A M . ZOOLOCIST, 7:397-413 (1967).
Evolution of the Nasal Structure in the Lower Tetrapods
THOMAS S. PARSONS
Department of Zoology, University of Toronto, Toronto, Ontario, Canada
SYNOPSIS. The gross structure of the nasal cavities and the distribution of the
various types of epithelium lining them are described briefly; each living order of
amphibians and reptiles possesses a characteristic and distinctive pattern. In most
groups there are two sensory areas, one lined by olfactory epithelium with nerve
libers leading to the main olfactory bulb and the other by vomeronasal epithelium
with fibers to the accessory bulb. All amniotes except turtles have the vomeronasal
epithelium in a ventromedial outpocketing of the nose, the Jacobson's organ, and
have one or more conchae projecting into the nasal cavity from the lateral wall.
Although urodeles and turtles possess the simplest nasal structure, it is not possible
to show that they are primitive or to define a basic pattern for either amphibians or
reptiles; all the living orders are specialized and the nasal anatomy of extinct
orders is unknown. Thus it is impossible, at present, to give a convincing picture
of the course of nasal evolution in the lower tetrapods.
Despite the rather optimistic title of this
paper, I shall, unfortunately, be able to do
iittle more than make a few guesses about
the evolution of the nose. I can and will
mention briefly the major features of the
nasal anatomy of the living orders of
amphibians and reptiles, but all of these
are more or less specialized. Truly primitive
amphibians and reptiles are known only
as fossils and, since the nasal capsules are
virtually never ossified in them, their nasal
anatomy cannot be studied directly. It is
possible to attempt working back to a common and hopefully primitive pattern from
the living forms, but such an attempt is
dangerous since it generally involves unlikely assumptions, e.g., that the loss of
structures is uncommon and that secondary
simplification is rare.
The literature on the nose is extensive.
The most important review is that by
Matthes (1934). Other major works include
those of Sarasin and Sarasin (1887-1890,
gymnophionans), Seyclel (1895, amphibians; 1896, turtles), Hoppe (1934, rhynchocephalians), Schuch (1934, urodeles),
Bertau (1935, crocodilians), Helling (1938,
anurans), Malan (1946, squamates), Pratt
I wish to thank Dr. Margaret C. Parsons for
her assistance in the preparation of this manuscript.
Some of the work reported here was supported by
Grant A-1724 from the National Research Council
of Canada.
(1948, squamates), Stebbins (1948, squamates), Bellairs and Boyd (1950, squamates), and Parsons (1959a, reptiles). Most
of the following descriptions are based on
these works, although others, specifically
cited in various places, were also used.
Further references may be obtained from
the bibliographies given by Matthes (1934),
Parsons (1959a), and the other papers
cited.
In the following descriptions and discussion I shall limit myself to a consideration
of the structure of the nasal cavities with
brief comments on their innervation and
development. The structure of the nasal
capsule and the nasal physiology with its
behavioral aspects are also important for
any complete understanding of nasal evolution, but time does not permit their consideration here. Before describing the various groups I should first review the major
subdivisions and structures of the tetrapod
nose.
MAJOR NASAL STRUCTURES
The nasal cavities of most tetrapods may
be divided into three main parts. In most
cases the largest is the central cavum nasi
proprium, a variably shaped but typically
enlarged cavity which is lined, in part, by
the sensory olfactory epithelium. Anterior
to this, between it and the external naris,
(397)
398
THOMAS S. PARSONS
there may be a more or less tubular
vestibulum. The latter is often lined by
squamous epithelium resembling the epidermis and is sometimes said to be formed
from epidermal epithelium rather than
from epithelium derived from the nasal
placode of the embryo, but these characters
are variable or difficult to determine; thus,
the term vestibulum is here used in a gross
morphological sense referring to any moreor-less tubular connection between the external naris and the main portion of the
nasal cavity. Posterior to the cavum nasi
proprium there is commonly another tubular portion, the nasopharyngeal duct,
leading to the choana or internal naris.
Some authors restrict the term nasopharyngeal duct to the channel dorsal to a
well-formed secondary palate, but I will
here use it for any posterior tubular
portion of the nasal cavity and will not, at
this time, consider the very extensive
literature on the types of palates in reptiles
and their relationships to the nasal cavities
(for reviews of this topic see the papers of
Fuchs, 1915, and Parsons, 1959a). Either
the external naris or the choana may enter
the cavum nasi proprium directly in which
case the vestibulum or the nasopharyngeal
duct is not present.
Projections of the lateral nasal wall of
the cavum nasi proprium (or, more rarely,
of the vestibulum) into the nasal cavity are
termed conchae. Although Gegenbaur
(1873) and de Beer (1937) have proposed
different and even mutually exclusive
definitions in an attempt to give greater
precision to this term, I prefer to use
concha in a general sense. Neither of the
restricted definitions assists in the recognition of homologies nor even of general structural similarities and the more
general usage of the term is convenient
(see Parsons, 1959a, for a discussion of
these definitions). Conchae are found only
in amniotes.
The Jacobson's or vomeronasal organ is
frequently an important accessory olfactory
organ in tetrapods. It has been defined in
two different ways. Some authors restrict
the term to a ventromedial outpocketing of
the nasal cavity which forms a distinct
sensory structure; in many cases it becomes
associated with the oral cavity of the adult
and loses its connection with the nasal
cavity. Other workers, most notably Seydel
(1895 and 1896), have considered not only
such distinct outpocketings to be the
Jacobson's organs, but also areas of sensory
epithelium presumably homologous to
them in forms that lack such outpocketings.
Their homology is recognized by three
main characters: first, the sensory epithelium of Jacobson's organ in the broad sense
lacks Bowman's glands while these glands
are present in the olfactory epithelium of
virtually all tetrapods (neotenic urodeles
and one genus of sea snakes are the only
known exceptions); second, the olfactory
nerve fibers from jacobson's organ tend to
lead to the accessory olfactory bulb while
those from the olfactory epithelium lead to
the main olfactory bulb; and, third, Jacobson's organ tends to be ventrally located
while the olfactory epithelium lies mainly
in the dorsal parts of the cavum nasi proprium. Although in this paper I shall use
the first and more restricted definition of
Jacobson's organ, I wish to emphasize the
homology of that organ with those regions
lined by sensory epithelium which meets
the three criteria presented above. Such epithelium is here termed vomeronasal epithelium in contrast to the remaining types of
epithelia found in the cavum nasi proprium, sensory olfactory epithelium and nonsensory respiratory epithelium. In no case
does a tetrapod possess both a true Jacobson's organ and other areas of vomeronasal
epithelium within the nasal cavity.
SARCOPTERYGIAN
FISHES
Since the sarcopterygian fishes are universally accepted as the ancestors of the
tetrapods, it seems logical to start a discussion of the evolution of tetrapod noses with
a few words on their nasal anatomy. Unfortunately, however, such a procedure tells
us essentially nothing about the nasal
cavities of the most primitive land forms.
The best known sarcopterygians are the
lungfish; they have been described most
399
TETRAPOD NASAL STRUCTURE
recently by Bertmar (1965 and 19666) and
Thomson (1965). In the Dipnoi the nasal
cavities are basically like those of most
other fish and show few, if any, tetrapod
characters. They are relatively simple sacs
with numerous olfactory folds or lamellae.
Although the posterior nostril does open
into the oral cavity, there is general agreement that this opening does not correspond
to the choana of tetrapods, a structure completely lacking in the lungfish. Various
workers have described different parts of
the dipnoan nasal cavity as a Jacobson's
organ, but Bertmar (1965) has shown that
there is no evidence for the existence of any
such organ in lungfish except, possibly, for
Rudebeck's (1944) report of a rudimentary
accessory olfactory bulb. I am unconvinced
by Rudebeck's description and doubt that
an accessory bulb is present.
The crossopterygians include the actual
ancestors of tetrapods and are thus of great
interest. The only living representatives of
this order are coelacanths, a highly divergent group in which the nasal cavities lack
choanae and bear little resemblance to
those of tetrapods. Rhipidistians, which
presumably did resemble primitive tetrapods, are extinct and therefore only their
skeletal anatomy can be studied. Jarvik
(1942), in a very detailed study of the
snout of these forms, believed that some of
them, the Osteolepiformes of his classification, showed marked resemblances to the
modern Anura while others, the Porolepiformes, were more similar to the Urodela.
However Thomson (1964) has questioned
the validity of Jarvik's conclusions and
does not accept the division of the rhipidistians into osteolepiforms and porolepiforms in Jarvik's sense. Both authors reported certain ridges and depressions in the
bony wall of the nasal capsule; although
Jarvik tried to correlate these with soft
structures of the nose, Thomson stated (p.
347) that "It is not possible to decide with
any degree of certainty whether or not the
apparent morphological subdivisions of the
nasal capsule represent any functional anatomical features of the nasal sac." Jarvik
believed that he could demonstrate the
presence and, to a certain extent, the shape
of a Jacobson's organ in some rhipidistians,
but, on the basis of Thomson's study, I feel
that any such identification of Jacobson's
organ must be considered extremely tentative although quite possibly correct. In
any event the uncertainty is great enough
to make further speculation on rhipidistian
noses unprofitable for the purposes of this
paper; for detailed descriptions, speculations, and references, see the papers by
Jarvik (1942) and Thomson (1964).
URODELA
The nasal cavities of many urodeles are
very simple (Fig. 1). There is little or no
vestibulum and no nasopharyngeal duct.
In most forms, such as Triturus and Salamandra, the cavum nasi proprium consists
of a rather large, dorsoventrally-flattened,
ovoid chamber. Along much of its lateral
or ventrolateral margin, there is a lower,
lateral, groove-like extension (Figs. 1A and
B); this extension is termed the "seitliche
Nasenrinne" in most of the German literature and the lateral nasal sinus in the English. The lachrymal duct enters the
anterior part of this sinus. Its posterior
half bears vomeronasal epithelium and thus
is often called the Jacobson's organ. Olfactory epithelium covers much of the
dorsal and ventral walls plus the anterior
part of the medial wall of the main portion
of the cavum nasi proprium. Vomeronasal
epithelium occurs laterally and ventrolaterally in the posterior half of the lateral
nasal sinus and the remaining parts of the
cavum are lined by respiratory epithelium.
Although the pattern just described may
be considered typical for fully metamorphosed forms, considerable variation is
seen when the neotenic urodeles are considered. Some, such as neotenic Ambystoma
(axolotls), resemble the metamorphosed
forms closely and others, such as Proteus,
have much simplified nasal cavities with no
lateral nasal sinus. Siren (Fig. 1C) is quite
distinctive, having an inverted T-shaped
"lateral nasal sinus" which lies ventral to
the medial half of the main portion of the
cavum nasi proprium. In many neotenic
400
THOMAS S. PARSONS
CNP
LNS
CNP
CNP— 1
I— LNS
FIG. 1. A. Dorsal view of the ventral half of
the nasal cavity of Triturus (mainly after Matthes,
1934, and Schuch, 1934). B. Transverse section
through the nasal cavity of Triturus (after Seydel,
1895). In this and subsequent figures of sections,
olfactory epithelium is lined, vomeronasal epi-
thelium is cross-hatched, and non-sensory epithelium
is solid black. C. Transverse section through the
nasal cavity of Siren (after Seydel, 1895). D. Diagram of the nasal area of a urodele in transverse
section showing the nasal innervation (after Parsons, 19596).
urodeles the nasal epithelium is thrown
into moderately high folds, quite similar to
the olfactory folds of fish, and Bowman's
glands are often completely lacking in the
olfactory epithelium. Not all the neotenous
forms have been studied in detail and the
extent of the variation in them cannot be
stated.
The olfactory and vomeronasal epithelia
give rise to nerve fibers which extend
posteromcdially to enter the main and accessory olfactory bulbs, the latter being a
rather indistinct posterior prolongation of
the lateral side of the main olfactory bulb.
All of the fibers from the vomeronasal
epithelium pass ventral to the nasal cavity
in their path to the bulb and tend to enter
the accessory bulb while those from the olfactory epithelium may pass either dorsal
or ventral to the nasal cavity and tend to
enter the main bulb (Fig. ID). Herrick
(1921) gave the most detailed description
of the olfactory nerves and bulbs in a
urodele and stated that the separation of
the fibers from the olfactory and vomeronasal epithelia was not complete.
There is a very extensive literature on
the embryology of the nasal cavities of
urodeles. Most of it concerns the method of
formation of the choanae, which is quite
different from that seen in amniotes and
has caused some workers to deny the
homology of the choanae in the two groups.
Bertmar (1966a) has restudied this problem and concluded that the choanae are
indeed homologous in all tetrapods; the
reader is referred to his paper for a discussion of the earlier work and many refer-
401
TETRAPOD NASAL STRUCTURE
CNP
B
CNP
CH
FIG. 2. A. Ventral view of a model of the left
nasal sac of Ichthyophis (after Sarasin and
Sarasin, 1887-1890). B. Transverse section through
the nasal cavity of Ichthyophis (after Sarasin and
Sarasin, 1887-1890). C. Transverse sections through
the nasal cavity of a larval Ichthyophis (after
Sarasin and Sarasin, 1887-1890). The midline is to
ihe left; the section to the upper left is the most
anterior and that to the lower right the most
posterior.
ences. It appears most probable that there
are no basic differences between the nasal
cavities of urodeles and those of other
tetrapods, but that the urodeles have considerably modified (specialized) the developmental processes leading to the adult
configuration.
medial three-quarters of the cavum and
respiratory epithelium the lateral quarter.
The external naris enters the anterior end
of the nasal cavity and the choana enters
the oral cavity from the posterolateral corner of the cavum nasi proprium. Anterior
to the choana and ventral to the cavum
there is a diverticulum lined by respiratory
epithelium. Just dorsal to this diverticulum, a tubular structure enters the medial
choanal wall. The tube immediately turns
anteriorly and then laterally so that it extends transversely beneath the lateral half
of the cavum; the lachrymal duct enters its
lateral end. Vomeronasal epithelium forms
the ventral wall of this tube which is, therefore, generally termed the Jacobson's
organ.
The innervation of the gymnophionan
nose is not well known but appears to resemble that of urodeles. A small accessory
olfactory bulb is present laterally, and the
vomeronasal epithelium sends nerve fibers
to the ventral branch of the olfactory nerve;
whether or not the fibers entering the ac-
GYMNOPHIONA
Ichthyophis is the best known gymnophionan and almost all of the following
description is based on it; the other genera
which have been studied appear to be
basically similar.
There is essentially no vestibulum and,
although the posterior connection to the
choana is slightly drawn out, no wellmarked nasopharyngeal duct. The cavum
nasi proprium is a large, dorsoventrallyflattened chamber (Figs. 2A and B), more
or less triangular in shape with the apex
anterior. Its ventral wall bulges dorsally
into the cavity, forming an olfactory eminence resembling somewhat that found in
anurans. Olfactory epithelium lines the
402
THOMAS S. PARSONS
A.
MC
LD
FIG. 3. A. Posterior view of the anterior half
of a model of the left nasal cavity of Bufo (after
Matthes, 1934). B. Anterior view of the posterior
half of a model of the left nasal cavity of Bufo
(after Matthes, 1934). C. Tranverse section through
the nasal cavity of Alytes (after Helling, 1938).
D. Transverse section through the nasal cavity of
Pipa (after Matthes, 1934). E. Diagram of the
nasal area of an anuran in transverse section showing the nasal innervation.
cessory olfactory bulb are those from the
vomeronasal epithelium has not, to my
knowledge, been clearly demonstrated, but
it appears likely judging by the situation
in other tetrapods.
The embryology of the nasal cavity of
gymnophionans is of interest because in
some ways it resembles that of amniotes
and in others that of urodeles and anurans.
The basic pattern is like that of amniotes: the nasal placode becomes indented
to form a nasal pit, the pit lengthens and
extends posteriorly into the roof of the oral
cavity, and lateral and medial nasal processes grow ventrally and fuse ventral to
the center of the pit, thus separating the
anterior external naris from the posterior
choana. According to Sarasin and Sarasin
(1887-1890), Jacobson's organ first appears
as a ventral or even ventromedial outgrowth of the nasal cavity which later
becomes displaced laterally although it en-
ters the medial side of the choana at all
stages. Transverse sections through the
anterior part of the nasal region of larvae
show a structure similar to that of urodeles,
while posteriorly they resemble sections of
amniote embryos (Fig. 2C).
ANURA
Anurans possess the most complex nasal
cavities of any amphibians. There is no
nasopharyngeal duct and little or no vestibulum, but the cavum nasi proprium is
typically subdivided into a series of three
chambers or cavities (Fig. 3).
Dorsally and somewhat medially there is
a large, nearly spherical, principal cavity.
In most cases the floor of this cavity forms
an olfactory eminence projecting into the
cavity; the eminence may be either a
simple, more-or-less hemispherical swelling
or a thinner, lamellar projection, the
dorsal end of which frequently curves
403
TETRAPOD NASAL STRUCTURE
either medially or laterally and thus resembles the conchae found in amniotes.
The external naris may enter the principal
cavity directly (Fig. 3A) or there may be a
vertical flap of tissue separating off a vestibulum, the latter sometimes entering the
more ventral middle cavity (Fig. 3C). The
choana enters the oral cavity from the
posterolateral corner of the floor of the
principal cavity.
Ventral to the anterolateral portion of
the principal cavity there is a small middle
cavity (all of these parts of the nose have
been given many names; I shall not attempt to mention the numerous synonyms
here). This cavity, which is dorsoventrally
flattened, is connected to the principal
cavity dorsolaterally and to the inferior
cavity ventromedially. The lachrymal duct
enters its posterolateral end. As noted
above, if a vestibulum is formed it may enter the middle cavity rather than the principal cavity. The third and most complex
chamber is the inferior cavity. This is a
large, dorsoventrally-flattened chamber lying ventral and ventrolateral to the principal cavity and posteroventral to the middle
cavity. Anteriorly it is connected to the ventromedial end of the middle cavity, and
farther posteriorly it is narrowly connected
to the principal cavity and enters the
choana. The inferior cavity is commonly
divided into two main parts, a smaller
medial recess and a much larger lateral
recess.
Olfactory epithelium lines almost all of
the principal cavity except for its lateral
side where it is connected to the external
naris, choana, and other chambers. Vomeronasal epithelium is found only in the
medial recess of the inferior cavity which
is thus frequently termed Jacobson's organ.
The remainder of the nasal cavity, the
lateral portion of the principal cavity, all
of the middle cavity, and most of the inferior cavity including all of its lateral
recess, is lined by respiratory epithelium.
There is considerable variation among
the anurans, but most of it is in details of
the pattern described above. However,
some forms are quite different. For exam-
ple, in Pipa the cavum nasi proprium is a
relatively simple, dorsoventrally-flattened
chamber which has a narrow lumen lined
by respiratory epithelium along its center,
but wider lumina and olfactory epithelium
both medially and laterally (Fig. 3D). The
vomeronasal epithelium is restricted to a
small diverticulum that projects anterolaterally from the posterolateral part of the
nasal cavity.
Anurans possess a small accesssory olfactory bulb located on the lateral surface
of the forebrain posterior to the main olfactory bulb. According to McCotter
(1917) and others, nerve fibers from the
vomeronasal epithelium run to the accessory bulb, and fibers from the olfactory
epithelium to the main bulb with little
mixing although they are in contact for
part of their course (Fig. 3E).
Most studies of anuran nasal embryology
have been concerned largely with the development of the choanae. In general, the
process is similar to that seen in urodeles
and, although anurans have not been
much studied recently so definite statements cannot be made, it seems probable
that Bertmar's (1966a) findings on urodeles
are also applicable to anurans and that,
despite the peculiarities in their development, anuran choanae are homologous
with those of other tetrapods.
TESTUDINES
The nasal cavities of most turtles are
relatively simple. There is a short tubular
vestibulum leading posteriorly from the
external naris to the cavum nasi proprium
and, posteriorly, a nasopharyngeal duct of
variable length connecting the cavum and
the oral cavity. At the posterior end of this
duct there is frequently a flap or one or
more papillae along the lateral margin of
the choana. In some forms the nasopharyngeal duct has a small anterolateral
recess. The cavum nasi proprium may be
divided into two parts, a posterodorsal olfactory region and a ventral intermediate
region. Both the vestibulum and the nasopharyngeal duct are connected to the latter
region (Fig. 4A).
404
THOMAS S. PARSONS
A.
FIG. 4. A. Medial view of the lateral wall of
the nasal cavity of Emys (after Seydel, 1896).
B. Transverse section through the nasal cavity
of Emys (after Seydel, 1896). C. Medial view of
the lateral wall of the nasal cavity of Chelonia
(after Parsons, 1959a). D. Diagram of the nasal
area of a turtle in transverse section showing the
nasal innervation (after Parsons, 1959b).
The olfactory region is a large, relatively
simple cavity, roughly hemispherical but
flattened lateromedially. Its ventral side
is open to the intermediate region from
which it is normally separated by low
ridges. On the lateral wall of the olfactory
region there may be a rather low and
generally quite indistinct projection into
its lumen; this has been called a concha,
but it does not closely resemble the conchae
of other forms and I prefer to call it the
Muschelwulst.
The intermediate region varies. In most
turtles it is a large and quite simple chamber with various low ridges along its walls.
These ridges separate a series of shallow
sulci. In emydines and Chelydra there is a
crescentic anterior sulcus and, posterior to
that, three or four longitudinally arranged
sulci (Fig. 4B), but tortoises appear to have
only a single sulcus along the medial
wall of the intermediate region. In sea
turtles the intermediate region is a narrower, almost duct-like structure with
prominent dorsal and ventral recesses anteriorly (Fig. 4C).
Almost all of the olfactory region is lined
by olfactory epithelium. Vomeronasal epithelium lines the sulci of the intermediate
region or, in sea turtles, the recesses of that
region. The ridges between the olfactory
and intermediate regions and between the
sulci (or in sea turtles the walls of the
tubular portion of the intermediate region) bear respiratory epithelium. The
vestibulum is lined mainly by stratified
squamous epithelium but may have respiratory epithelium posteriorly, and the
nasopharyngeal duct has respiratory or
other non-sensory epithelium.
TETRAPOD NASAL STRUCTURE
Turtles possess a large accessory olfactory
bulb that lies posterodorsal to the main
olfactory bulb. The nerve fibers from all of
the vomeronasal epithelium plus those
from the olfactory epithelium of the medial wall of the olfactory region form the
medial trunk of the olfactory nerve most of
whose fibers lead to the accessory bulb.
Fibers from the dorsal and lateral walls of
the olfactory region form the lateral trunk
of the olfactory nerve which enters the
main bulb (Fig. 4D). There is some dispute
over the exact arrangement of the nerve
trunks and the degree of separation between the fibers from the different regions
of the nasal cavity, but most workers have
thought that all fibers from the vomeronasal epithelium reach the accessory bulb
and all those from the olfactory epithelium
the main bulb (see Parsons, 1959a, for further discussion and citation of varying opinions on these points).
The nasal embryology of turtles is quite
simple. The nasal placode becomes indented to form a nasal pit. This pit elongates so that its posterior end comes to
lie in the roof of the oral cavity. Medial
and lateral nasal processes develop, extending ventrally on either side of the
nasal pit and eventually fusing ventral to
the middle of the pit. This fusion separates
the anterior external naris from the
posterior choana and converts the nasal
cavity into a chamber with a restricted
opening at each end. The various ridges
along the surface of the cavum nasi proprium form gradually in place until the
adult configuration is reached. In some
turtles there is considerable development
of a secondary palate (in a broad sense)
and hence elongation of the nasopharyngeal
duct.
KHYNCIIOCEI'IIALIA
The nasal anatomy of Splienodon has
been studied by few workers and many
details of its structure are not well known.
The vestibulum is a very short tube leading
medially from the external naris to the
large cavum nasi proprium. The latter
chamber opens ventrally, throughout the
405
greater part of its length, into the oral
cavity through the long choana; there is no
nasopharyngeal duct (Fig. 5A). Although
the cavum nasi proprium opens into the
mouth, the opening is not straight (Fig.
5B). The ventral end of the nasal septum
projects laterally forming a vomerine
cushion and, just ventral to that, choanal
folds project medially from the lateral
margins of the palate. This arrangement
presumably prevents food particles from
becoming lodged within the nasal cavities.
The large cavum nasi proprium has two
incompletely separated conchae projecting
into it from the lateral wall. The anterior
concha is attached along a line from just
posterior to the external naris to the middle of the cavum and slopes from anterodorsal to posteroventral. From its posterior
end, the posterior concha continues posterodorsally, extending nearly to the posterior end of the cavum. The free margins
of the conchae, especially the posterior one,
tend to curl ventrally. Several different
parts of the cavum are defined on the basis
of their relationships to the conchae, but
they need not be considered here.
Jacobson's organ is a tubular structure
lying along the nasal septum and opening
into the anteroventral part of the medial
wall of the cavum nasi proprium through a
narrow connection near its anterior end.
The lachrymal duct enters the lateral wall
of the cavum opposite it. Some authors
have disagreed on the exact nature of the
connections of these structures, but the
statements just given represent the most
widely held opinions.
Olfactory epithelium lines the dorsal
half of the cavum nasi proprium, roughly
the dorsal surfaces of the conchae and those
parts dorsal to the conchae, and vomeronasal epithelium is restricted to the roof of
Jacobson's organ. The ventral half of the
cavum and the floor of Jacobson's organ
bear respiratory epithelium and the vestibulum is lined by stratified squamous epithelium.
Splienodon possesses a small accessory olfactory bulb located well posteriorly on
the dorsomedial wall of the main olfactory
406
T H O M A S S. PARSONS
FIG. 5. A. Medial view of the lateral wall o£
the nasal cavity of Sphenodon (after Hoppe, 1934).
B. Transverse section through the nasal cavity of
Sphenodon (after Hoppe, 1934). C. Transverse section through the nasal area of an embryo of
Thamnophis shortly before the fusion of the nasal
processes (after Parsons, 1959a). D. Transverse section through the nasal area of an embryo of Thamnophis shortly after the fusion of the nasal processes (after Parsons, 1959a).
bulb. The nerve fibers from Jacobson's
organ mingle with those from the olfactory
epithelium and have, to my knowledge,
never been traced to their connections in
the brain (Parsons, 1959a). Presumably, as
in other forms, fibers from Jacobson's
organ enter the accessory bulb while those
from the cavum nasi proprium lead to the
main bulb.
The nasal embryology of Sphenodon
resembles that of all amniotes with the exception of turtles. The external naris and
choana are separated as in turtles, but two
further processes occur at roughly the same
time. Shortly before the lateral and medial
nasal processes fuse, an outpocketing of the
ventromedial wall of the nasal pit appears.
This outpocketing becomes the Jacobson's
organ of the adult and its size and rate of
development reflect its adult condition; it
is very small in forms, such as crocodilians
and birds, which lack this organ as adults
and very large in those, such as most
squamates (Fig. 5C), in which it is prominent in adults. At about the same time
or very shortly thereafter, the concha first
appears as an inpocketing of the lateral
nasal wall (Fig. 5D). In Sphenodon
Jacobson's organ retains its embryonic
position as an outpocketing of the ventromedial nasal wall, but the development
of the concha is more complex. Certainly
the posterior concha of the adult forms
from the original embryonic concha. Since
the two conchae are always continuous, the
anterior one also probably develops from
TETRAPOD NASAL STRI'CTURE
407
FIG. 6. A. Medial view of the lateral wall of
the nasal cavity of Lacerta (after Leydig, 1872).
B. Transverse section through the Jacobson's organ of Anguis (mainly after Bellairs and Boyd,
1950). C. Transverse section through the nasal
cavity of Anguis (after Bellairs and Boyd, 1950).
D. Lateral view of the dissected nasal cavity of
Callisaurus (after Stebbins, 1948). E. Diagram of
the nasal area of a squamate in transverse section
showing the nasal innervation (after Parsons,
19596).
the original concha, but it is possible that
the anterior concha is a new and separate
structure that is found only in Sphenodon.
prominent concha projecting medially
from its lateral wall (Fig. 6C). As in
Sphenodon, numerous parts of the cavum
may be recognized, but they are not important for this study. Posteriorly, in snakes
and some lizards, there may be a short nasopharyngeal duct, but in most lizards the
cavum nasi proprium enters the oral cavity
directly. The choana may either be short
and lie ventral to the posterior end of the
cavum or it may be a long slit-like opening
resembling that of Sphenodon; in either
case its structure is similar to that of
Sphenodon with a vomerine cushion at the
base of the nasal septum and a medially
projecting choanal fold ventrolateral to it.
Jacobson's organ is a separate, roughly
spherical structure lying ventral to the
posterior part of the vestibulum or the an-
SQUAMATA
The Squamata are by far the largest and
most diversified order of living reptiles and
their nasal anatomy, as might be expected,
shows considerable variation. There is,
however, a general pattern which, despite
numerous modifications in various forms,
does appear to be typical for the group.
This may be seen in Leydig's (1872) oftencopied drawing of Lacerta (Fig. 6A).
The vestibulum is a relatively small but
distinct chamber entered anterolaterally by
the external naris and connecting posteriorly with the cavum nasi proprium.
The latter is a large chamber with a single
408
THOMAS S. PARSONS
terior part of the cavum (Fig. 6B). Its ven- Stebbins (1948) has studied this variation
Lral side is normally invaginated to form a in a series of lizards and shown that vestilarge mushroom body which fills most of bular modification is often related to the
the organ and leaves only a narrow lumen. prevention of sand entering the nasal cavFrom the posteroventral part of Jacobson's ities in desert-inhabiting forms. Iguanids
organ there is a very narrow duct leading and agamids show the greatest range of
to the palate and entering the oral cavity vestibular structures, but members of sevanterior to the choana; there is, in the eral other lizard families may also be
adult, no direct connection between Jacob- greatly modified.
son's organ and the remainder of the nasal
Squamates typically have a very large accavity. The lachrymal duct enters the duct cessory olfactory bulb which lies posterior
of Jacobson's organ, the choana or other and medial or dorsomedial to the main
adjacent parts of the nasal cavity or palate, olfactory bulb. The nerve fibers from
or both.
Jacobson's organ form a quite sharply
In forms such as that described, olfactory separate part of the olfactory nerve, the
epithelium lines the dorsal or posterodorsal vomeronasal nerve, leading to the accesparts of the cavum nasi proprium, roughly sory bulb, and fibers from the olfactory
the dorsal surface of the concha and parts epithelium of the nasal cavity form another
dorsal or posterior to the concha. Vo- trunk leading to the main bulb (Fig. 6E);
meronasal epithelium is restricted to the there appears to be very little if any interroof and sides of Jacobson's organ. The change of fibers between the two trunks.
floor of Jacobson's organ, the ventral and The degree of development of the accessory
anterior parts of the cavum nasi proprium, and main bulbs is closely correlated with
and the nasopharyngeal duct (if present) the amounts of vomeronasal and olfactory
all bear respiratory epithelium. Stratified epithelia.
squamous epithelium typically lines the
The nasal embryology of squamates is
vestibulum, but that region is quite vari- essentially as described in the section on
able and other epithelial types may occur Sphenodon. Only one concha, developed
there.
from the embryonic concha, is present. The
Although the pattern just described does only complication is that the anterior part
seem to be typical for squamates as a of the embryonic choana becomes closed in
whole, there are numerous variants. Snakes such a way that a small anterior remnant
are apparently a rather homogeneous is left as the duct of Jacobson's organ
group; the vestibulum is short, Jacobson's which is thus separated from the adult
organ is very well developed, and a short choana. The posterior extent of such
nasopharyngeal duct is present. In aquatic closure or fusion varies, causing the variforms the concha may be lost and the ation in the size and position of the adult
amount of olfactory epithelium greatly choanae already mentioned.
reduced. Lizards are more variable. The
CROCODILIA
olfactory areas, the concha, and Jacobson's
organ may be poorly developed or even, as
Crocodilians possess exceedingly complex
in some chameleontids, completely absent; nasal cavities with a large number of recessuch a general reduction in the olfactory ses and accessory sinuses opening off the
apparatus seems most frequently to be main chamber. All of the genera which
associated with arboreal habits although have been studied are very similar and one
many arboreal forms have very well devel- description will suffice for the Order. The
oped nasal organs. The greatest variation vestibulum is a short vertical tube leading
occurs in the vestibulum which may be- ventrally from the external naris to the
come greatly elongated and even overlie the anterior end of the large cavum nasi procavum nasi proprium and enter the pos- prium. From somewhere near the middle
terior end of the latter chamber (Fig. 6D). of the floor of the latter chamber a very
409
TETRAPOD NASAL STRUCTURE
l—ECR
EN
EN
— PRC
PTC—I
-CO
FIG. 7. A. Medial view of the lateral wall of
the nasal cavity of Alligator (after Parsons, 1959a).
B. Diagrammatic dorsal view of the nasal cavity
of a crocodilian showing the various recesses and
sinuses (mainly after Bertau, 1935).
long and narrow nasopharyngeal duct
leads posteriorly to the choana. Crocodilians have a fully formed secondary
palate so that the choanae enter the posterior end of the oral cavity. Jacobson's
organ is completely lacking in adults and
the lachrymal duct enters the lateral wall
of the cavum nasi proprium near the anterior end of the latter.
There are three conchae projecting into
the cavum from its lateral wall (Fig. 7A).
The preconcha and the concha are elongated and partially connected while the
postconcha is an isolated oval structure
bulging into the lumen. The preconcha
and concha are separated by a preconchal
recess and the concha and postconcha by an
extraconchal recess; both are really part
of the cavum nasi proprium. All of the
other spaces are outgrowths of the cavum
comparable to the accessory sinuses of mammals (Fig. 7B). They are the anteroventral
maxillary sinus, the caviconchal recess lat-
eral to the concha, the postconchal cavity
within the postconcha, the postturbinal sinus connecting the extraconchal recess and
the postconchal cavity, and the posterolateral recess lying ventrolateral to the postconcha. The last recess is found in Alligator and Melanosuchus but not in Crocodylus.
Olfactory epithelium lines the parts of
the cavum nasi proprium dorsal and
posterior to the conchae, including the
dorsal surfaces of the conchae and the dorsal parts of the preconchal and extraconchal recesses. Respiratory epithelium lines
the more anterior and ventral parts of the
cavum and all of the accessory sinuses.
There is no vomeronasal epithelium. Stratified squamous epithelium is found in the
vestibulum, and some non-sensory epithelium, not to my knowledge well described, lines the nasopharyngeal duct.
Correlated with the absence of Jacobson's
organ is the lack of any accessory olfactory
410
THOMAS S. PARSONS
bulb in crocodilians. Nerve fibers from the
olfactory epithelium lead, as in all cases, to
the olfactory bulb.
The nasal embryology of crocodilians is
complex (Bertau, 1935). The embryonic
outpocketing of the nasal pit which in
other amniotes forms Jacobson's organ is
poorly developed and quickly disappears.
Both the preconcha and concha develop
from the single early embryonic concha,
but the postconcha is a separate structure
at all stages and forms as an inpocketing
of the posterolateral nasal wall; it has no
apparent homologue in other reptiles. The
various accessory sinuses and recesses are
outpocketings of the nasal cavity and tend
to appear only in quite late embryonic
stages, slowly enlarging to reach the adult
condition.
HIGHER TETRAPODS
Although birds and mammals fall outside the scope of this paper, both are
descended from reptiles and hence a brief
survey of their nasal structure may be helpful before considering the evolutionary
history of reptilian noses. However, no attempt will be made to show the range of
variation or to describe any details of their
nasal anatomy.
Birds commonly possess a relatively large
vestibulum which is not grossly distinct
from the cavum nasi proprium. There is
no nasopharyngeal duct and the cavum
enters the oral cavity directly. As in crocodilians there are three conchae along the
lateral nasal wall. Although the concha and
postconcha are essentially the same in the
two groups, the preconchae are very different; as already noted the crocodilian
preconcha forms as part of the concha and
lies in the cavum nasi proprium, but the
avian preconcha is an independent structure of vestibular origin. Jacobson's organ
is lacking and the olfactory epithelium is
generally reduced in extent. The kiwi is an
exception in having a well developed olfactory sense and a series of olfactory conchae in place of a single postconcha.
Mammals are very variable. Some, such
as whales and bats, have reduced olfactory
organs, but in most the nasal cavities are
well developed. The vestibulum is defined
histologically and is rarely a grossly separable chamber. Within the large cavum nasi
proprium there are a number of conchae:
the anteroventral maxilloturbinal which
appears to represent the embryonic concha,
a more dorsal nasoturbinal, and a series of
more posterior ethmoturbinals. There are
also several accessory sinuses within the
bones surrounding the nose. The nasopharyngeal duct is long and the secondary
palate well developed. Jacobson's organ is
usually present as a quite small tubular
structure lying along the nasal septum. In
the adult, it may be connected to the nasal
cavity, to the oral cavity, or to both. Nerve
fibers from Jacobson's organ lead to an
accessory olfactory bulb, while those from
the nasal cavity lead to the main olfactory
bulb as in other forms.
DISCUSSION: TETRAPOD NASAL EVOLUTION
From the descriptions just given, it seems
clear that most tetrapods have two quite
distinct sensory areas in the nose. One is
lined by olfactory epithelium with Bowman's glands, typically sends nerve fibers to
the main olfactory bulb, and is more or less
dorsally located; the other, Jacobson's organ in a broad sense, is lined by vomeronasal epithelium without Bowman's glands,
typically sends nerve fibers to the accessory
olfactory bulb, and is more or less ventrally,
most commonly ventromedially, located.
Although some forms have lost one or both
sensory areas secondarily, this division does
seem to be primitive for tetrapods. Fish,
on the other hand, do not show any comparable separation of sensory areas. No
living fish, to my knowledge, has any Bowman's glands nor is there ever a division of
the olfactory bulb into main and accessory
bulbs (as already noted, I do not accept
Rudebeck's, 1944, suggestion of such a
separation in lungfish). Presumably, therefore, the distinction between olfactory and
vomeronasal areas first appeared either in
primitive amphibians or in their rhipidistian ancestors. The first alternative is
suggested by the incomplete separation of
TETRAPOD NASAL STRUCTURE
the areas in modern urodeles in which the
accessory olfactory bulb is poorly developed, and the second by Jarvik's (1942)
studies on crossopterygians; none of the
evidence is really convincing, and the time
of origin of Jacobson's organ or equivalent
structures cannot at present be determined.
Much of the more recent history of these
areas seems to be almost as obscure as their
origins, but there does seem to be a common pattern with modifications in all
amniotes with the exception of turtles; in
all these forms Jacobson's organ appears as
a ventromedial outpocketing of the early
embryonic nasal cavity and, at an almost
equally early stage, a single lateral concha
is formed. Thus, it seems logical to postulate an ancestral form whose nasal anatomy resembled closely that of Sphenodon
except that it had only a single concha
resembling that of a squamate. The changes
from such a form that may have occurred
in the evolution of the living groups can
quickly be summarized. In rhynchocephalians a second or anterior concha developed
either by the splitting of the original
concha or as a new projection from the
lateral nasal wall. In squamates the anterior part of the choana became partially
closed isolating Jacobson's organ and its
duct from the rest of the nasal cavity; in
some forms the fusion was extensive enough
to produce a short secondary palate (the
last in a broad sense). Archosaurs lost
Jacobson's organ, developed a new posterior projection of the lateral nasal wall,
the postconcha, and then divided into several lines, two of which survive. In one, the
crocodilians, the original concha became
divided into a preconcha and a concha, and
a large secondary palate was formed; in the
other, the birds, a vestibular concha
evolved. Finally in the mammal-like reptiles more conchae, the nasoturbinal and
ethmoturbinals, were formed and a secondary palate developed.
This scheme leaves the position of the
turtles in doubt. They do not have any
normally developed concha; although the
Muschelwulst and various ridges have been
thought to represent the concha, there is no
411
real evidence that any of them does.
Neither do turtles have a true Jacobson's
organ; rather the vomeronasal epithelium
lines a sizable portion of the main nasal
chamber. I have, therefore, suggested
(Parsons, 1959£>) that turtles diverged from
the primitive reptilian stock before any
of the other surviving groups of amniotes.
Such a suggestion agreed well with certain
opinions then current on the early evolution of reptiles (Olson, 1947) although it
was in marked disagreement with other
theories (e.g., those of Watson, 1957). A
more recent paper by Olson (1965) has
shown fallacies in the earlier work on
reptilian phylogeny, but has not clarified
the phylogenetic position of the turtles. It
is possible that turtles are descended from
a stock possessing the normal amniote nasal
characters and that they have lost the
concha and secondarily replaced Jacobson's
organ with a simpler structure, but I find
this hard to believe. However no theories
based on the changes in a single organ are
reliable and, until further palaeontological
evidence is available, the phylogenetic position of turtles and the evolutionary history
of their nasal cavities will probably remain
unknown.
The situation with regard to the three
orders of living amphibians is similar.
There are several theories concerning their
phylogeny (Parsons and Williams, 1963),
but none of them is supported by enough
evidence to be really convincing. Each of
the three orders has a distinctive pattern of
nasal anatomy, and, in the absence of evidence showing their probable relationships,
it hardly seems worthwhile to try to imagine intermediate morphological stages. The
nasal history of the amphibians is further
complicated by the occurrence of neoteny,
with consequent aquatic life and the related nasal modifications, in many groups
of urodeles and by the considerable differences in the early nasal embryology of
anurans and urodeles as compared with all
other tetrapods.
Thus, I am really unable to add anything important to the discussion of nasal
evolution in primitive tetrapods that I
412
THOMAS S. PARSONS
wrote seven years ago. Certainly urodeles
and turtles have the simplest nasal cavities
and are very similar. One possible theory is
that they are primitive and that all other
groups have gradually added further complexities. Such a theory is easy to diagram
and does not necessarily conflict with
phylogenetic schemes based on the fossil
record; unfortunately there is no evidence
to support it. It is, of course, equally possible to take a more complex starting point
and either add further complications or
lose them in different lines; again there is
no evidence and, as a further problem, no
real reason to select any particular pattern
as the starting point. We know that parallelism can occur in nasal evolution: a
preconcha in both birds and crocodilians
and a secondary palate in both crocodilians
and mammals. We know that structures can
be lost: the Jacobson's organ of crocodilians
and others and the concha of various lizards. We do not know the nasal morphology of extinct groups or the phylogenetic
history of several of the living orders.
Therefore we can only make guesses about
the early stages in the nasal evolution of
tetrapods.
ABBREVIATIONS USED ON FIGURES
AC, Anterior concha; AOB, Accessory olfactory
bull): CCR, Caviconchal recess; CD, Choanal diverticulum; CF, Choanal fold; CH, Choana; CNP,
Cavum nasi proprium; CO, Concha; DR, Dorsal recess of intermediate region; ECR, Extraconchal recess; EN, External naris; IC, Inferior cavity; IR, Intermediate region; JO, Jacobson's organ (or equivalent structures in amphibians); LD, Lachrymal duct;
LNS, Lateral nasal sinus; LR, Lateral recess of inferior cavity; MB, Mushroom body; MC, Middle
cavity: MOB, Main olfactory bulb; MR, Medial recess of inferior cavity; MXS, Maxillary sinus; ND,
Nasopharyngeal duct; NPT, Nasal pit; OE, Olfactory eminence; OR, Olfactory region; PC, Principal
cavity: I'CC. Postconchal cavity; PCO, Posterior concha; PCR, Prechonchal recess; PLR, Posterolateral
recess; PRC, Preconcha; PTC, Postconcha; PTS,
Postturbinal sinus; VC, Vomerine cushion; VE,
Vestibulum; VR, Ventral recess of intermediate region.
REFERENCES
Bellairs, A. d'A., and J. D. Boyd. 1950. The lachrymal apparatus in lizards and snakes. II. The
anterior part of the lachrymal duct and its relationship with the palate and with the nasal
and vomeronasal organs. Proc. Zoo!. Soc. (London) 120:269-310.
Bertau, M. 1935. Zur Entwicklungsgeschichte des
Geruchsorgans der Krokodile. Z. Anat. Errtwickl.
104:168-202.
Bertmar G. 1965. The olfactory organ and upper
lips in Dipnoi, an embryological study. Acta
Zool. 46:1-40.
Bertmar, G. 1966a. On the ontogeny and homology
of the choanal tubes and choanae in Urodela.
Acta Zool. 47:43-59.
Bertmar, G. 19666. The development of skeleton,
blood-vessels and nerves in the dipnoan snout,
with a discussion on the homology of the dipnoan
posterior nostrils. Acta Zool. 47:81-150.
de Beer, G. R. 1937. The development of the
vertebrate skull. Oxford Univ. Press, Oxford,
xxiv -f 552 p.
Fuchs, H. 1915. Ober den Bau und die Entwicklung
des Schadels der Chelone imbricata. Ein Beitrag
zur Entwicklungsgeschichte und vergleichenden
Anatomie des Wirbeltierschadels. Erster Teil:
Das Primordialskelett des Neurocraniums und
des Kieferbogens. In A. Voeltzkow, Reise in
Ostafrika in den Jahren 1903-1905, Wissenschaftliche Ergebnisse 5:1-325.
Gegenbaur, C. 1873. Ober die Nasenmuscheln der
Vogel. Z. Naturwiss. (Jena) 7:1-21.
Helling, H. 1938. Das Geruchsorgan der Anuren,
verleichendmorphologisch betrachtet. Z. Anat.
Entwickl. 108:587-643.
Herrick, C. J. 1921. The connections of the
vomeronasal nerve, accessory olfactory bulb and
amygdala in Amphibia. J. Comp. Neurol. 33:213280.
Hoppe, G. 1934. Das Geruchsorgan von Hatteria
pmictata. Z. Anat. Entwickl. 102:434-461.
Jarvik, E. 1942. On the structure of the snout of
crossopterygians and lower gnathostomes in
general. Zool. Bidrag 21:235-675.
Leydig, F. 1872. Die in Deutschland lebenden Arten
der Saurier. H. Laupp'sohen Bu<chhandlung,
Tubingen, vii -|- 262 p.
Malan, M. E. 1946. Contributions to the comparative
anatomy of the nasal capsule and the organ of
Jacobson of the Lacertilia. Ann. Univ. Stellenbosch (A) 24:69-137.
Matthes, E. 1934. Geruchsorgan. In Bolk, Goppert,
Lubosch, and Kallius, (ed.), Handbuch der vergleichenden Anatomie der Wirbeltiere. Urban
und Schwarzenberg, Berlin and Wien. 2(2):879948.
McCotter, R. E. 1917. The vomero-nasal apparatus in Chrysemys punctata and Rana catesbiana.
Anat. Rec. 13:51-67.
Olson, E. C. 1947. The family Diadectidae and its
bearing on the classification of reptiles. Fieldiana:Geol. 11:1-53.
Olson, E. C. 1965. Relationships of Seymouria, Diadectes, and Chelonia. Am. Zoologist 5:295-307.
Parsons, T. S. 1959a. Studies on the comparative
embryology of the reptilian nose. Bull. Mus.
TETRAPOD NASAL STRUCTURE
Com p. Zool. Harvard Coll. 120:101-277.
Parsons, T. S. 19596. Nasal anatomy and the
phytogeny of reptiles. Evolution 13:175-187.
Parsons, T. S., and E. E. Williams. 1963. The relationships of the modern Amphibia: A reexamination. Quart. Rev. Biol. 38:26-53.
Pratt, C. W. McE. 1948. The morphology of the
ethmoidal region of Sphenodon and lizards. Proc.
Zool. Soc. (London) 118:171-201.
Rudebeck, R. 1944. Does an accessory olfactory
bulb exist in Dipnoi? Acta Zool. 25:89-96.
Sarasin, P., and F. Sarasin. 1887-1890. Zur Entwicklungsgeschichte und Anatomie der ceylonischen
Blindwiihle Ichthyophis glutinosus, L. In Ergebnisse naturwissenschaftlicher Forschung auf
Ceylon. Kreidels, Wiesbaden. 2:263 p.
Schuch, K. 1934. Das Geruchsorgan von Triton
alpestris. Eine morphologische, histologische und
entwicklungsgeschichtliche Untersuchung. Zool.
Jahrb., Abt. Anat. 59:69-134.
413
Seydel, O. 1895. Uber die Nasenhohle und das
jacobson'sche Organ der Amphibien. Eine vergleichend-anatomische Untersuchung. Morphol.
Jahrb. 23:453-543.
Seydel, O. 1896. uber die Nasenhohle und das
Jacobson'sche Organ der Land- und Sumpfschildkroten. Festchr. 70 Geburtst. C. Gegenbaur
2:385-486.
Stebbins, R. C. 1948. Nasal structure in lizards with
reference to olfaction and conditioning of the
inspired air. Am. J. Anat. 83:183-221.
Thomson, K. S. 1964. The comparative anatomy
of the snout in rhipidistian fishes. Bull. Mus.
Comp. Zool. Harvard Coll. 131:313-357.
Thomson, K. S. 1965. The nasal apparatus in
Dipnoi, with special reference to Protopterus.
Proc. Zool. Soc. (London) 145:207-238.
Watson, D. M. S. 1957. On Millerosaurus and the
early history of the sauropsid reptiles. Phil.
Trans. Roy. Soc. (London), B, 240:325-400.