AMER. ZOOL., 13:1205-1213 (1973).
Mechanisms of Sound Production in Delphinid Cetaceans:
A Review and some Anatomical Considerations
WILLTAM E.
EVANS
Naval Undersea Center, San Diego, California 92132
AND
PAUL F. A. MADERSON
Department of Biology, Brooklyn College, Brooklyn, New York 11210
SYNOPSIS. The past literature describing the possible sites o£ the sound-producing
mechanisms in delphinid cetaceans is reviewed. The morphology o£ the nasal sac
system of delphinids which has been implicated in the production of sounds, 'by most
investigations, is discussed with special emphasis placed on the physical characteristics of these sounds. New data on the histological structure of the epithelia throughout the nasal region of a delphinid are presented with some suggestions as to its
function. The presence and structure of glandular tissues are described along with
a discussion of their potential role in the production of sound. It is concluded that
the theories implicating the nasal sac systems of odontocete cetaceans in the production of sound are additionally supported by certain anatomical specializations adjacent to the tissues of this system.
All the theories to date concerning the
mechanism of delphinid sound production
have implicated the larynx (arytenoepiglottic tube), the complicated diverticuli associated with the blowhole mechanism, the
large muscular plugs that seal off the internal nares, or various combinations of
these. The driving mechanism has been
thought to he pneumatic, mechanical
(muscle-driven), or both. Various combinations of internal sound transmission paths
have been considered: air—muscle/fat—
water; air—bone—water; tissue—water (Norris, 1969; Evans, 1973).
Attempts have been made to construct
conceptual models of the delphinid sound
source so that the models could be compared with existing anatomical structures
as an aid in localizing the sound source.
Unfortunately most of the current ideas,
with the exceptions of Norris and Harvey
(1972) and Evans (1973), have not considered the acoustical parameters of the
signals being produced by the "theoretical"
Maderson's work is supported in part by grams
AM-15515 and CA-10844 from the National Institute of Health and C.U.N.Y. Doctoral Faculty
Award 1574.
sound source. Other aspects of these various
theoretical mechanisms have been discussed
in detail elsewhere (Evans, 1973) and will
not, therefore, be reviewed in this paper.
Evans and Prescott (1962) postulated a
dual sound source involving the laryngeal
mechanism (arytenoepiglottic tube) for
whistles, the nasal plugs with associated
sacs for pulses. Norris (1964, 1969) seems
to favor the nasal sac system for pulse production and, in general, a tissue-water
transmission path in which the sound is
projected through the "melon" into water.
In addition he endorses the frequently suggested idea that the melon acts as an
acoustic lens and functions in the formation of the beam of sound. This theory
has received additional support from the
recent study by Norris and Harvey (1973)
on sound transmission in the porpoise
head and from the work of Vasanasi and
Malius (1972). Recent measurements made
using contact transducers on both the
melon and the rostrum in two species indicate that echoranging pulses are projected equally efficiently from both the
rostrum and the melon. Analysis of data
recorded with a multiple array of attached
1205
1206
WILLIAM E.
EVANS AND PAUL E. A.
MADERSON
cast the nasal sac system in two possible
extreme roles: that of the only active
sound-producing system, or that of a reservoir for storing "recycled" air during the
underwater vocalizations produced by another structure, e.g., the larynx. In fact, all
theories imply a partial "storage role" for
some or all of the nasal system components.
Consideration of the two extreme roles permits certain predictions to be made regarding aspects of sac anatomy which can
be investigated directly.
If the sounds were produced solely in
the larynx, with the sac system serving only
as a reservoir for recycling, one would predict a relatively simple system, of homogeneous gross and microscopic structure
lacking noteworthy localized specializations. This prediction is not borne out by
such studies as those of Lawrence and
Schevill (1956) or Mead (1972). If, on the
other hand, the nasal sac system were
assumed to be the source of the sounds, one
would predict anatomical and histological
diversity, with specializations appropriate
to the various roles of the component
elements.
The odontocete nasal system is one which
defies satisfactory verbal description and
certainly reduction to two-dimensional
graphic representation, although several
excellent attempts to overcome the inherent
complexities are available (Lawrence and
Schevill, 1956; Evans and Prescott, 1962;
Schenkkan, 1971; Mead, 1972). The horizontal section through the system of an
adult T. truncatus shown in Figure 1 gives
some indication of the problem.
Fundamentally, the system consists of a
single nasal passage, formed by the fusion
of paired passages exiting the bony skull,
running toward the dorsally situated "blowhole," with several pairs (the actual number varying according to the species and
the criteria of the investigator) of laterally
arising diverticula. The entire system is
bounded anteriorly by the nasal plug, a
massive muscular organ which effects closure
THE ANATOMY AND FUNCTION OF THE
of the nasal passages (Lawrence and
NASAL SAC SYSTEM
Schevill, 1956; Mead, 1972) and posteriorly
The various theories previously discussed bv the assvmetrical, concave, anterior sur-
sensors places the source in the vicinity of
the nasal plugs at a depth of 1.5-2.0 cm
(Direcks et al., 1971). These data were used
by Evans (1973) to propose a sound transmission path with both bone and adipose
tissue components. A mechanical source
without dependence on air flow, and thus
independent of depth effects, could have
definite advantages. Movements of the external parts of the blowhole mechanism
have been observed and discussed by several
authors, e.g., Norris (1968) and Evans and
Prescott (1962). Even though the paired
muscular nasal plugs fit tightly into the
external bony nares, they are capable of
considerable movement. It is suggested
that as these plugs are moved mechanically
or pneumatically against the hard edge of
the external bony nares, "relaxation oscillations," with resultant acoustic pulses, are
generated by alternate resistance and release of the plugs' movements. The sound
produced would thus follow the paths described by Norris and Harvey (1973); first,
from the muscular plug through the melon
and into the water; or second, from the
plug through the melon, along the premaxillary bones, and radiate into the water
from the tip of the rostrum. This is in contrast to Purves' (1967) contention that all
the sound is radiated from the rostrum.
The "relaxation-oscillation" mechanisms
are appealing because of their efficient
energy conversion capabilities, especially
when one considers the sound levels measured. However, such mechanisms would
place certain demands on the tissues of the
nasal region, notably with respect to tolerance of shearing forces produced by high
velocity air currents and the possible need
for lubrication. We will now present new
anatomical and histological data concerning the nasal pasages and diverticula of
Tursiops truncatus, which we believe reinforce the theory of sound production derived from acoustic studies.
DELPHJNID SOUND PRODUCTION
u
1207
FIG. 1. A horizontal section across the nasal region o£ Tursiops truncatus approximately 1.5 cm
below the blowhole, viewed from the dorsal surface. Note that the section reveals the full length
of the right posterior nasofrontal (tubular) sac
(RPNF) and its junction with the right inferior
vestibule (RIV), while the homologous left elements lie approximately 1.0 cm ventral to this
section. The grid lines are 3.8 cm apart. Other
abbreviations: BL—blowhole ligament; LANF—
left anterior nasofrontal sac; LVS—left vestibular
sac; LPNF—left posterior nasofrontal sac; RANF—
right anterior nasofrontal sac; RVS—right vestibular sac; x—location of glandular tissue (Figs.
7, 8). The anterior nasofrontal sacs have flags inserted in their lumina.
face of the cranium. The simplest possible
representation of this system is shown in
Figure 2, which also attempts to indicate
the approximate inclinations of the various
diverticula after their origin from the
single nasal passage. The "distortion" of
this fundamental plan can be seen if Figure
2 is compared with Figures 1 and 3, which
indicate that all the sacs and tubes are
flattened to a greater or lesser degree, so
that: (i) the epithelial surface area is
greatly increased, and (ii) there is a high
probability of actual temporary physical
juxtapositioning of opposing epithelial surfaces. If we add to these data the fact that
fresh dissection material suggests a flexibility and mobility of the entire system
comparable to that of the lips of a small
boy making obnoxious noises, we can begin
to appreciate how the sac system might
produce sounds.
Either theory of nasal sac function suggests that a column of air passes through
the system at high speed. Since air passing over an epithelial surface will exert a
lateral shearing force on the tissue, a
priori one would predict that an anatomical arrangement minimizing epithelial surface area would be present. Furthermore,
if the functions of the sac system were
simply that of a reservoir for the recycling
of a given volume of air, not only would
simple gross anatomy be predictable, but
one would expect epithelial homogeneity
throughout the system. Neither of these
predictions is fulfilled.
In all genera, although variable from
species to species, there is a pair of dorsalmost "vestibular sacs," ventralmost "premaxillary sacs" (lying beneath the posteroventral margin of the nasal plug), and between them the "tubular sacs" (nasofrontal
sacs) with anterior and posterior extensions
(Fig. 2). The presence of distinct "accessory
sacs" (Schenkkan, 1971; Mead, 1972), "connecting sacs" (Lawrence and Schevill,
1956), and paired "inferior vestibules"
(Mead, 1972) seems to be somewhat variable
and/or dependent on the interpretation
of a particular investigator, but both are
1208
WILLIAM E. EVANS AND PAUL F. A. MADERSON
RIGHT VESTIBULAR SAC
_.
ANTERIOR
——XTXTEN->ION
- * - - * • • • '
r*.
•v..
NASOFRONTAL/
^
POSTERIOR
EXTENSION
— I - INFEPIOR VESTIBULE
LEFT PREMAXILLARY SAC
\
X
XA
A
X X
X
X
X
x
)
TUBULAR SAC
-7
RIGHT ACCESSORY/
> r r
'
•
•
•
.
•
•
•
' "
. ' . • • •
CONNECTING SAC
BONY NARES
LEFT VESTIBULAR
SAC OPENING INTO
NASAL PASSAGE •
LEFT MARGIN OF BLOWHOLE
LEFT NASOFRONTAL SAC
ANT. EXT.
MELON
POST. EXT
INFERIOR
VESTIBULE
BLOWHOLE LIGAMENT
GLANDULAR
REGION
DIAGONAL
MEMBRANE
PREMAXILLARY
SAC
DELPHINID SOUND PRODUCTION
1209
sufficiently distinct to be identified in T.
truncatus. It is important to emphasize
that not only is there variation in form
and/or presence of all of the abovemention elements between genera and
species, but that within at least one
species—Delphinus delphis L.—there may
be noticeable quantitative variation in size
between individuals (Evans, unpublished).
In all animals thus far studied, the right
and left components not only show a relative asymmetry of quantitative development which is characteristic of many
aspects of odontocete head anatomy, but
also show a spatial asymmetry with respect
to the head axes in a manner which is
not predicated by the bony elements.
The entire nasal region is lined throughout by a stratified squamous parakeratotic
epithelium which basically resembles that
of the cetacean body epidermis (Spearman,
1972), although in the nasal region, the
"corneous" layer is somewhat thinner.
There are no indications of mucus-secreting or specialized sensory regions of any
description. Lack of mucus-producing cells
presumably reflects the fact that in an
aquatic environment, the relative humidity
of the air within the nasal system is always
sufficiently high so that dessication is never
a serious problem (Coulombe et al., 1965).
The lack of sensory elements confirms the
long-assumed anosmatic nature of the
odontocete nose. The epithelia throughout
have a general similarity to those of the
human lips and buccal regions and this
serves to reinforce the analogy of the
potential for noise production by those
parts of the human body.
The histological structure of the epithelia
throughout the nasal region can be divided
into three broad categories. In those
regions where the gross appearance is
relatively smooth and unwrinkled and
where the relationships of the epithelium
to the underlying tissues suggest relative
immobility, i.e., the ventralmost nasal passages and the ventral aspects of the nasal
plug leading into the premaxillary sacs,
the epithelium is smooth, the cells are
aligned parallel to the surface, and the
dermal papillae are not very well developed
(Fig. 4). In the vestibular sacs, which are
conspicuously wrinkled, and which have
been demonstrated to be capable of inflation {Evans and Prescott, 1962), the
epithelial histology is quite different (Fig.
5). The dermal papillae are well developed
and are oriented perpendicular to the
epithelial surface. T h e surface of the
epithelium is crenate, and above each
paipillar apex, the corneal cells are arranged
in regularly wavy rows. All features of the
epithelium in the vestibular sacs suggest
a functional adaptation directed primarily
towards stretching, rather than to resistance to surface shearing forces seen in the
first category (Fig- 4). The epithelial
structure throughout the accessory sacs,
inferior vestibules, and nasofrontal sacs
varies between these two extremes (Fig. 6).
The farther away from the actual nasal
passage, the less determinate is the
epithelial structure. This is particularly
true as one approaches the blind ends of
the anterior and posterior extensions of
the nasofrontal sacs.
Around the inferior vestibular surfaces,
just extending into the posterior nasofrontal sacs (Fig. 2), there are distinct modifications of the epithelial structure (Maderson, 1968). On the right side there are
about 20, and on the left perhaps only
half as many, crescentic pores approxknate-
FIG. 2. A highly schematic representation of the
nasal sac system of Tursiops Iruncatus viewed as
a transparent object from the posterior aspect.
Note tha* all axes are greatly distorted, and no
attempt has been made to indicate the right/left
asymmetry in terms of either size of homologous
links, or with respect to spatial orientation. The
position X X X X X indicates the location of the
blowhole ligament. Nomenclature after Lawrence
and Scheville (1956) and Mead (1972) .
FIG. 3. A diagrammatic drawing of a sagittal section through the nasal region of Tursiops truncalus taken at the axis Z-Z in Figure 2. An attempt has been made to show the general relationships of the elements further to the left of the
head.
1210
WILLIAM E.
EVANS AND PAUL F. A. MADERSON
DELPHTNID SOUND PRODUCTION
1211
The acoustic data currently available
suggest most forcibly that delphinid phonations are produced in the nasal region. The
figure of 1.5-2.0 cm beneath the blowhole
margin provided by Diercks et al. (1971)
as the site of origin would seem to correspond to the region where the lip of the
nasal plug abuts the blowhole ligament
(Fig. 3). While this location is only one of
many which anatomical study shows close
abutment of opposing epithelia, it is immediately adjacent to the glandular structures, so that it is appropriate to consider
the possible function of the latter. Their
small total bulk suggests that they could
not be salt glands, and their anatomy is
so different from such organs (Waterman,
1971, p. 587) that they cannot be interpreted as vestigial structures. They are
similar in some ways to Steno's glands
found in other mammals (Moe and Bojsen-Moller, 1971), but it is unlikely that
they serve the humidifying function proposed by these authors. If we assume that
sound production is effected by a relaxation-oscillation mechanism involving rapid intermittent juxtapositioning of the opposing epithelia of the posterior nasal plug,
and those of the ventral blowhole ligament, and circumnarial region in a rapidly moving airstream, then the glandular
secretions could lubricate the tissues involved, and thus minimize mechanical
damage.
Other available anatomical data seem to
strengthen this postulate. Gross and microscopic analysis suggest that only the
vestibular sacs regularly expand and deflate, and Norris (1964) has indicated that
not only could they serve as reservoirs for
recycled air, but that this activity would
also permit them to act as sound reflectors.
Mead (1972) suggests, therefore, that the
different sizes and shapes of the vestibular
sacs in different species might permit differences in the shape of sound fields. Mead
(1972) states that the premaxillary sacs
"are probably the best situated for storage
and recycling of air for sound production."
We suggest that their gross and microscopic structure does not reflect a distensible
unit comparable to that of the vestibular
sacs, but rather a mechanism permitting
antero-postero movement of the nasal plug,
ensuring a tight fit of the ventral aspect of
the latter against the floor of the "sac" during intermittent contact of the posterior
face with the blowhole ligament and the
circumnarial tissues. Lawrence and Schevill (1956) suggested that the nasofrontal
sacs (their "tubular sacs") functioned as
pneumatic seals around the nasal passage.
We agree with Mead's (1972) contention
that this function could be better served
by large muscle masses in the same area,
and note his comment that in Grampus
the left anterior nasofrontal sac is entirely
FIC. 4. Photomicrograph of the epithelial structure at the base of external nares in Tursiops
truncatus.
FIG. 5. Photomicrograph of the epithelial structure of the left vestibular sac o€ Tursiops truncatus.
FIG. 6. Photomicrograph of the epithelial struc-
ture of the posterior nasofrontal sac of Tursiops
truncatus.
FIG. 7. Photomicrograph of the opening of a glandular duct in the right inferior vestibule of Tursiops truncatus.
FIG. 8. Photomicrograph of the distal acini of the
gland shown in Figure 7.
ly 1.0 mm long (Fig. 7). These lead into
compound acinar, exiocrine glands, running into the sub-epithelial tissues, which
are larger on the right than on the left.
Material in the acinar lumina probably
derives by apocrine secretion from the simple cuboidal epithelium. The secreted
material does not have mucinous properties and may contain some lipid (Fig. 8).
Similar structures have also been seen in
Kogia, and Mead (1972) refers to "glandular epithelia or tissues" in Inia geoffrensis, Phocoena phocoena, and Phocoenoides
dalli, but offers no histological descriptions. In all cases the location includes the
inferior vestibular, nasofrontal sac tissues.
DISCUSSION
1212
WILLIAM E.
EVANS AND PAUL F. A.
absent. While the intra-specific variation
which we have commented upon has not
yet been quantified, it seems most unlikely
that any significant variation would be
"permitted" by natural selection if the
nasofrontal sacs played any active major
role in such a sophisticated function as
delphinid phonation. Schenkkan (1971)
and Mead (1972) both draw attention to
the considerable diversity in structure and
degree of development of the accessory
sacs and vestibular regions between genera. Mead (1972) makes frequent reference
to the possibility that any and all diverticula could function as storage areas for
recycled air. However, in the light of Norris' (1964) suggestion that an inflated vestibular sac could act as a sound reflector,
it is important to note that if the nasofrontal-vestibular accessory region did become wholly or partially filled with air,
then we would assume that they would
play a similar reflecting role. According to
this premise there should be a relationship
between the details of the presence and degree of development of these various components and the shape of the sound field
produced by particular genera. Since there
are insufficient data available to establish
such a relationship, it is simpler to assume
that air storage is not the primary function of these diverticula.
Our histological data, derived from studies on Tursiops and Kogia, and comments
by Mead (1972) on the other genera, suggest that glandular secretion is an important function of the vestibular-nasofrontal
regions. We have suggested that lubrication of the posterior nasal plug tissues
might be the function of these secretions.
We have also indicated that it may be the
vestibular sacs alone which serve as recycling storage areas. Therefore, the highspeed current of air which passes up the
paired narial openings towards the vestibular sacs might tend to blow the glandular secretions back up the nasofrontal
system, thus deflecting them away from the
surfacts which should be lubricated. However, Mead (1972) suggests that the intrinsic musculature of the nasofrontal sacs
MADKRSON
would permit their emptying and filling.
Therefore, if we assume that the functions
of the nasofrontal-vestibular accessory regions are secretory, and also storage of the
secreted materials, we can propose the following answers to some of the problems
which have been raised. During periods of
non-sound production, the opening of the
vestibular-nasofrontal accessory system into
the nasal passage could be occluded by the
nasal plug being drawn back tightly against
the blowhole ligament (Fig. 2). During
this time, glandular secretions could accumulate within the lumina, especially of the
nasofrontal sacs due to relaxation of the
intrinsic musculature. During sound production, anterior movement of the nasal
plug would permit expression of the glandular secretion which, aided by active expulsion by contraction of the intrinsic musculature, would not only lubricate the opposing epithelial surfaces, but possibly also
prevent the entry of air into this system
of diverticula. This explanation satisfies
the problem of the possibility of air-filling
creating an acoustic reflector, but, should
it be proven that there is indeed a correlation between vestibular-nasofrontal accessory anatomy and the shape of the sound
fields in different genera, the model can
be modified without altering the fundamental functions proposed here.
CONCLUSIONS
Following an extensive review of the
nasal anatomy of a variety of odontocete
genera, Mead (1972) states: "In summary,
it appears that the structures most likely
to be involved in sound production are
those in the vicinity of the nasal plugs."
We have found that this premise is supported by recent acoustic studies (Diercks
et al., 1971; Evans, 1973) and by certain
anatomical specializations adjacent to these
tissues described in the present paper. Further substantiation of the model presented
here must await demonstration of specialized glandular structures in similar regions
in all other sound-producing genera, histochemiial identification of the secretions
DELPHINID SOUND PRODUCTION
produced by analysis of fresh material, and
finally, correlations between the anatomical diversity now known to exist between
genera and species and the acoustic properties of the sounds produced by them.
REFERENCES
Coulombe, H. N., S. H. Ridgway, and W. E.
Evans. 1965. Respiratory water exchange in two
species of porpoise. Science 149:86-88.
Diercks, J. J., R. T. Trochta, R. L. Greenlaw, and
W. E. Evans. 1971. Recording and analysis of
dolphin echolocaition signals. J. Acoust. Soc.
Amer. 49:1729-1732.
Evans, W. E. 1973. A discussion of echolocation
•by cetaceans based on experiments with marine
delphinids and one species of freshwater dolphin.
J. Acoust. Soc. Amer. 54:191-199.
Evans, W. E., and J. H. Prescott. 1962. Observations of the sound production capabilities of
the bottlenose porpoise: a study of whistles and
clicks. Zoologica 47:121-128.
Lawrence, B., and W. E. Schevill. 1956. The functional anatomy of the delphinid nose. Bull. Mus.
Comp. Zool. (Harvard) 114:103-151.
Maderson, P. F. A. 1968. The histology of the
nasal epithelia of Tursiops truncatus (Cetacea)
with preliminary observations on a series of
glandular structures. Amer. Zool. 8:810. (Abstr.)
Mead, J. G. 1972. On the anatomy of the external
nasal passages and facial complex in the family
Delphinidae of the order Cetacea. Doctoral
Thesis, Univ. of Chicago.
Moe, H., and F. Bojsen-Moller. 1971. The fine
structure of the lateral nasal gland (Steno's
1213
gland) of the rat. J. Ultrastruct. Res. 36:127148.
Norris, K. S. 1964. Some problems of echolocation
in cetaceans, p. 317-336. In W. N. Tavolga [ed.],
Marine bioacoustics. Pergamon Press, New York.
Norris, K. S. 1968. The evolution of acoustic mechanisms in odontocete cetaceans, p. 297-324. In
E. T. Drake [ed.], Evolution and environment.
Yale Univ. Press, New Haven.
Norris, K. S. 1969. The echolocation of marine
mammals, p. 391-423. In H. T. Anderson [ed.],
The 'biology of marine mammals. Academic
Press, New York.
Norris, K. S., and G. W. Harvey. 1972. A theory
for the function of the spermaceti organ of the
sperm whale {Physeter catodon, L.), p. 397-417.
In Animal orientation and navigation, NASA
SP-262, Sci. and Tech. Office NASA, Washington,
D.C.
Norris, K. S., and G. W. Harvey. 1973. Sound transmission in the porpoise head. Science (In press)
Purves, P. E. 1967. Anatomical and experimental
observations on the cetacean sonar system, p.
197-270. In R. G. Busnel [ed.], Animal sonar systems, biology and bionics. Imprimerie LouisJean, GAP, Haute-Alpes.
Schenkkan, E. J. 1971. The occurrence and position of the "connecting sac" in the nasal tract
complex of small odontocetes (Mammalia,
Cetacea) . Beaufortia 19:37-43.
Spearman, R. I. C. 1972. The epidermal stratum
corneum of the whale. J. Anat. 113:373-381.
Vasanasi, V., and D. C. Malius. 1972. Triacylglycerols characteristic of porpoise acoustic tissues:
molecular structures of dilsovaleroylglycerides.
Science 176:4037, p. 926-928.
Waterman, A. J. 1971. Chordate structure and
function. Macmillan, New York.