the
Anura have probably separated from the Stegocephalan ancestor as far
back as the late Devonian or early Carboniferous period.

68 ILLINOIS BIOLOGICAL MONOGRAPHS [68

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1876. On the structure and development of the skull in the Batrachia. Phil. Trans.
Roy. Soc. London, 166:601-669, 9pl.

1877. On the structure and development of the skull in the Urodelous Amphibia. Phil.
Trans. Roy. Soc. London. 167:529-597, 9pl.

1881. On the structure and development of the skull in the Batrachia. Phil. Trans.
Roy. Soc. London. 172:1-266, 44pl.

Peter, Von K.
1898. Die Entwicklung und functionelle Gestaltung des Schidels von Ichthyophis
glutinosus. Morph. Jahrb., 25:555-627, 3pl.
Pinkus, F.
1894. Die Hirnnerven des Protopterus annectans. Morph. Arb., 4:275-346, 7pl.
Pratt, Jutta B.

1897. The development of the cartilaginous skull and of the branchial and hypoglossal

musculature in Necturus. Morph. Jahrb., 25:377-459, 3pl.
SaraAsIN, P. und F.

1890. Ergebnisse naturwissenschaftlicher Forschungen auf Ceylon. Bd. II. Zur Ent-
wicklungsgeschichte und Anatomie der ceylonesischen Blindwiihle Ichthyophis
glutinosus. Wiesbaden, 263 pp., 24pl.

SEWERTZOFF, A.

1897. Beitrag zur Entwickelungsgeschichte des Wirbeltierschadel. Anat. Anz., 13:409-
425.

SEYDEL, Von O. .

1895. Uber die Nasenhdhle und das Jacobson’sche Organ der Amphibien. Morph.
Jahrb., 23:453-543, 22figs.

Stour, P.

1879. Zur Entwickelungsgeschichte des Urodelenschidels. Zeitsch. wiss. Zool., 33:

477-526, 2pl.
StraucH, ALEX.
1870. Revision der Salamandriden-Gattungen. Men. Acad. Imp. Sciences St. Peters-

burg, 16.
Terry, R. J.
1906. The nasal skeleton of Amblystoma punctatum. Trans. Acad. Science, St. Louis.
16:95-124, 4pl.

VoELTzKOW und DODERLEIN.
1901. Beitrige zur Entwicklungsgeschichte der Reptilien, III. Zur Frage nach der Bild-
ung der Bauchrippen. Abh. Senckenb. Naturf. Gesell., 26:313-336, 2pl.
WIepersHEm, R.
1877. Das Kopfskelet der Urodelen. Morph. Jahrb., 3:352-448, 459-548.
1879. Die Anatomie der Gymnophionen. Jena.

70 ILLINOIS BIOLOGICAL MONOGRAPHS (70
Wiper, H. H.
A contribution to the anatomy of Siren lacertina. Zool. Jahrb., Anat., 4:653-

1891.

696, 11ipl.
1892. Die Nasengegend von Menopoma alleghaniense und Amphiuma tridactylum
Zool. Jahrb., Anat., 5:155-176,
The skeletal system of Necturus maculatus. Mem. Boston Soc. Nat. Hist.,
5:387-438, 6pl.

Winstow, Guy M.
1898. Thechondrocranium in the Ichthyopsida. Tufts Coll. Stud., 1:147-201, 4pL.

1903

ZITTEL, K. A.
1887. Handbuch der Palaeontologie. Miinchen.

71)

THE NASAL ORGAN IN AMPHIBIA—HIGGINS

PLATE I

71

72 ILLINOIS BIOLOGICAL MONOGRAPHS

EXPLANATION OF PLATE

Fig. 1.—Dorsal view of model of nasal capsule of Amblystoma punctatum 11 mm. long.
Fig. 2.—Dorsal view of model of nasal capsule of Amblystoma punctatum 20 mm. long.
Fig. 3.—Dorsal view of model of nasal capsule of Amblystoma punctatum 25 mm. long.

Fig. 4.—Side view of model of nasal capsule of Amblystoma punctatum 25 mm. long.

Fig. 5.—Dorsal view of model of nasal capsule of Amblystoma punctatum 34 mm. long.
Fig. 6.—Ventral view of model of nasal capsule of Amblystoma punctatum 34 mm. long.
Fig. 7.—Dorsal view of model of nasal capsule of Amblystoma punctatum 45 mm. long.
Fig. 8.—Ventral view of model of nasal capsule of Amblystoma punctatum 45 mm. long.

ce columna ethmoidalis mni median nasal incisure
ort crista trabeculae pa processus antorbitalis
ca cornu trabeculae pb planum basale

fenn fenestra narina pe pons ethmoidalis

{ni _ foramen nasalis internus pt planum tectale

fo foramen olfactorius fo planum verticale

ins internasal space t trabecula

[72

ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME VI

HIGGINS NASAL ORGAN IN AMPHIBIA PLATE I

73)

THE NASAL ORGAN IN AMPHIBIA—HIGGINS

PLATE II

73

74 ILLINOIS BIOLOGICAL MONOGRAPHS [74

EXPLANATION OF PLATE

Fig. 9.—Dorsal view of model of nasal capsule of Amblystoma punctatum 55 mm. long.

Fig. 10.—Dorsal view of model of nasal capsule of Amblystoma punctatum at the end of meta-
morphosis.

Fig. 11.—Dorsal view of model of nasal capsule of Salamandra maculata 25 mm. long.

Fig. 12.—Dorsal view of model of nasal capsule of Salamandra maculata 38 mm. long.

Fig. 13.—Dorsal view of model of nasal capsule of Salamandra maculata at the end of meta-
morphosis.

Fig. 14.—Dorsal view of model of nasal capsule of Diemictylus viridescens 38 mm. long.

¢ cupola fo foramen olfactorius
co cavum cranii fon foramen orbito-nasalis
ce columna ethmoidalis ins internasal space

cep cephalic process le lamina externa

cp caudal process lm lamina medialis

ct cornu trabeculae pa _ processus antorbitalis
cn external naris pb planum basale

fen eth fenestra ethmoidalis pnp prenasal process
fenic fenestra infra-conchalis pt planum tectale

June foramen nasalis externus fo — planum verticale

tni foramen nasalis internus

ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME VI

HIGGINS NASAL ORGAN IN AMPHIBIA PLATE IJ

75)

THE NASAL ORGAN IN AMPHIBIA—HIGGINS

PLATE ITI

75

76 ILLINOIS BIOLOGICAL MONOGRAPHS

EXPLANATION OF PLATE

Fig. 15.—Dorsal view of model of nasal capsule of an adult Diemictylus viridescens.

Fig. 16—Dorsal view of model of nasal capsule of Triton cristatus 28 mm. long.
Fig. 17.—Dorsal view of model of nasal capsule of Triton cristatus 35 mm. long.

Fig. 18.—Dorsal view of model of nasal capsule of Spelerpes bilineatus 15 mm. long.
Fig. 19.—Dorsal view of model of nasal capsule of Spelerpes bilineatus 37 mm. long.
Fig. 20.—Dorsal view of model of nasal capsule of Spelerpes bilineatus 46 mm. long.

c cupola ins internasal space

ee columna ethmoidalis lm lamina medialis

ort crista trabeculae pa _ processus antorbitalis
ct cornu trabeculae pb _ planum basale

cn external naris pe pons ethmoidalis

fen eth fenestra ethmoidalis pnp prenasal process

fen ic fenestra infra-conchalis pt planum tectale

fo foramen olfactorius t trabecula

fon foramen orbito-nasalis

{76

ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME VI

HIGGINS NASAL ORGAN IN AMPHIBIA PLATE IIT

77)

THE NASAL ORGAN IN AMPHIBIA—HIGGINS

PEATE IV

77

78 ILLINOIS BIOLOGICAL MONOGRAPHS [78

EXPLANATION OF PLATE

Fig. 21.—Side view of model of nasal capsule of Spelerpes bilineatus 46 mm. long.

Fig. 22.—Side view of model of nasal capsule of Cryptobranchus alleghaniensis two weeks old.
Fig. 23.—Dorsal view of model of nasal capsule of Cryptobranchus alleghaniensis five weeks old.

Fig. 24.—Ventral view of model of nasal capsule of Cryptobranchus alleghaniensis three months

old.

Fig. 25.—Dorsal view of model of nasal capsule of Necturus maculatus 25 mm. long.
Fig. 26.—Dorsal view of model of nasal capsule of Necturus maculatus 30 mm. long.
Fig. 27.—Dorsal view of model of nasal capsule of a young adult of Plethodon erythronotus.

c cupola

ce columna ethmoidalis °
ort crista trabeculae

ct cornu trabeculae

en external naris

fne foramen nasalis externus
ins internasal space

le lamina externa
ln lamina medialis

mnt

median nasal incisure
processus antorbitalis
planum basale
prenasal process
pterygoid process
planum tectale
planum verticale
quadrate

trabecula

ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME VI

27
HIGGINS NASAL ORGAN IN AMPHIBIA PLATE IV

79)

THE NASAL ORGAN IN AMPHIBIA—HIGGINS

PLATE V

79

80 ILLINOIS BIOLOGICAL MONOGRAPHS

EXPLANATION OF PLATE

Fig. 28.—Dorsal view of model of nasal capsule of Necturus maculatus 45 mm. long.
Fig. 29.—Dorsal view of model of nasal capsule of a young larva of Amphiuma means.
Fig. 30.—Ventral view of model of nasal capsule of an older larva of Amphiuma means.
Fig. 31.—Dorsal view of model of nasal capsule of Amphiuma means 82 mm. long.

Fig. 32.—Dorsal view of model of nasal capsule of a young larva of Epicrium glutinosum.

Fig. 33.—Dorsal view of model of nasal capsule of Epicrium glutinosum 90 mm. long.

al p alary process fne foramen nasalis externus
¢ cupola fon foramen orbito-nasalis
ce columna ethmoidalis ins internasal space

cep cephalic process le lamina externa

ch choana pa processus antorbitalis

or circumnarial ring pb planum basale

ort crista trabeculae pob preorbital band

ct cornu trabeculae pp pterygoid process

en external naris pv _ planum verticale

fen pr fenestrated process t trabecula

[80

ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME VI

HIGGINS NASAL ORGAN IN AMPHIBIA PLATE V

81]

THE NASAL ORGAN IN AMPHIBIA—HIGGINS

PLATE VI

81

82

ILLINOIS BIOLOGICAL MONOGRAPHS [82

EXPLANATION OF PLATE

Fig. 34.—Dorsal view of model of nasal capsule of a young larva of Pipa americana.

Fig. 35.—Ventral view of the same model of Pipa americana.

Fig. 36.—Dorsal view of model of nasal capsule of Bufo americana 9 mm. body length.

Fig. 37.—Posterior view of anterior half of model of nasal capsule of Bufo americana 9 mm.
body length.

Fig. 38.—Dorsal view of model of nasal capsule of the adult Hyla pickeringii.

Fig. 39.—Side view of model of nasal capsule of the adult Hyla pickeringii.

Fig. 40.—Dorsal view of model of nasal capsule of Rana viridescens 28 mm. total length.

anc
ce
a

alinasal cartilage
columna ethmoidalis
cavum inferius

cavum medium

cavum superius

cornu trabeculae
external naris

fenestra naso-basalis
foramen nasalis internus
foramen olfactorius
foramen orbito-nasalis
internasal space

inferior prenasal cartilage

la

le .
mpq
oc
pe
pb
bp
pt
pu
ge
sa

labial cartilage

lamina externa

muscularis process of quadrate
oblique cartilage

pons ethmoidalis

planum basale

pterygoid process

planum tectale

planum verticale
quadrato-ethmoidalis process
solum anterius

superior prenasal cartilage
trabecula

ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME VI

HIGGINS NASAL ORGAN IN AMPHIBIA PLATE VI

83]

THE NASAL ORGAN IN AMPHIBIA—HIGGINS

PLATE VII

84 ILLINOIS BIOLOGICAL MONOGRAPHS [84

EXPLANATION OF PLATE

Fig. 41.—Transverse section through the anterior part of the nasal organ of Amblystoma punc-
tatum 13 mm. long.

Fig. 42.—Transverse section through the middle region of the nasal organ of the same animal.

Fig. 43.—Transverse section through the choanal region of Amblystoma punctatum 20 mm.
long.

Fig. 44.—Transverse section through the pons ethmoidalis of Amblystoma punctatum 25 mm.
long.

Fig. 45.—Transverse section just anterior to the planum verticale of Amblystoma punctatum

55 mm. long.
Fig. 46.—Transverse section through the planum verticale of same animal.
Fig. 47.—Transverse section through the planum verticale of Amblystoma punctatum at the
end of metamorphosis.
Fig. 48.—Transverse section through the lamina medialis of same animal.
Fig. 49.—Transverse section through the external naris of Salamandra maculata 25 mm. long.
Fig. 50.—Transverse section through the choana of the same animal.
Fig. 51.—Transverse section through the fenestra ethmoidalis of Salamandra maculata 38 mm.

long.

Fig. 52.—Transverse section through the planum basale of Salamandra maculata at the end of
metamorphosis.

ce columna ethmoidalis ng nasal glands

ch choana no nasal organ

ct cornu trabeculae ol olfactory lobe

en external naris p profundus branch of the fifth nerve

fen eth fenestra ethmoidalis pa processus antorbitalis

fo foramen olfactorius pb planum basale

ig intermaxillary gland pe pons ethmoidalis

Ig glands of Jacobson pt planum tectale

jo organ of Jacobson pv — planum verticale

ld lacrimal duct s superficialis of the fifth nerve

lm lamina medialis t trabecula

le lamina externa

ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME VI

HIGGINS NASAL ORGAN IN AMPHIBIA PLATE VII

a =
1
.

ny

a

a
.

a
cn

85)

THE NASAL ORGAN IN AM PHIBIA—HIGGINS

PLATE VIII

85

86

Fig.

Fig.
Fig.

Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.

ILLINOIS BIOLOGICAL MONOGRAPHS [86

EXPLANATION OF PLATE

53.—Transverse section through the foramen olfactorius of Diemictylus viridescens 38 mm.
long.

54.—Transverse section through the anterior part of the nasal organ of the same animal.
55.—Transverse section through the foramen olfactorius of the adult Diemictylus virides-
cens.

56.—Transverse section through the pons ethmoidalis of Triton cristatus 28 mm. long.
57.—Transverse section through the planum basale of Triton cristatus 35 mm. long.
58.—Transverse section through the planum basale of Cryptobranchus alleghaniensis five
weeks old.

59.—Transverse section through the anterior end of the nasal organs of Speler pes bilinea-
tus 15 mm. long.

60.—Transverse section just anterior to the planum basale of S peler pes bilineatus 37 mm.
long.

61.—Transverse section through the same region of Speler pes bilineatus 46 mm. long.
62.—Transverse section through the choanal region of Plethodon erythronotus adult.
63.—Transverse section through the lamina medialis of the same animal.

columna ethmoidalis no nasal organ

choana ol __ olfactory lobe

cornu trabeculae on olfactory nerve

foramen olfactorius oo _ optic organ

foramen orbito-nasalis p profundus of the fifth nerve
intermaxillary gland pb planum basale

organ of Jacobson pe — pons ethmoidalis

lacrimal duct pm __ premaxillary bone

lamina externa pt planum tectale

lamina medialis pv _ planum verticale

maxillary bone s superficialis of the fifth nerve
nasal bone t trabecula

nasal glands v vomer

ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME VI

HIGGINS NASAL ORGAN IN AMPHIBIA PLATE VIII

_ 87)

THE NASAL ORGAN IN AMPHIBIA—HIGGINS

PLATE 1X

87

88

ILLINOIS BIOLOGICAL MONOGRAPHS [88

EXPLANATION OF PLATE

. 64.—Transverse section through the planum basale of Necturus maculatus 30 mm. long.
. 65.—Transverse section through the posterior part of the fenestrated process of Necturus

maculatus 45 mm. long.

. 66.—Transverse section through the planum verticale of the younger larva of Epicrium

glutinosum,

ig. 67.—Transverse section through the same region of a 90 mm. Epicrium.
ig. 68.—Transverse section through the planum basale of the same animal.

Fig. 69.—Transverse section through the planum verticale of the older Amphiuma means larva

Fig. 70.—Transverse section anterior to the planum verticale of Amphiuma means 82 mm.
long.

Fig. 71.—Transverse section through the planum basale of the same animal.

Fig. 72.—Transverse section through the anterior planum basale of a larva of Pipa americana.

Fig. 73.—Transverse section slightly posterior to the above.

Fig. 74.—Transverse section through planum verticale of Pipa americana.

Fig. 75.—Transverse section through the choanal region of Pipa americana.

Fig. 76.—Transverse section through the external naris of Hyla pickeringii.

al p alary process al olfactory lobe

anc alinasal cartilage on olfactory nerve

ce columna ethmoidalis ond dorsal root of olfactory nerve

ch choana onv ventral root of olfactory nerve

ct cornu trabeculae oo — optic organ

€ ethmoid bone ? profundus branch of the fifth nerve

en external naris pb planum basale

eng external nasal glands pf — prefrontal

fen nb fenestra naso-basalis pm premaxillary

fen pr fenestrated process pp pterygoid process

fr frontal ps parasphenoid

tg intermaxillary gland pt planum tectale

jo organ of Jacobson ~v _ planum verticale

le lamina externa s superficialis of the fifth nerve

m maxillary bone spc superior prenasal cartilage

n nasal bone v vomer

7) nasal organ

0c oblique cartilage

ILLINOIS BIOLOGICAL MONOGRAPHS

VOLUME VI

o Ct
“pp :

HIGGINS

NASAL ORGAN IN AMPHIBIA

PLATE IX

89)

THE NASAL ORGAN IN AMPHIBIA—HIGGINS

PLATE X

89

90

ILLINOIS BIOLOGICAL MONOGRAPHS (90

EXPLANATION OF PLATE

Fig. 77.—Transverse section posterior to the external naris of the adult Hyla pickeringii.

Fig. 78.—Transverse section through the lamina externa of the same animal.

Fig. 79.—Transverse section through the choana of a 9 mm. Bufo americana.

Fig. 80.—Transverse section through the fenestra naso-basalis of Bufo.

Fig. 81.—Transverse section slightly anterior to the preceding section.

Fig. 82.—Transverse section through the external naris of the same animal.

Fig. 83.—Transverse section through the muscularis process of the quadrate of Rana viridescens
28 mm. long.

Fig. 84.—Transverse section through the pons ethmoidalis of the same animal.

Fig. 85.—Dorsal view of model of the nasal capsule of a young adult of Rana viridescens.

Fig. 86.—Side view of model of the nasal capsule of the same animal.

amp
anc
cc
ce
ch
crs
ort
fen nb
fon
fs
ag
ipe
jo
Id

anterior maxillary process
alinasal cartilage

cavum cranii

columna ethmoidalis
choana

crista subnasalis

crista trabeculae

fenestra naso-basalis
foramen orbito-nasalis
frontal branch of superficialis
intermaxillary gland
inferior prenasal cartilage
organ of Jacobson
lacrimal duct

lamina externa
muscularis process of quadrate
nasal organ

oblique cartilage

olfactory nerve

planum basale

pons ethmoidalis
pterygoid process

platum tectale

planum verticale
quadrato-ethmoidalis
solum anterius

superior prenasal cartilage
trabecula

ILLINOIS BIOLOGICAL MONOGRAPHS VOLUME VI

HIGGINS NASAL ORGAN IN AMPHIBIA PLATE X

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The nasal organ in Amphibia, ‘
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