Anatomy of the External

Nasal Passages and Facial Complex

in the Delphinidae

(Mammalia: Cetacea)

JAMES G, MEAD

miut.

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY • NUMBER 207
SERIAL PUBLICATIONS OF THE SMITHSONIAN INSTITUTION

The emphasis upon publications as a means of diffusing knowledge was expressed

by the first Secretary of the Smithsonian Institution. In his formal plan for the Institution, Joseph Henry articulated a program that included the following statement:

"It is proposed to publish a series of reports, giving an account of the new discoveries

in science, and of the changes made from year to year in all branches of knowledge."

This keynote of basic research has been adhered to over the years in the issuance

of thousands of titles in serial publications under the Smithsonian imprint, commencing with Smithsonian Contributions to Knowledge in 1848 and continuing with

the following active series:

Smithsonian Annals of Flight

Smithsonian Contributions to Anthropology

Smithsonian Contributions to Astrophysics

Smithsonian Contributions to Botany

Smithsonian Contributions to the Earth Sciences

Smithsonian Contributions to Paleobiology

Smithsonian Contributions to Zoology

Smithsonian Studies in History and Technology

In these series, the Institution publishes original articles and monographs dealing

with the research and collections of its several museums and offices and of professional

colleagues at other institutions of learning. These papers report newly acquired facts,

synoptic interpretations of data, or original theory in specialized fields. These publications are distributed by mailing lists to libraries, laboratories, and other interested

institutions and specialists throughout the world. Individual copies may be obtained

from the Smithsonian Institution Press as long as stocks are available.

S. DILLON RIPLEY

Secretary

Smithsonian Institution
SMITHSONIA N CONTRIBUTION S T O ZOOLOG Y • NUMBE R 20 7

Anatomy of the External

Nasal Passages and Facial Complex

in the Delphinidae

(Mammalia: Getacea)

James G. Mead

SMITHSONIAN INSTITUTION PRESS

City of Washington

1975
ABSTRACT

Mead James G. Anatomy of the External Nasal Passages and Facial Complex

in the Delphinidae (Mammalia: Cetacea). Smithsonian Contributions to Zoology,

number 207, 72 pages, 26 figures, 3 tables, 1975.—This study is concerned with

the comparative anatomy of the external nasal passages and associated structures

in delphinid odontocetes. It has been possible to assemble detailed anatomical

information for nearly all of the delphinid genera. Comparative data for the

other small toothed whales is considered in such detail as is available.

The function of the structures associated with the external nasal passages has

been poorly understood, partly due to a lack of understanding of their anatomy.

I have drawn functional conclusions from the basis of this comparative study,

but these are largely unsupported by experimental data.

The nasal musculature is concerned both with opening and closing the nasal

passage during respiration, and with movement of air between the nasal diverticula during sound production. The nasal diverticula are part of the acoustic

system of these animals, and function both as air reservoirs and as reflective

elements to focus the emitted sound field. The potential area of sound production is limited to the deep structures around the external body nares. The melon

probably serves as an acoustic channel. Cranial asymmetry in odontocetes is

related to specialized sound-producing mechanisms involving predominantly the

right nasal passage.

The nasal structures have formed a very important functional complex in the

evolution of odontocetes, and are important from a phyletic viewpoint. This

study has shown that the genera Tursiops, Stenella, and Delphinus form a relatively generalized group within the Delphinidae. The bulbous-headed genera

Grampus, Globicephala, and Pseudorca clearly represent independent specializations. The other families of odontocetes differ considerably from the delphinids

in their facial anatomy.

The anatomical diversity in this region suggests an acoustic diversity which

remains to be demonstrated experimentally.

OFFICIAL PUBLICATION DATE is handstamped in a limited number of initial copies and is recorded

in the Institution's annual report, Smithsonian Year. SI PRESS NUMBER 5387. SERIES COVER

DESIGN: The coral Montastrea cavernosa (Linnaeus).

Library of Congress Cataloging in Publication Data

Mead, James G.

Anatomy of the external nasal passages and facial complex in the Delphinidae (Mammalia:

Cetacea)

(Smithsonian contributions to zoology, no. 207)

Supt. of Docs, no.: SI 1.27:207

1. Delphinidae. 2. Nose. 3. Face. 4. Skull. I. Title. II. Series: Smithsonian Institution.

Smithsonian contributions to zoology, no. 207.

QL1.S54 no. 207 [QL737.C432] 591'.08s [599'.53] 75-619034
Contents

Page

Introduction 1

Historical Review • 1

General Aspects of the Facial Anatomy of Mammals 2

Questions of Odontocete Facial Anatomy . 4

Acknowledgments 5

Descriptive Anatomy 5

Introduction 5

Delphinidae 6

Delphininae . 6

Tursiops 6

Stenella 15

Delphinus 17

Lagenorhynchus 18

Lagenodelphis 19

Grampus 19

Orcininae 22

Orcinus 22

Pseudorca 23

Globicephala 24

Steninae 26

Steno 26

Sotalia 28

Cephalorhynchinae • 28

Cephalorhynchus 28

Lissodelphinae 29

Lissodelphis 29

Phocoenidae 30

Phocoena, Phocoenoides, Neophocaena 30

Monodontidae 31

Monodon 31

Delphinapterus 31

Platanistidae 32

Platanista 32

Lipotes 33

Pontoporia 33

Inia . 33

Summary of Descriptive Anatomy 34

Nasal Passage and Diverticula . 34

Musculature 34

Melon 34

Other Structures 35
j v SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Page

Function of the Facial Complex 35

Introduction 35

Respiratory Considerations . 35

Nasal Passage and Diverticula 36

Musculature 37

Melon 40

Glandular Structures 41

Functional Basis of Sound Production 42

Review 42

Anatomical Considerations 46

Functional Aspects of Cranial Asymmetry 48

Review 48

Anatomical Considerations 51

Summary of Facial Complex Function 53

Nasal Diverticula 53

Nasal Musculature 53

Other Structures 54

Experimental Approaches . 54

Phyletic Relations of the Delphinidae 54

Relationships within the Delphinidae 54

Relationships to Other Families 56

Relationships of Bulbous-headed Delphinids 57

General Considerations 57

Comparison of Pseudorca, Globicephala, and Grampus 58

Origin of the Odontocete Nasal Apparatus 61

Appendix 1: Classification of the Odontocetes (Toothed Whales) 64

Appendix 2: Tables 65

Literature Cited 67
Anatomy of the External

Nasal Passages and Facial Complex

in the Delphinidae

(Mammalia: Cetacea)

James G. Mead

INTRODUCTION

Historical Review

The structure of the Cetacea (whales, porpoises,

and dolphins) has long fascinated anatomists and

students of natural history in general. Many features of cetacean anatomy were familiar to the

classical natural historians, notably Pliny the Elder

and Aristotle. During the middle ages, cetacea

were frequently treated in general works on natural history (Olaus Magnus, Gesner, Rondeletius,

and others), but emphasis was on the fabulous

aspects of the larger members of the order. The

first work exclusively on the anatomy of a cetacean

is John Ray's "Account of the Dissection of a

Porpess" (1671). This paper is particularly interesting, in that it contains a description of the nasal

passages and diverticula, as well as some speculations upon their function.

The peak of activity on cetacean anatomy occurred during the 19th century, when such workers

as Turner, Flower, Murie, Rapp, Kukenthal, Stannius, and others produced thousands of pages of

descriptive anatomy. During the 20th century this

work was continued by Howell, Schulte, Beddard,

Huber, Slijper, and others.

Of the smaller cetaceans, Phocoena phocoena

James G. Mead, Department of Vertebrate Zoology, National

Museum of Natural History, Smithsonian Institution, Washington, D. C. 20560.

(the harbor porpoise) has been the most frequently

and most thoroughly described (e.g., Ray, 1671;

Stannius, 1849; von Baer, 1826; Rawitz, 1900), due

to its abundance along the European coast and its

convenient size. The pilot whale (Globicephala

melaena) has also been the frequent subject of

anatomical investigations (Macalister, 1867; Turner, 1867; and most notably Murie, 1873), due to

the frequency of its strandings along the European

coasts. Aside from these, the best descriptions of

the anatomy of smaller cetaceans are usually of

rare and unusual animals (e.g., Neophocaena,

Howell, 1927; Kogia, Danois, 1910; Kernan and

Schulte, 1918; Monodon, Huber, 1934). Delphinine

cetaceans have received less attention, and very

little published information exists for Tursiops

truncatus, the ubiquitous experimental animal of

the present time.

Relatively few of the many hundreds of papers

dealing with the anatomy of cetaceans contain

information on the structures of the facial region.

Some of the early papers (Ray, 1671; Hunter, 1787;

Cuvier, 1836) on general anatomy mention the

structure of the nasal passage, or comment briefly

on the musculature surrounding it. Von Baer

(1826) appears to have been the first to focus on

the structure of the cetacean nose, based upon dissections of Phocoena. Sibson (1848) described the

nasal apparatus in Phocoena and Murie (1870,
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

1873) went into some detail in discussing the facial

structures of a variety of odontocetes. Gruhl (1911)

commented extensively on the diverticula in a

number of species. (Purves, 1967, and Moris, 1969,

have given brief descriptions of the facial anatomy

of Steno and Phocoena.)

The principal recent works dealing with the

anatomy and function of the nasal apparatus are

those of Lawrence and Schevill (1956), who were

primarily concerned with the respiratory functions

of these structures, Schenkkan (1971, 1972, 1973),

and Schenkkan and Purves (1973). Schenkkan

(1973) presented an extensive treatment of the

comparative functional anatomy of the nasal tract

of odontocetes. His data filled in many of the gaps

in my material and have been utilized extensively

in the present paper. Many of the differences between his work and mine probably stem from the

fact that Phocoena formed the comparative framework of his study, whereas I used Stenella.

Since the discovery of the possibility of echolocation in odontocetes in the early 1950s (Kellogg,

et al., 1953; Schevill and Lawrence, 1956), and its

experimental demonstration in 1961 (Norris et al.,

1961), the anatomy of structures potentially involved in sound production and reception has

received considerable attention. The question of

sound reception has been treated by Reysenbach

de Haan (1957) and Fraser and Purves (1960).

Evans and Prescott (1962) and Norris (1964) have

considered the problems of sound production, while

Norris (1969) has provided the most recent general

survey of the problems of echolocation in cetaceans.

The structures comprising the facial region of

the odontocetes, i.e., the nasal passages and their

diverticula, the fatty melon, and the muscles associated with these, have frequently been implicated

in sound production (Lawrence and Schevill, 1956;

Evans and Prescott, 1962; Norris, 1968). Questions

relating to the mechanism of sound production,

such as which structures are involved and how the

acoustic energy is conducted from the sound

source (s), focused, modulated, and otherwise

altered, are still under debate.

General Aspects of the Facial Anatomy of

Mammals

The face, as it is generally thought of in human

terms, consists of the anterior portion of the head,

containing the nose, mouth, and eyes. To a certain

extent this area can be considered separate from

the remainder of the head, or cranium. Thus conceived, the bony elements of the face are the maxillae, premaxillae, nasals, vomer, palatines, zygomatics, and frontals. This division of the head

corresponds approximately with the distribution

of motor elements associated with the facial nerve,

and with the sensory distribution of the trigeminal

nerve.

The anatomy of the mammalian face is complex

(see Huber, 1930; Edgeworth, 1935; Miller et al,

1964), and presumably has been throughout much

of its evolutionary history.

The soft tissues consist of a series of muscles

disposed about the orifices of the face and largely

concerned with manipulation of these, the skin and

various specialized portions of the skin (lips, eyelids, etc.), and the vascular and nervous supplies

of these elements. The structures within the facial

orifices (eyes, tongue, etc.) could logically be

included in this group and would greatly expand

this list. However, these are extremely specialized

and are better considered separately.

The nose is generally a complex structure in

mammals, and even in terrestrial mammals it is

capable of being opened and closed to a considerable extent. This is accomplished by various portions of the m. maxillonasolabialis acting upon the

cartilages comprising the skeleton of the nasal aperture. In addition, the area of the nose is usually

highly sensitive and is abundantly supplied with

nerves and blood vessels. The complexity of the

mammalian nose has provided the basis for a great

variety of evolutionary modifications, exemplified

by the noses of pigs, elephants, tapirs, bats, moles,

and whales. Boas and Pauli (1908) give an excellent picture of the diversity of mammalian noses.

The cetacean face has become specialized as a

result of the demands of an aquatic existence, and

presents a number of differences from that of terrestrial mammals. The nose occupies a dorsal rather

than a terminal position on the rostrum, and the

facial musculature has become largely concerned

with opening and closing the nasal aperture. Cetacea are, in fact, one of the very few groups of

mammals incapable of facial expression, as the

areas of the mouth and eyes are relatively

immobile.

The orbit has moved laterally and ventrally and
NUMBER 207

now bears a closer relationship to the base of the

cranium than to the rest of the face. There has

been extensive alteration of the bones of the skull

(Miller, 1923), differing in detail in the two suborders of cetaceans.

In view of the modifications seen in the cetacean

head, it is useful to redefine the area of the face.

One of the immediately striking aspects of a cetacean skull (when viewed from above) is the flat

expanse of bone formed by the dorsal surface of

the rostrum and cranium. This surface is bounded

by the lateral edge of the rostrum, the supraorbital

process of the frontal, and the temporal and nuchal

crests (Figure 1). This area can be usefully defined

as the face in this group of animals, as it forms an

area concerned with the operation of the highly

modified cetacean nose. The orbit, while still surrounded by what is technically facial musculature,

does not fit into the functional area of the face in

pmx

sop

FIGURE 1.—Skulls of modern cetaceans (after Kellogg, 1928):

a, Tursiops truncatus, an odontocete, lateral view; b, T. truncatus, dorsal view; c, Balaenoptera edeni, a mysticete, lateral

view; d, B. edeni, dorsal view. (fr = frontal, mx = maxilla,

na = nasal, nc = nuchal crest, sop = supraorbital process, tc =

temporal crest, pmx = premaxilla.)

vs

I V

FIGURE 2.—Head of a delphinid: a, diagramatic sagittal section; b, detail of the above. (af = anterior fold, bhl = blowhole ligament, bnp = bony nasal passage, iv = inferior vestibule, lnp = lip of the nasal plug, m = melon, ns = nasofrontal

sac, np = nasal plug, pf=posterior fold, ps = premaxillary sac,

sc = spiracular cavity, vs = vestibular sac.)
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

the same manner that it does in terrestrial mammals, nor does the mouth.

The skull of mysticetes has been modified along

different lines than that of the odontocetes, the

primary modification apparently being the develop

ment of a large rostrum as part of the feeding

mechanism. If the braincase is taken as the point

of reference, the nasal passages have not been displaced posterodorsally, as they have in odontocetes.

Carte and Macalister (1868) provide the best

description of the facial structures of a mysticete.

The musculature associated with the nares is extensive, but there are no diverticula, nor is there anything comparable to the large melon of odontocetes. Viewed from the side, the facial region of

mysticetes appears very low and flat compared to

that of odontocetes.

In the odontocetes, the nasal aperture has migrated posterodorsally, and now opens on the dorsal

surface of the head. The musculature associated

with the nasal passage has increased in size and

complexity, as have the passages themselves. Instead

of a relatively simple passage, as in the mysticetes,

there is a complicated series of diverticula and

valves within the nose of the toothed whales (Figure 2). An accessory structure, the melon, has

developed anterior to the nasal passage, greatly

increasing the bulk of the facial apparatus. The

acme of these is seen in the nose of the sperm

whale, which constitutes on the order of one-third

of the weight of the entire animal.

The development of a complex nasal apparatus,

particularly the elaboration of a fatty melon, is

one of the principal distinctions between odontocetes and mysticetes. The differences in the structure of the bony elements of the face can be followed well back into the fossil record (Kellogg,

1928), suggesting that the adaptive aspects of these

formed one of the bases for differentiation of the

two suborders. Mysticete differentiation appears to

have depended upon the development of a novel

feeding apparatus, while odontocetes remained relatively conservative in that aspect, and have elaborated the nasal apparatus and associated structures.

Numerous anatomists have attempted to homologize the structures of the cetacean nose with those

of the other mammals (von Baer, 1826; Murie,

1870, 1873; Anthony, 1926). The diverticula have

been compared with the turbinals of other mammals and with the nasal sacs of the tapir, the saiga

antelope, and the horse. Murie (1870) attempted

to homologize the nasal musculature with the various facial muscles of man. It is my belief, however,

that the melon, nasal diverticula, and differentiation of the nasal musculature have been derived

independently in cetaceans. Huber's (1934) brief

homology of the nasal musculature with the m.

maxillonasolabialis appears to be the most rational

approach to the question of muscle homologies.

The archaeocetes do not appear to have possessed

a specialized nasal apparatus, making it unlikely

that anything but the most generalized of mammalian homologies is applicable to the modern

Cetacea.

Questions of Odontocete Facial Anatomy

A thorough understanding of the anatomy of

this region is essential before we can hope to understand the functions in which it is involved. This

is particularly true of a system like the odontocete

nose, which does not appear to have an analogue

in any other mammalian structure. I have described

the components of the facial complex and their

relationships to one another in order to see if they

form discernible functional systems. To an extent

this has been possible, particularly with simpler

mechanical functions, such as opening and closing

of the blowhole and nasal passages.

Many of the potential functions of this region

are more subtle or complex and cannot be approached in this manner. In order to elucidate

these, I have undertaken a comparative study,

hoping to find structural differences which could

be correlated with observed behavioral or ecologic

differences.

This type of comparative approach is useful not

only in terms of the answers which it provides, but

also the questions which it poses. The range of

external morphology in the head of small odontocetes indicates the possibility of a wide range of

internal structure. If such structural diversity is

demonstrated, it will suggest a functional diversity

which must then be looked for in the living

animals.

Specialization of the facial region of odontocetes

has probably been an important factor in their

evolution and is thus important phyletically as

well as functionally. Relationships among the living

odontocetes are poorly understood at present. An
NUMBER 207

examination of one of their more important functional complexes will provide a new basis for interpreting phyletic relationships in this group. This

is particularly true where questions of possible

convergence are involved, as in the bulbous-headed

delphinids.

The significance of the asymmetry of the skull in

odontocetes has never been satisfactorily explained.

This is because the relationship of the bony asymmetry to the soft tissues of the head has never been

examined. Such an approach is essential to an

understanding of the functional significance of this

character.

A detailed anatomical study will also provide a

basis for experimental work on these animals,

which has previously been hampered by a lack of

information on the structures involved.

The literature pertaining to these problems is

voluminous and somewhat confusing. I have

attempted to review much of this and to clarify

some of the points of confusion.

Acknowledgments

This work was begun and substantially completed during my tenure as a graduate student at

the University of Chicago, and, as any dissertation,

owes a great deal to many people. Leonard

Radinsky, Charles Oxnard, George Rabb, Leigh

Van Valen, and Edward D. Mitchell served on the

dissertation committee, read the manuscript at

various stages, and provided much valuable criticism. I would like to express particular appreciation to James Hopson, my major professor, without

whose patience and assistance this work would

never have succeeded. I am also grateful to my

fellow graduate students, particularly Timothy L.

Strickler, who participated in many phases of this

study, and to my wife, Rebecca.

One of the greatest obstacles faced by a comparative study of this sort is the availability of

specimens. The material used in the studj was

provided by the following: William A. Walker,

Marineland of the Pacific; Edward D. Mitchell,

Fisheries Research Board of Canada; David K.

Caldwell, University of Florida; the Shedd Aquarium, Chicago; William F. Perrin, Southwest Fisheries Center; Robert Jones, University of California

at Berkeley; Robert L. Brownell; Allen Wolman

and Dale Rice, Marine Mammal Biology Laboratory, Seattle. I would also like to thank the people,

too numerous to mention, who spent time unsuccessfully trying to obtain material for this study.

I am particularly indebted to Edward D. Mitchell,

not only for providing material, but also for the

use of his laboratory facilities and library, remunerative employment, the drawing used in Figure

10, and a continuing flow of advice.

While I was at the University of Chicago, this

work was supported by grants from the Hinds Fund

and a fellowship from the Center for Graduate

Studies in Systematic Zoology and Paleontology at

the Field Museum of Natural History.

DESCRIPTIVE ANATOMY

Introduction

I have dissected the facial region in a series of

delphinids, consisting of members of the following

genera: Tursiops, Stenella, Grampus, Lagenorhynchus, Lagenodelphis, Orcinus, Pseudorca, Globicephala, Steno, and Cephalorhynchus. In addition,

I have dissected specimens of Phocoena, Phocoenoides, Inia, and Pontoporia, and have compiled

such comparative data as is available for other

genera. The families Physeteridae and Ziphiidae

have been deliberately omitted, as they appear to

be strikingly different and constitute a separate

problem.

The techniques employed consisted of gross dissection, along with gross coronal and sagittal sections of the soft structures of the facial region. The

dissections were limited to the area dorsal and

medial to the supraorbital process of the frontal

and the temporal crest, and anterior to the nuchal

crest. Extensive photographs were taken as a record

of the dissections. A large series of specimens of

Stenella, covering a wide size range, was dissected
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

and the nasal muscles fixed and weighed in order

to determine whether there was any asymmetry in

the muscular system.

I have chosen the common bottle-nosed dolphin,

Tursiops truncatus, as the standard of comparison,

and will describe it first. There are two outstanding reasons for this choice. First, Tursiops appears

to be a relatively generalized delphinid, from which

the conditions seen in the other genera could be

readily derived. Second, it has become the standard

experimental animal and, as such, there are data

available for it that are lacking for the less common animals. Unfortunately, I found material

difficult to obtain for Tursiops, and I have not

been able to dissect enough animals to establish

the range of individual variation in this species.

The descriptions that follow have not taken into

account the asymmetry seen in some of the facial

structures, as this will be treated in detail in a

later section. In general, the descriptions of the

nasal passages and diverticula begin with the deep

structures and proceed to the superficial ones, while

the muscular descriptions follow the opposite order.

DELPHINIDAE

DELPHININAE

Tursiops

MATERIALS.—The specimens of Tursiops truncatus consisted of the heads of two adult females and

a 53.5 cm male fetus. One adult head and that of

the fetus were dissected, while the other adult head

was frozen and sectioned coronally at 2 cm intervals.

NASAL PASSAGE AND DIVERTICULA.—The central

structure in the facial region of odontocetes is the

nasal passage. As in all mammals, the nasal passage

is a paired structure within the confines of the

skull. As the paired passages exit from the skull,

they are separated for a short distance by a cartilaginous nasal septum. Beyond this septum, they fuse

into a single passage and proceed dorsally through

the soft tissue. The nasal passages and diverticula

are lined throughout with a thin, darkly pigmented,

squamous epithelium.

Within the mass of soft tissue on the dorsal

surface of the skull, the nasal passages send off a

series of paired diverticula. In T. truncatus, as in

most small odontocetes, there are four pairs of

these situated in the soft tissues surrounding the

nasal passage. These diverticula are distensible to

varying degrees, but are not generally moveable

within the surrounding tissues.

Immediately dorsal to their exit from the skull,

while they are still separated by the septum, the

nasal passages send two diverticula, the premaxillary sacs (Murie, 1870), anteriorly along the dorsal

surface of the rostrum (Figures 2, 4). The ventral

surface of these diverticula lies directly upon the

periosteum of the premaxillae, while the dorsal

surface is in contact with the nasal plug muscle.

These are the largest of the pairs of diverticula in

T. truncatus.

The lateral margins of the nasal passages, as they

exit from the skull, are bounded (and slightly

occluded) by the diagonal membranes (Lawrence

and Schevill, 1956) (Figure 3). These membranes

run at an angle from the anterolateral wall of the

nasal passage, just internal to its exit from the

skull, posterodorsally to attach to the posterior end

of the nasal septum. They are thin membranes,

consisting only of the reflected nasal epithelium

with a slight amount of connective tissue and sometimes a few muscle fibers. In T. truncatus, as in

most of the delphinids, they are 1 to 1.5 cm wide.

Along the posterior edge of the nasal passages,

FIGURE 3.—Diagramatic dorsal view of the structures adjacent to the external bony nares in Tursiops truncatus.

(bnp=bony nasal passage, dm=diagonal membrane, ps=premaxillary sac.)
FIGURE 4.—Diagramatic views of the nasal diverticula of Tursiops truncatus: a, oblique view of

the intact diverticula; b, same view, vestibular sacs and part of the spiracular cavity removed.

(as=accessory sac, b = blowhole, bhl = blowhole ligament, iv = inferior vestibule, np=nasal plug,

ns=nasofrontal sac, ps=premaxillary sac, sc=spiracular cavity, vs=vestibular sac.)
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

just external to the diagonal membranes, lies a pair

of small chambers, the inferior vestibules (Gallardo, 1913) (Figures 2, 4). These extend dorsally and

posteriorly toward the vertex of the skull. A small

muscle (which will be discussed later) lies beneath

the posterior wall of these chambers. The anterior

wall is formed by the blowhole ligament, which

runs from the anterior tip of the vertex anterolaterally to the lateral edge of the premaxilla.

Dorsally the inferior vestibule opens into the nasofrontal sac, laterally into the accessory sac (described later). Schenkkan (1973) mentioned a

"small ventral extension" near the entrance of the

nasofrontal sacs to the nasal passage (inferior vestibule) in Tursiops. I did not find this in my limited

material, and am unable to interpret its significance.

The nasal plugs (Lawrence and Schevill, 1956)

are two fleshy bodies which protrude posteriorly

from the anterior wall of the 'nasal passage, just

dorsal to the premaxillary sacs (Figures 2, 4). They

are oval ventrally, where they fit into the bony

nares. Their free margins are produced into lips,

which fit into the paired inferior vestibules (Figure 2). The body of the nasal plugs consists of the

nasal plug muscle (Lawrence and Schevill, 1956),

which lies in a dense connective tissue matrix. This

muscle originates from the premaxilla anterior to

the premaxillary sac. Dorsally it grades into the fat

of the melon. In T. truncatus, as in most of the

other delphinids examined, the fat of the melon

extends only onto the right nasal plug, as noted

by Norris (1969) in Delphinus.

Opening laterally from the inferior vestibule is

the accessory sac (Schenkkan, 1971 = connecting

sac of Lawrence and Scheville, 1956). This diverticulum extends laterally for a short distance, then

turns anteriorly around the attachment of the blowhole ligament to the premaxilla (Figure 4). It is

smaller than the other diverticula, 1 cm or less in

diameter and 1 to 2 cm long. It ends blindly in the

posterolateral tissues of the nasal plug muscle. As

with the other diverticula, the accessory sacs are

paired, the right being the larger. The mouth of

this diverticulum appears to be occluded by a lateral extension of the lip of the nasal plug when

the nasal plug is in place over the bony nares.

Schenkkan (1971) pointed out that this diverticulum doesn't connect anything, and applied the

term "accessory sac," as the term "connecting sac"

was misleading. The structure termed "connecting

sac" by Evans and Prescott (1962), which connects

the nasofrontal sac with the nasal passage, is probably the inferior vestibule.

The nasofrontal sac (Murie, 1870 = tubular sac

of Lawrence and Schevill, 1956) lies in the tissues

surrounding the nasal passage, dorsal to the nasal

plugs (Figures 2, 4). It is convenient to speak of an

anterior and a posterior part of the nasofrontal sac,

with respect to the nasal passage. The posterior

part ends as a blind sac medially, just posterior to

the nasal septum. It extends, laterally, around the

edge of the nasal passage, where it becomes continuous with the anterior part. The blind termini

of both parts abut against the corresponding terminus of the contralateral sac. The collapsed diameter of this sac is about 1 cm, the length of the

right sac about 10 cm, the left about 7 cm. The

reflection of the sac around the lateral edge of the

nasal passage is referred to as the angle of the nasofrontal sac. In T. truncatus the angle is slightly

lobulated, particularly on the right side (Gruhl,

1911). The nasofrontal sac in T. truncatus is darkly

pigmented throughout its length. The posterior

part of the nasofrontal sac opens ventrally, by

means of a transverse slit, into the inferior vestibule.

The blowhole ligament (Lawrence and Schevill,

1956) is a strong connective tissue band, running

laterally from the anterior tip of the vertex to the

lateral edge of the premaxilla, just anterior to the

accessory sac. It lies anterior and ventral to the

nasofrontal sac, crossing anterodorsal to the communication of the latter with the inferior vestibule

(Figure 4). It is widest medially, where it forms a

substrate for the attachment of some of the musculature associated with the nasofrontal sacs. Laterally it becomes narrower and thicker. It sometimes

gives off a branch which passes posteriorly, dorsal

to the mouth of the accessory sac, and attaches to

the premaxilla just posterior to the accessory sac.

Purves and Pilleri (1973), in their description of

Platanista, found the homoloque of the blowhole

ligament to be cartilaginous, and considered it

equivalent to the crus lateralis of the lower nasal

cartilages of terrestrial mammals.

Immediately anterior to the midportion of the

blowhole ligament is an elliptical body (Figures

10, 16), which seems to be composed of yellowish

adipose tissue in a fine connective tissue matrix.

This body lies between the blowhole ligament and

the posterior wall of the nasal passage, and pro-
NUMBER 207

duces the faint ridge of the posterior fold (description follows).

The central portion of the nasal passage, dorsal

to the nasal plugs, has generally been referred to

in the literature as the spiracular cavity (Figures

2, 4). It is into this cavity that the inferior vestibule

opens ventrally and the vestibular sacs (description

follows) open dorsally. In morbid material of delphinids, this cavity appears as a transverse slit

extending from the nasal plugs upward to the

blowhole. It has been generally ignored as an

anatomical entity in this group, but is important

from a comparative standpoint, as it becomes

highly modified in some other odontocetes.

Dorsal to the nasal plugs, the spiracular cavity

opens into a pair of lateral diverticula, the vestibular sacs (Lawrence and Schevill, 1956) (Figures 2,

4, 6). These are wide flat diverticula, extending laterally from the nasal passage in a horizontal plane.

They are about 6 cm wide and 4 cm long. In the

morbid state the walls of these diverticula are wrinkled, indicating a certain amount of distensibility.

In T. truncatus, as in a few other species, there is

an indication of a small anterior lobe on the left

vestibular sac (Figure 24). This may be variable

and possibly accounts for the reverse asymmetry

noted by Schenkkan (1973) in one of his specimens.

On the anterior wall of the spiracular cavity, just

ventral to the vestibular sacs, is a small recess. This

extends horizontally across the wall of the spiracular cavity and forms a lip (the anterior fold of

Lawrence and Schevill, 1956) between it and the

vestibular sac (Figure 2). The posterior wall of the

spiracular cavity is produced into a slight ridge at

this point (the posterior fold of Lawrence and

Schevill, 1956), which fits against the recess in the

anterior wall, and is overlain by the anterior fold

when the nasal passage is closed.

The nasal passage opens onto the surface of the

head through the blowhole. The blowhole is

crescentic, with the concavity facing anteriorly.

Seen in cross section, the anterior lip of the blowhole is convex, fitting into a concavity in the posterior wall just ventral to the posterior lip. The

anterior lip of the blowhole is relatively soft and

mobile, while the posterior lip is more rigid.

MUSCULATURE.—The musculature associated with

the nasal passage is extremely complex and, until

the work of Lawrence and Schevill (1956), had not

received detailed anatomical coverage. Huber

(1934) stated that this muscular complex represents

an elaboration of the primitive m. maxillonasolabialis of mammals. Lawrence and Schevill (1956)

recognized six layers within this complex. I have

modified their plan slightly, as I was not able to

separate the muscles consistently according to their

definitions (particularly across the wide range of

morphologic types with which I was dealing). I

have, however, used their terminology with some

modifications where necessary.

The most superficial of the muscles associated

with the nasal passage is the pars posteroexternus

(pe). This muscle originates along the posterior

half of the supraorbital process, the temporal crest,

and a variable portion of the nuchal crest (Figure

5). It runs medially, posterior to the nasal passage,

to insert upon the vertex and into the contralateral

muscle. As is the case with all of the nasal muscles,

pe grades into the adjacent musculature. Anterolaterally it is gradational with the pars intermedius; posteriorly it is gradational with the pars

anteroexternus. I have found that I could make

consistent separations at its insertion, as its fibers

have a much more medial orientation that those of

the underlying muscle. This differs from the definition of Lawrence and Schevill (1956:119) in that

it includes none of the musculature which is in

direct contact with the vestibular sac.

The pars intermedius (i) consists of deep fibers

from the same muscle mass as pe, which diverge

from pe in an anterior direction (Figure 5). It

originates deep to pe, along the posterior half of

the supraorbital process, and inserts into the mass

of heavy connective tissue dorsal to the nasal plugs.

This follows the definition of Lawrence and Schevill (1956:121).

The pars anteroexternus (ae) is a much larger

muscle than either pe or i (Figure 6). It originates

from the anterior end of the supraorbital process

to the temporal and nuchal crests and the adjacent

bony surface (usually frontal, but occasionally

including the maxilla). Posteromedially it occupies

the fossa between the vertex and the nuchal crest.

The anteriormost fibers insert across the midline

into the contralateral muscle. Posteriorly the fibers

come to insert first upon the anterior wall of the

nasal passage, then the lateral edge, and finally the

posterior wall and the dorsal edge of the blowhole

ligament (Figure 6). The vestibular sac is contained within this muscle, which is loosely attached
10

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

to it both dorsally and ventrally. Thus ae presents

a series of fibers converging upon the nasal passage. Lawrence and Schevill (1956:122) defined ae

as only the anterior portion of the muscle described

above. Since I could find no consistent separation

into an anterior and a posterior portion, and, as

the modified definition seems to result in a functional entity, I have redefined this muscle.

Ae is most easily defined in dissection at its posterior insertion, where its anteriorly directed fibers

present a marked contrast to the underlying fibers

of the pars posterointernus. Although the directions of these two sets of fibers are quite different,

they are thoroughly intermeshed, forming an aponeurosis just dorsal to the nasofrontal sacs. Ae can

be separated from the pars posterointernus at its

insertion, but merges with it along its origin. Anteriorly ae becomes continuous with the underlying

fibers of the pars anterointernus at both origin and

insertion, and also with the posterior fibers of the

rostral muscle.

The pars posterointernus (pi) lies just deep to

ae, taking its origin from the frontal (and/or maxilla) at the level of the eye (middle of the supraorbital process) (Figure 7). Its origin extends

posteriorly, then medially into the fossa between

the nuchal crest and the vertex. It inserts via a

flat tendon, which runs in an arc posterior to the

nasal passage, into the contralateral muscle and the

aponeurosis formed with the fibers of insertion of

ae. Lawrence and Schevill's definition of pi (1956:

123) includes only the posterior portion of what I

have called ae. I cannot find a muscle or portion

of a muscle in their description corresponding to

what I have defined as pi. Accordingly, I was

tempted to substitute a new name to avoid confusion, but felt that this would require a complete

substitution for their names, which form a topographic system. I have found this system to be

particularly useful, and so have retained it, completely redefining pi.

Pi is easily separated at its insertion from the

rest of the muscles, although at its origin it is

indistinguishable from both the overlying (ae) and

underlying (ai) muscles.

The deepest and largest of the muscles associated

with the nasal passages is the pars anterointernus

(ai). This muscle takes its origin from a broad area

of the ascending process of the maxilla, between

the origins of ae and pi and the lateral border of

the premaxilla (Figure 8). It is indistinguishable

anteriorly from the medial rostral muscle. In order

to separate these two, I have arbitrarily drawn a

line from the anterior end of the supraorbital crest

medially to the premaxilla, and have called everything posterior to this line pars anterointernus.

The insertion of this muscle is into the connective

tissue mass anterior to the nasal passage, and

through it to the contralateral muscle. This muscle

is fanshaped, the posterior fibers running anteriorly

across the midline, the lateral fibers passing

directly medially and the anterior fibers running

posteriorly. A few of the deep anterior fibers of ai,

instead of inserting across the midline anterior to

the nasal passage, cross the fibers of insertion of

the posterior portion of the muscle and attach to

the lateral edge of the nasal passage. This definition represents a fusion of the pars anterointernus

and the pars profundus of Lawrence and Schevill

(1956:123-126).

The rostral musculature consists of an elongate

block lying along either side of the rostrum (Figures

8, 9). In transverse section this is seen to consist of

fibers radiating from a central area of origin along

the maxilla into the tissue of the lip, dermis, and

melon. This block of muscle can be divided into

two portions, with slightly differing fiber orientation. These are a lateral portion, primarily associated with the lip and the connective tissue adjacent to the melon, and a medial portion, which

inserts into the melon (Figure 9). The separation

between these two portions is seen in transverse

section as a diffuse zone of connective tissue. If this

separation is followed posteriorly, it becomes apparent that the lateral portion is continuous with the

superficial musculature of the nasal passage (pe, i,

ae and pi), while the medial portion is continuous

with the deep musculature (ai). This separation

becomes quite striking at the level of the antorbital

notch, where there is frequently a strong ridge

produced on the maxilla along the line of separation of the two parts.

The separation of the rostral muscle into lateral

and medial parts, continuous with different portions of the nasal musculature, raises the question

of the homologies of these muscle blocks. Huber

(1934) considered the posterior musculature to be

homologous with the parts nasalis of the m. maxillonasolabialis, while the rostral musculature was

considered to be homologous with the pars labialis
NUMBER 207 11

of that muscle. The continuity of the rostral musculature with the posterior musculature suggests

that if a division is to be made, it is between medial

and lateral elements, not anterior and posterior.

While this is a question best approached through

developmental studies, it seems useful to tentatively

designate the lateral rostral musculature and its

associated nasal musculature (pe, i, ae and pi) as

ae

FIGURE 5.—Oblique view of the superficial nasal musculature of Tursiops truncatus. (ae = pars

anteroexternus, b = blowhole, i = pars intermedius, pe = pars posteroexternus, rm = rostral muscle,

v = vertex.)

FIGURE 6.—Oblique view of the nasal musculature of Tursiops truncatus, at a slightly deeper

level than Figure 5. Pars posteroexternus, pars intermedius, and part of pars anteroexternus

removed to expose the vestibular sacs. (ae = pars anteroexternus, rm = rostral muscle, vs = vestibular sac.)
12

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

derivatives of the pars labialis and the medial

rostral musculature and ai as derivatives of the

pars nasalis of the m. maxillonasolabialis.

These descriptions are complicated and confusing, and a genreal summary may be useful at this

point. The most superficial muscle, pe, runs from a

ns

ai

FIGURE 7.—Oblique view of the nasal musculature of Tursiops truncalus, at a level intermediate between Figures 6 and 8. Pars anteroexternus completely removed. (ai = pars anterointernus, ns=nasofrontal sac, pi = pars posterointernus, rm = rostral muscle.)

dmm

im

ns

rm

FIGURE 8.—Oblique view of the deep nasal musculature of Tursiops truncalus. Pars posterointernus completely removed. (ai = pars anterointernus, dmm = diagonal membrane muscle,

im = intrinsic muscle, ns = nasofrontal sac, rm = rostral muscle.)
NUMBER 207 13

lateral origin to a medial insertion, posterior to

the nasal passage. Ae lies immediately under pe

and consists of fibers converging upon the nasal

passage from the margins of the facial region. Between these two muscles, and continuous at its

origin with both of them is i. This muscle differs

from ae and pe in having a more anterior insertion, and thus a different fiber direction. Pi is continuous at its origin with ae, but differs in having

an insertion entirely posterior to the nasal passage

(as does pe). Ai is continuous at its origin with pi,

but inserts entirely anterior to the nasal passage,

giving it a markedly different orientation. Ae and

ai are continuous anteriorly with each other and

with the rostral musculature. Posteriorly ae and ai

are separated by pi.

Associated with the vertex and the nasofrontal

sacs are a series of small muscles whose relationships are difficult to demonstrate. The muscle fibers

are extremely fine and permeated with an equally

fine connective tissue matrix which grades into the

connective tissue of the adjacent structures. Lawrence and Schevill (1956) refer to this group of

muscles as the intrinsic musculature (of the nasofrontal sac). They separate it into a major portion

lying posterior and lateral to the nasofrontal sacs,

and a minor portion lying anterior. I have found

the two to be continuous, and refer to the portions

described by them merely as the intrinsic muscle

(of the nasofrontal sac) (Figure 8).

In T. truncatus this muscle originates from the

anterodorsal surface of the vertex and the medial

end of the nasofrontal sac. It passes laterally, along

the anterior, ventral, and posterior aspects of the

FIGURE 9.—Cross sections of the rostral structures of Tursiops truncatus (adult female): a, 10

cm posterior to the tip of the rostrum; b, 14 cm posterior to the tip of the rostrum; c, 18 cm

posterior to the tip of the rostrum (at the level of the antorbital notch). (an = antorbital notch,

dct = dermal connective tissue, m = melon, npm = nasal plug muscle, r = rostrum, rm = rostral muscle, rm-l=lateral portion of the rostral muscle, rm-m = medial portion of the rostral muscle.)
14

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

nasofrontal sacs, occasionally completely encompassing the sac. Throughout its length, its connective tissue matrix is closely associated with that of

the adjacent structures, particularly the nasofrontal

sac and blowhole ligament. It passes on either side

of the communication of the nasofrontal sac with

the inferior vestibule, then turns anteriorly, entering the dorsolateral surface of the nasal plug mass

and merging with the nasal plug muscle.

Posterior and ventral to the intrinsic muscle lies

another small muscle of similar composition. Due

to the complexity of this region, this muscle has

escaped the attention of earlier workers. It originates from the anterolateral surface of the vertex,

lateral and deep to the intrinsic muscle. It then

passes anteriorly, ventral to the intrinsic muscle

and nasofrontal sac, to insert along the attached

margin of the diagonal membrane. Very rarely it

sends a few fibers into the free portion of the membrane. Due to the connective tissue in'which these

muscles are imbedded, it is difficult to ascertain

the exact relationship of this muscle to the intrinsic

muscle. In some specimens it appears to be sharply

delimited from the intrinsic muscle, while in others

it seems to be continuous with it. I have designated

this the diagonal membrane muscle, in reference

to its insertion.

MELON.—A frequent problem in the literature

dealing with the odontocete nose is the distinction

between melon, adipose cushion, spermaceti organ,

and case. At one time or another, all of these

names have been applied to the adipose connective

tissue structure anterior to the nasal passage in

delphinids.

"Melon" is a term apparently originating in the

whaling industry, referring to the similarity of this

mass of tissue, when it is removed from the head

of the animal, to a section of melon (particularly

in Globicephala, where it resembles a section of

ripe muskmelon).

"Adipose cushion" is a term coined by Howell

(1930), who evidently did not care for the colloquial nature of "melon." He described this structure in some detail and specifically indicated that

he was referring to the smaller odontocetes.

The term "case" is another which has originated

in the whaling industry, where it was used in reference to the oil-filled cavity in the head of the sperm

whale.

Pouchet and Beauregard (1885) apparently originated the term "spermaceti organ" in reference to

the structure more colloquially known as the case.

Howell (1930) discussed the possible homology

of the adipose cushion (melon) and the spermaceti

organ (case), and decided that they were probably

unrelated. Raven and Gregory (1933), however,

were of the opinion that they were homologous,

and applied the term "spermaceti organ" to the

structure seen anterior to the nasal passages in

Monodon. This structure, however, appears to be

no different from the adipose cushion (melon) of

delphinids. Schenkkan and Purves (1973) examined

the anatomy of the nasal complex in physeterids

and concluded that the spermaceti organ in Physeter and Kogia was unrelated to the melon of

delphinids.

Despite the rather colloquial flavor of the term

"melon," it has been frequently and consistently

used in the literature, and I have elected to retain

it as applied to delphinids. This is specifically

equivalent to the term "adipose cushion" of Howell

(1930). I have not used Howell's term because of

its functional implications. The functions of this

structure are still not well enough understood that

we can afford to hamper our reasoning with terms

implying a specific function.

The term "spermaceti organ" should be restricted

to a distinct fatty body, separated from the other

facial structures by a connective tissue wall, as seen

in Physeter. The free usage of these terms in the

past few years has led to considerable confusion

as to which animals have a spermaceti organ and

which do not.

The melon lies approximately in the center of

the soft tissue mass of the face (Figures 2, 9). Laterally it grades into the rostral muscle and ventrally

into the nasal plug muscle. In some dissections, a

sharp distinction can be seen between the dorsal

surface of the melon and the adjacent connective

tissue of the dermis. This distinction seems to be

mainly on the basis of orientation and distribution

of blood vessels, the melon being less vascular than

the dermis. This is sometimes accentuated upon

exposure of a section to the air, the melon and the

dermis apparently oxidizing differently. This differentiation continues anteriorly, separating the dermis from the melon. Posteriorly the melon grades

into the nasal plug mass, penetrating into the tissue

of the right nasal plug.

Litchfield et al. (1973) have demonstrated topo-
NUMBER 207 15

graphic variation in the lipid content of the melon,

while Norris and Harvey (1974) have shown a

similar variation in acoustic properties of the

melon.

VASCULATURE.—The vascular supply of the facial

region in T. triincatus (as in the other delphinids)

is derived from blanches of the internal maxillary

artery emerging from the infraorbital foramina.

Branches from the posterior infraorbital foramina

ramify between the layers of the nasal musculature

and supply most of the region posterior to the

antorbital notch. A bundle of parallel vessels arises

from one of the anterior infraorbital foramina, just

medial to the antorbital notch, and courses anteriorly on the surface of the maxilla. At intervals

these vessels turn dorsally to supply the rostral

structures. The facial artery is small and appears

to supply only the area around the angle of the

mouth and, to a lesser extent, the tissue of the

upper lips. There is a prominent vascular system

in the superficial fascia over the nasal musculature,

which appears to be largely venous. It communicates posteriorly with occipital vessels and laterally

with temporal vessels.

None of the facial elements are heavily vascularized, the most prominent vasculature being that

of the posterior superficial fascia mentioned above.

The melon is markedly avascular, the large vessels

seen in its periphery being destined for the skin.

INNERVATION.—The sensory innervation of the

facial structures is derived from infraorbital

branches of the maxillary division of the trigeminal nerve. These emerge onto the surface of the

face through the various infraorbital foramina. Posteriorly, large branches of these nerves pass to the

nonmuscular structures associated with the nasal

passage, particularly the nasal plugs and the deep

structures around the vertex. The diverticula do

not appear to be heavily innervated, nor does the

melon (contra Huber, 1934). Khomenko (1970)

reported encapsulated nerve endings in the walls

of the diverticula, but did not state that they were

particularly abundant. The skin is known to be

heavily innervated (Palmer and Weddell, 1964),

but the patterns of this innervation could not be

determined grossly. Presumably the cutaneous

innervation is also derived from the infraorbital

branches of the trigeminal nerve, although occipital

nerves were seen to extend into the facial area in

a fetal T. truncatu.s. There are extensive anastamoses between elements of the facial and trigeminal

nerves, particularly between the layers of the nasal

musculature near their origins.

So far as is known, all of the motor innervation

of the nasal muscles is provided by the facial nerve.

This nerve passes anteriorly, beneath the orbit, to

emerge onto the face through the antorbital notch.

The facial nerve is heavily invested with connective

tissue throughout its length and is easily mistaken

for a tendinous structure. As it passes through the

antorbital notch it branches extensively in the

dense connective tissue filling the notch. Beyond

this point it has a diffuse distribution throughout

the layers of the facial muscles.

GLANDULAR STRUCTURES.—Glandular tissue has

recently been discovered in the area of the inferior

vestibule in T. triincatus (Maderson, 1968; Evans

and Maderson, 1973). These are small exocrine

glands, opening via minute crescentic pores. I overlooked these in my dissections, and it is possible

that their distribution throughout the delphinids

is more extensive than is now known.

The following descriptions of delphinid genera

are based upon comparison with T. truncatus, and,

in general, only the differences observed are treated

in any detail. The genera are treated in an appoximate taxonomic order, with those most similar to

Tursiops being described first.

Stenella

MATERIALS.—Forty-four individuals of Stenella

attenuata and S. longirostris were dissected, ranging

in size from neonates to large adults. Two adult

males of S. coernleoalba and one adult male of S.

plagiodon were also dissected.

The species of Stenella examined show very little

differentiation from the condition seen in Tursiops

truncatus, and constitute a relatively homogenous

group in their facial anatomy.

NASAL PASSAGES AND DIVERTICULA.—The premaxillary sac in Stenella was quite uniform in the

species examined, and was similar to that of T.

truncatus (Figure 24). The only difference noted

was a slight increase in the asymmetry of this

structure in S. cocruleoalba.

The nasal plugs showed little variation in Stenella, the right plug always being the larger and

having a proportionately larger lateral lip. As with
16

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

a

FIGURE 10.—Dorsal views of dissections of the nasal musculature of Stenella plagiodon (in each

view the structures on the lefthand side are dissected one level below those on the right):

a, superficial dissection; b, deep dissection. (ae = pars anteroexternus, ai = pars anterointernus,

dmm = diagonal membrane muscle, i = pars intermedius, ns = nasofrontal sac, pe = pars posteroexternus, pi = pars posterointernus, rm = rostral muscle, vs = vestibular sac.)
NUMBER 207 17

a number of characters, this asymmetry was slightly

greater in S. coendeoalba.

An accessory sac was present in all of the Stenella

examined. This sac was quite small, on the order

of 5 mm or less in length in all but S. coendeoalba,

where it was slightly more than 1 cm long. A posterior branch of the blowhole ligament, passing over

the mouth of the accessory sac, was seen in some

individuals of all of the Stenella species. It was

only seen on the left side.

The nasofrontal sac showed some variation in

the Stenella species. The posterior portions abut

against one another at the midline, as in T. truncatus. The anterior portions also meet in the midline and actually overlapped by about 1.5 cm in

the only specimen of 5. plagiodon examined. In

this instance the right sac lay dorsal to the left.

The pigmentation pattern of these sacs is highly

variable, and was not seen to fit any particular

scheme. The posterior portions are nearly always

darkly pigmented, but were light colored in some

specimens of S. attenuata and 5. longirostris. The

anterior portions are more variable. A common

situation was that in which the entire left anterior

portion was dark, while the medial portion of the

right was unpigmented. In addition to being longer,

the right anterior portion was slightly wider than

the left, more so in S. coendeoalba.

The vestibular sacs are of moderate size in Stenella, the left being somewhat larger than the right

in S. attenuata and S. longirostris. The left sac was

also situated more anteriorly than the right in

these two species. This was not the case in S. coeruleoalba and S. plagiodon, where the sacs were

roughly equal and both lay slightly more anterior

to the nasal passage. The anterior fold of the right

vestibular sac was consistently larger than the left

in S. attenuata and S. longirostris, the right usually

being 1.0 to 1.5 cm wide, while the left was 0.2 cm

or less. The opposite was true in 5. plagiodon,

where the left anterior fold was about 1.5 cm wide,

the right 0.8 cm. In S. coendeoalba the right anterior fold was extremely large, 2.0 cm wide, while

the left was on the order of 0.2 cm.

MUSCULATURE.—Outside of minor individual

variation in the extent of origin of layers of the

posterior musculature, and in the relative size of

some of these layers, there were no observable

differences in the nasal musculature.

The intrinsic musculature of the nasofrontal sac

showed no variations within the Stenella species,

with the exception of being slightly larger in S.

coendeoalba.

The diagonal membrane muscle is subject to

considerable variation in Stenella. It is generally

larger on the right side, although the reverse was

true in one S. attenuata. As it passes ventral to the

blowhole ligament, a few fibers may attach to the

ligament. There is considerable variation in the

extent to which this muscle enters the diagonal

membrane. As in T. truncatus, it usually does not.

However, in one specimen of S. attenuata the muscle on the left side extended to the free edge of the

membrane, while that on the right did not enter

the membrane at all. In another specimen of S.

attenuata a few of the lateral fibers of both muscles

entered the free portion of the membrane. This

muscle was extremely large in S. coeruleoalba, but

did not enter the free portion of the membrane.

OTHER STRUCTURES.—The anterior rostral structures, both the muculature and the melon, showed

no noticeable variation throughout the Stenella

species, nor any appreciable differences from the

condition seen in T. truncatus.

Delphinus

NASAL PASSAGES AND DIVERTICULA.—The arrangement of the nasal apparatus in Delphinus delphis

is very similar to that of Tursiops and Stenella, as

shown by Gruhl (1911), Lawrence and Schevill

(1956), and Schenkkan (1973). Gruhl's work is

particularly useful, as he illustrated the diverticula

in a number of individuals, including a fetus.

The vestibular sac is very similar to that of

Tursiops and Stenella, particularly in the presence

of a small anterior lobe on the left side.

The nasofrontal sac is virtually indistinguishable

from that of Stenella, and does not have the lobulations seen on the angle of the right sac in T.

truncatus. Gruhl's illustration of the nasofrontal

sac of a 53.8 cm fetus is of interest, in that it shows

a marked asymmetry in the degree of development

of the right and left sacs, the right sac developing

its anterior portion more rapidly than the left. The

accessory sac is similar to that of T. truncatus, and

is slightly larger than that of all of the Stenella

species, except S. coeruleoalba.

MUSCULATURE.—The musculature appears to be

no different from that of Tursiops.
18

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

OTHER STRUCTURES.—The melon and the rostral

structures are similar to those of Tursiops.

Lagenorhynchus

MATERIALS.—One juvenile Lagenorhynchus albirostris and a juvenile L. acutus were dissected.

NASAL PASSAGES AND DIVERTICULA.—The premaxillary sacs of L. albirostris differ from those of Tursiops and Stenella in having a lateral diverticulum

on the right side (lateral premaxillary sac). This

diverticulum opens along the middle two-thirds of

the lateral surface of the right premaxillary sac,

extends about 1 cm lateral to the edge of that sac,

and ends blindly about 1 cm posterior to the posterior margin of its orifice (Figure 14). This structure

was either very small or lacking on the left. Nothing similar to this diverticulum has been seen in

any of the other dissections, except that of a juvenile Lagenodelphis hosei. Schenkkan (1973) did not

mention this diverticulum, though he dissected

nine specimens of this species. Its presence in the

single specimen which I examined might be considered anomolous, were it not also seen in a juvenile Lagenodelphis hosei. There was but a trace

of it, however, in an adult female Lagenodelphis

hosei, raising the possibility that it may be a juvenile character which is lost with age. This diverticulum was absent in the single L. acutus specimen

which I dissected, and is not mentioned in Schenkkan's account of this species. It also seems to be

lacking in L. obliquidens and L. obscurus (Schenkkan, 1973).

The nasofrontal sacs in L. albirostris are extremely

different from most of the other delphinids. In the

specimen examined, these were injected with

silastic rubber, so some idea of their distended size

was gained. The posterior portion of the nasofrontal sacs is approximately the same size as in T.

truncatus, but the anterior portion is much larger.

The increase in size is confined to the width of

the sacs, and the sacs do not overlap one another.

In this specimen the anterior portion of the left

nasofrontal sac lay on the lateral surface of the

nasal plug mass, while that of the right extended

onto the anterior surface, crossing the midline. The

right sac appeared to be about twice the size of the

left, although neither was expanded to its maximum extent. The distension of the sacs was limited

more by the adjacent tissues than by the dimensions of the sac itself. Murie (1871) apparently

overlooked the nasofrontal sacs in his description

of L. albirostris. Schenkkan (1973) found the same

condition in the L. albirostris which he dissected.

Hypertophy of the nasofrontal sacs is* apparently

limited to L. albirostris, as those of L. obscurus

(Gallardo, 1913; Schenkkan, 1973), L. obliquidens

(Schenkkan, 1973), and L. acutus (Schenkkan,

1973) are similar in development to those of

Tursiops.

The accessory sacs in the specimen of L. albirostris which I dissected were relatively large, particularly the right sac, which measured 3 cm long

by 1 cm wide. Schenkkan (1973) also noted that

these diverticula were large in this species, and

described a caudal portion extending posterior to

their communication with the inferior vestibule.

He noted a similar caudal extension on the right

accessory sac in L. acutus, though I did not find

this in the single specimen which I dissected. The

accessory sacs in L. obliquidens and L. obscurus are

essentially similar to those of Tursiops (Schenkkan,

1973).

The vestibular sacs of L. albirostris presented no

pronounced differences from those of Tursiops. The

anterior folds were large on both sides, that on the

right being about 1.5 cm wide, the left 1.0 cm. The

folds usually seen in the walls of the vestibular sac

were deeper in this specimen than in T. truncatus,

and some of them seemed to be permanent features

(i.e., incapable of distension). Schenkkan (1973)

noted that the ventral walls of the vestibular sacs

in L. albirostris were thickened, which probably

correlates with my observations on folding. Schenkkan (1973) described extensive tabulation in the

lateral edge of the vestibular sacs in L. acutus, and

I found a similar condition in the specimen which

I dissected. He also noted that their placement was

more caudal to the blowhole, which agrees with

my dissection. Schenkkan's (1973) specimen of L.

obliquidens was damaged, but did not appear to

present any major differences from Tursiops.

Schenkkan (1973) noted a reverse asymmetry in the

vestibular sacs of L. obscurus, the left being larger

than the right, though apparently to no great

extent, as it is not apparent in his illustration of

this species. Gallardo's (1913) comments are too

brief to provide a comparison.

MUSCULATURE.—The nasal musculature in L.

albirostris differed in a few details from that of
NUMBER 207 19

T. truncatus. Pe inserted almost entirely across the

midline, with only a few fibers attaching to the

vertex. There was no discernible i on either side.

The tendons of insertion of ae and pi formed more

of an aponeurosis than in T. truncatus, and were

more intimately attached to the connective tissue

above the posterior end of the nasal septum. The

nasal musculature in L. acutus presented no

discernible differences from that of Tursiops.

The intrinsic muscles, the muscle of the diagonal

membrane, and the membrane itself in both species

examined presented no differences from those of

T. truncatus. Nor did the nasal plugs show any

unusual features.

OTHER STRUCTURES.—The structures of the rostrum showed a few differences from those of T.

truncatus. The distinction between the medial and

lateral rostral muscles was greater in L. albirostris.

There was an area of extremely dense connective

tissue in the dermis just anterior to the blowhole.

The connective tissue in this area is ordinarily

slightly denser than in the rest of the dermis, but

not as strikingly so as in this specimen.

Lagenodelphis

MATERIAL.—A juvenile male and an adult female

of Lagenodelphis hosei were dissected.

NASAL PASSAGES AND DIVERTICULA.—The premaxillary sac possessed a small diverticulum on the

right side (lateral premaxillary sac) similar to that

seen in Lagenorhynchus albirostris (Figure 13).

This was more pronounced in the juvenile male,

hence may be related either to age, sex, or individual variation. Otherwise the premaxillary sacs were

similar to those of Tursiops truncatus.

The accessory sac was very small on the left,

appearing as a slight indentation in the lateral wall

of the inferior vestibule. That on the right was

quite large, extending 1 cm anterior to the blowhole ligament.

The nasofrontal sacs were similar to those of

T. truncatus. While the right sac was larger than

the left, neither showed any sign of the expansion

seen in Lagenorhynchus albirostris. The two sacs

were darkly pigmented throughout, met anterior

to the nasal passage in the juvenile, and overlapped

anteriorly by about 1 cm in the adult. The angle

of the right sac was slightly lobulated, as in T.

truncatus.

The vestibular sacs were of nearly equal sizes,

the right being possibly a little larger than the left.

They did not extend as far laterally as in T. truncatus, ending very close to the lateral edge of the

nasal passage. The portion of the sacs posterior to

the nasal passage was larger than the portion anterior. The anterior fold was quite large on the right,

comparable to the condition seen in Lagenorhynchus albirostris and Stenella coeruleoalba.

None of the deep structures associated with the

nasal passage (intrinsic muscles, diagonal membrane and muscle, blowhole ligament, and nasal

plugs) were noticeably different from those of T.

truncatus.

MUSCULATURE.—The nasal musculature of L.

hosei showed no outstanding differences from that

of T. truncatus. Pe was well developed and inserted

across the midline between the vertex and the nasal

passage. Its origin extended further posteromedially

than in T. truncatus, making it a little more difficult to separate from ae. There appeared to be no

differentiation of a pars intermedius. The superficial fibers of ae had a more anterior orientation

than in T. truncatus, but this became more medial

in the deeper layers. The posterior insertion of ae

was less well differentiated than in T. truncatus.

OTHER STRUCTURES.—The only noticeable difference from T. truncatus in the rostral structures

was a sharper differentiation of the rostral musculature into medial and lateral portions. The melon

showed no unusual features.

Grampus

MATERIALS.—One adult male of Grampus griseus

was dissected.

NASAL PASSAGE AND DIVERTICULA.—The right premaxillary sac is disproportionately larger than the

left in G. griseus (Figure 25). This increase has

taken place in the posterolateral portion of the sac,

where the additional space is occupied by an unusually large lateral lip of the nasal plug. The

lateral lip on the right side is about 2 cm wide,

while that of the left side is only 0.5 cm. There are

no lateral diverticula from the premaxillary sac,

and, aside from the lateral lip, the nasal plugs were

as in Tursiops truncatus.

The accessory sac was somewhat larger than that

of T. truncatus, the right one being 2.0 cm long,

the left 1.5 cm long. None of the previous workers
20

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

ae

FIGURE 11.—Grampus griseus (dissection of the nasal musculature, dorsal views): a, superficial muscles removed to level

of vestibular sacs; b, ae removed; c, pi removed. (ae = pars

antcroexternus, ai = pars anterointernus, ns = nasofrontal sac,

pi = pars posterointernus, sc = spiracular cavity, v = vertex,

vs = vestibular sac.)

(Murie, 1870; Bouvier, 1889; Danois, 1911) mention

a structure which could be interpreted as this sac.

The nasofrontal sacs present some striking differences from those of T. truncatus (Figures 11, 25).

The posterior portions of the sacs are similar to

those of T. truncatus, but the anterior portion of

the right sac is considerably larger, though not

nearly so much as that of Lagenorhynchns albirostris. The greatest difference is seen on the left side,

where the anterior portion was lacking, the posterior portion ending about 1 cm lateral to the edge

of the nasal passage. Murie (1870) described essentially the same situation in the specimen of G.

griseus examined by him. His illustration of the

diverticula, however, appears to be slightly in error,

and gives the impression that the anterior portion

of the right nasofrontal sac opens into the inferior

vestibule independent of the posterior portion.

This gave rise to Bouvier's (1889) mention of a

"sac facial impair," which added to the confusion

surrounding the nasal diverticula.

The vestibular sac of G. griseus was unusual in

that the left was larger than the right by about

10%, and extended farther laterally (Figure 25).

Both vestibular sacs lay more posterior to the nasal

passage than in T. truncatus. The anterior folds

were not particularly unusual, that of the right side

being about 0.8 cm wide, while that of the left was

barely discernible.

MUSCULATURE.—The intrinsic musculature of the

nasofrontal sac was slightly larger than in T. truncatus, and its gradation into the lateral portion of

the nasal plug muscle was more clearly seen. Along

its posteromedial origin some of its fibers interdigitated with fibers of the diagonal membrane muscle.

Otherwise the two were quite distinct. The diagonal membranes were of approximately equal size,

and neither muscle reached the free edge of the

membrane. Murie (1870) seems to have been the

only author to notice the difference between the

intrinsic muscle and the muscle of the diagonal

membrane. The muscle labeled "1 " in his figure 1

appears to represent the latter muscle, although he

did not discern its insertion into the diagonal

membrane.

The pars posteroexternus of G. griseus differs

markedly from that of T. truncatus (Figure 11).

It originates from the posterior fourth of the supraorbital process, runs posteromedially along the

temporal crest, and inserts upon the lateral portion
NUMBER 207 21

of the nuchal crest. This muscle was about twice

as large on the left as it was on the right. The fibers

of pe were heavily invested with fat and connective

tissue, giving an appearance unlike the rest of the

posterior nasal musculature. On its deep surface

it was gradational with ae. A small superficial slip

of muscle on the anterior surface of ae may have

represented a poorly differentiated i. Pi was unusual

in that there was a deep posterior portion which

originated from the lateral surface of the vertex,

medial and deep to the posterior origin of ai. Normally pi originates entirely posterior and superficial

to ai.

The rostral muscles were considerably different

from those of T. truncatus. They were larger than

in that species, particularly the medial portion

(Figure 12). The differentiation between the lateral

and medial portions was sharper in G. griseus than

in T. truncatus. This differentiation is associated

with a strong crest along the lateral edge of the

maxilla, which marked the separation of the two

muscle bodies.

OTHER STRUCTURES.—The melon of G. griseus is

much larger than that of most delphinids (Figures

12, 25). This is particularly true in the posterolateral portions, producing a slightly bilobate,

bulbous forehead. The expansion of the forehead

is largely due to an increase in the size of the

melon, with little corresponding increase in the

heavy dermal connective tissue external to it. The

result is a very soft mass of tissue, in marked contrast to the other bulbous-headed genera which I

have examined.

Aside from some of the points mentioned above,

this description agrees with that of Murie (1870).

Bouvier (1889) merely compiled data from earlier

literature. The description of a 125 cm fetal G.

griseus by Danois (1911 is confused with regard

to the nasal diverticula. He illustrated what

appears to be the posterior portions of both nasofrontal sacs, and shows nothing which could be an

anterior portion. This might be due to the stage

of development of the specimen, although it was

relatively large. It will be recalled that the anterior

portion of the right nasofrontal sac was well developed in a 53.8 cm fetus of Delphinus delphis

described by Gruhl (1911).

There is some confusion introduced into the literature by Murie's (1870, fig. 1) illustration of the

"maxillary sacs" as lying deep to the nasofrontal

FIGURE 12.—Grampus griseus: a, sagittal section of the

rostral structures, superficial dissection of the nasal musculatue, oblique view; b, parasagittal section of the rostral

structures, same view as above, 5 cm lateral to above section; c, transverse section of rostral structures at level of

antorbital notch. (ae = pars anteroexternus, dct = dermal connective tissue, i = pars intermedius, m = melon, pe = pars postcroexternus, r = rostrum, rm = rostral muscle, rm-l=lateral

portion of rostral muscle, rm-m = medial portion of rostral

muscle; heavy lines indicate principal orientation of connective tissue fibers in the melon.)
22

sacs. From this they could be interpreted as being

the accessory sacs. Murie also mentioned that the

nasofrontal sac opened into the maxillary sac,

which would further support this conclusion. However, in his description of L. albirostris (1871), the

"maxillary sac" is clearly equivalent to the vestibular sac. Danois (1911) follows Murie in his illustration ("inspire de Murie") and shows the "sacs

maxillaires" as lying deep to the nasofrontal sacs.

I am of the opinion that the maxillary sacs are

equivalent to the vestibular sacs in both Murie's

and Danois' accounts, and that both were in error

as to their position. This seems more likely than

that both of them had missed the large vestibular

sacs and were describing the accessory sacs instead.

Further confusion arose as a result of Danois' labeling the spiracular cavity (bony nasal passages) of

Murie as spiracular sacs, and describing them as

though they were diverticula. It is clear that much

of this derives from Danois' misunderstanding of

Murie's illustration.

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

ORCININAE

Orcinus

MATERIALS.—One large adult male and an adult

female of Orcinus orca were dissected.

NASAL PASSAGE AND DIVERTICULA.—The premaxillary sacs of O. orca show no unusual features, and,

if anything, are relatively small. The diagonal membrane of the right is slightly larger than that on

the left.

The accessory sacs are small, relative to the size

of the animal. The right sac was about 3 cm long,

the left about half that size.

The anterior portion of the right nasofrontal sac

was 2-3 times the diameter of the left. The posterior portions of the nasofrontal sacs were not

notably larger in diameter than the left anterior

portion and were considerably smaller than the

right. Schenkkan (1973) stated that the posterior

portions were larger in diameter than the anterior

FICURE 13.—Orcinus orca: a, nasal musculature, dorsal view of the superficial dissection; b, nasal

musculature, dorsal view of dissection to level of vestibular sac. Dorsal wall of vestibular sac

removed, (ae-pars anteroexternus, npm = nasal plug muscle, pe = pars posteroexternus, sc =

spiracular cavity, tm = temporal muscle, v = vertex, vs = vestibular sac.)
NUMBER 207 23

in his material. He also noted that their terminations did not reach the mesial axis of the head,

whereas they met anteriorly in both of my specimens. Gruhl (1911) noted that the anterior portions of the nasofrontal sacs developed later than

the posterior in a series of Delphinns delphis which

he examined. Thus the differences between my

results and those of Schenkkan may merely reflect

age differences.

The vestibular sacs lay considerably posterior to

the nasal passage, quite different from their situation in Tursiops and Stenella. Schenkkan (1973)

stated that they lay lateral to the blowhole,

although his illustration shows them lying posterior, similar to the situation in my dissections.

They were subequal in size, the left being slightly

larger. There was a small anterior fold on the left

and a very large one (2 cm deep) on the right.

MUSCULATURE.—The nasal musculature of O. orca

exhibited a few peculiarities. The pars posteroexternus was well defined, inserting across the midline via a series of well-defined tendons (Figure 13),

instead of the aponeurosis seen in T. truncatus.

There was no pars intermedius, nor were there any

bv

dct

FIGURE 14.—Orcinus orca, sagittal section of rostral structures. (bv = blood vessel, dct = dermal connective tissue, m =

melon, npm^nasal plug muscle, r = rostrum.)

fibers of ae arising posterior to the blowhole and

inserting anterior to it. This is in marked contrast

to the rest of the delphinids. The posteromedial

fibers of ae inserted into the heavy posterior wall

of the nasal passage, instead of into the blowhole

ligament. However, as they were heavily intertwined with the posteromedial fibers of pi which

did insert upon the blowhole ligament, the functional insertion was unchanged.

The anterior portion of the intrinsic musculature ran diagonally across the dorsal surface of the

nasofrontal sac, but assumed a more parallel course,

grading into the rest of the muscle on the ventral

surface. The diagonal membrane muscle was continuous posteriorly with the intrinsic muscle. In

the large male the diagonal membrane muscle did

not enter the free portion of the membrane, but

did in the female.

The nasal musculature of Orcinus is generally

similar to that of Tursiops, and shows no particular resemblance to Phocoena, as implied by Schenkkan (1973).

OTHER STRUCTURES.—The rostral structures in O.

orca were relatively small (Figure 14). The medial

and lateral rostral muscles were well differentiated,

the latter entering the lips more than in other

delphinids. The melon was small and poorly differentiated. Its entry into the nasal plugs was strongly

asymmetrical, showing a clear fatty area on the

right side.

Pseudorca

MATERIALS.—An adult male and an adult female

of Pseudorca crassidens were dissected.

NASAL PASSAGES AND DIVERTICULA.—Pseudorca

crassidens is similar to Tursiops truncatus in the

anatomy of the facial structures. The premaxillary

sacs and nasal plugs present no unusual features,

nor do the nasofrontal sacs (Figures 25). The right

accessory sac is about 2 cm long, the left is much

smaller. A small posterior branch of the blowhole

ligament was seen on the right side. The vestibular

sacs lie mostly posterior to the nasal passage, and

are relatively small.

MUSCULATURE.—The pars posteroexternus of the

nasal musculature was poorly differentiated. There

was, however, a large pars intermedius. The rest of

the musculature was similar to that of T. truncatus.

The rostral muscles are relatively small, the lat-
24

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

eral rostral muscle entering into the lips more than

in most delphinids.

OTHER STRUCTURES.—The melon is surprisingly

small, the bulk of the facial mass being made up of

coarse dermal connective tissue in a fatty matrix.

There is a well-defined connection between the

melon and the right nasal plug.

A moderate degree of sexual dimorphism was

observed in the shape and size of the forehead in

Pseudorca (Figure 15). In the male the fatty connective tissue anterior to the melon extended farther anteriorly than in the female. No difference

could be seen in the melon, which is not welldefined in this species. A similar situation is seen

a

FIGURE 15.—Pseudorca crassidens, lateral views of the external appearance of the heads, showing the degree of sexual

dimorphism in external head shape: a, female; b, male.

in the illustrations of a saggital section of the forehead tissues of a male Pseudorca presented by

Richard (1936, pi. VI: fig. 10). A comparable situation exists in Globicephala, where the fatty connective tissue of the forehead is more extensive in

the adult males than in the females.

Globicephala

MATERIALS.—A large adult male and a neonate

of Globicephala melaena were dissected.

NASAL PASSAGES AND DIVERTICULA.—The premaxillary sacs and nasal plugs of G. melaena are similar

to those of Tursiops tnincatus, as is the diagonal

membrane.

The accessory sac on the right side is extremely

large, 4 cm long and 2 cm wide (Figures 16, 24),

while that of the left side is about 1 cm long by

1 cm wide.

The angle of the right nasofrontal sac in G.

melaena is extremely unusual (Figure 16). There

is a large lateral sacculation, which, when opened,

contains a series of trabeculea. These trabeculae

are formed by invaginations of the lateral wall of

this diverticulum containing slips of the intrinsic

musculature. This may allow the intrinsic musculature to compress this sacculation without affecting the rest of the diverticulum. The anterior

portion of the right nasofrontal sac is slightly

expanded, and is unpigmented in its medial half.

The anterior portions of the two sacs abut against

one another. The posterior portion of the left nasofrontal sac has an elongate posterior sacculation

along its posterodorsal surface. Internally this sacculation is separated from the rest of the sac by a

fold of epithelium.

The vestibular sacs are roughly equal in size.

They extend a short distance anterior to the nasal

passage, where they slope into the anterior lip of

the blowhole. Their greatest extent is posterolateral

to the nasal passage. The anterior folds are well

developed on both sides, the cleft beneath them

being about 1 cm deep. The anterior fold overhangs the slit of the nasal passage by 1.8 cm on the

left and 1.5 cm on the right. Stenella plagiodon

was the only other delphinid in which the left

anterior fold was larger than the right.

MUSCULATURE.—The general impression obtained

from a dorsal view of the nasal musculature of

G. melaena is that it has been anteroposteriorly
NUMBER 207 25

compressed (Figure 17). There is a well-developed

pe, which originates from the posterior third of the

supraorbital process and inserts across the midline

without attaching to the vertex. The pars intermedius is larger than in T. trurcatus and the other

delphinids, apparently having incorporated more

of the underlying fibers of ae into itself. Both pe

and i are heavily invested with fat and connective

tissue. Ai and pi are closely related posteromedially,

where they both originate in the fossa lateral to

the vertex. The deep posteromedial fibers of ae

grade into pi with no perceptible break. There

were several well-differentiated muscle fasciculi in

this zone of intergradation, giving the appearance

of a series of separate muscles interposed between

the fibers of ae and pi (Figure 17). The tendon of

insertion of pi is attached to the connective tissue

above the posterior end of the nasal septum.

The diagonal membrane muscle is well developed, but does not enter the free portion of either

ans

ans

FIGURE 16.—Globicephala melaena, nasal diverticula: a, dorsal view of nasofrontal sacs and

associated structures; b, dorsal view of the angle of the right nasofrontal sac, medial portion of

the dorsal wall of the sac reflected to show the internal trabeculae; c, dorsal view of the

posterior portion of the left nasofrontal sac, dorsal wall removed to show the internal partitioning of this portion of the sac; d, posterodorsal view of the right nasofrontal sac and associated diverticula. (ans = angle of nasofrontal sac, as = accessory sac, bhl = blowhole ligament,

dmm = diagonal membrane muscle, fb = yellow fat body, im = intrinsic muscle of nasofrontal

sac, iv = inferior vestibule, us = nasofrontal sac, sc = spiracular cavity, v = vertex.)
26

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

membrane. The intrinsic musculature of the nasofrontal sacs is also well developed but, aside from

entering the trabeculae of the angle of the right

sac, offers nothing apart from the usual delphinid

condition.

The rostral muscles in G. melaena are sharply

differentiated into lateral and medial portions.

They are not unusually large, particularly in relation to the size of the melon, and are not as large

relative to the size of the rostrum as in Grampus.

OTHER STRUCTURES.—The melon in G. melaena

is larger than that of any other delphinid examined. It extends dorsally to a level above the vertex,

and anteriorly about three quarters of the length

of the rostrum (Figures 18, 24). External to the

melon is a layer of fatty tissue containing numerous

large connective tissue bundles, similar to the condition seen in Pseudorca crassidens. Some of these

appear to be derived from the rostral muscle, others

from the dermis. There is an area of extremely

dense connective tissue in the dermis just anterior

to the blowhole, as noticed in Lagenorhynchus

albirostris.

The melon does not pervade the nasal plug

muscle as much as it does in the other delphinids.

The dorsal surface of the nasal plug mass was

uniformly muscular, with no sign of the asymmetrical invasion of the melon usually seen on the

right side. Cephalorhynchus is the only other

delphinid in which this is known to be the case.

As is generally known, there is sexual dimorphism in the shape of the head in Globicephala

(Figure 19), with the mass of forehead tissue in

adult males being larger and projecting farther

anterodorsally than in females. As I was only able

to examine an adult male, I was unable to determine whether or not this was reflected in the

internal structure of this area. I would expect that,

as was the case in Pseudorca, this dimorphism is

limited to an expansion of the fatty connective

tissue of the dermis and does not involve the melon.

So far as I have been able to determine, Pseudorca

and Globicephala are the only delphinids showing

sexual dimorphism in the facial region.

STENINAE

Steno

MATERIALS.—A young male Steno bredanensis

was dissected. Additional information on this species is available from Purves (1967).

sc

P'

FIGURE 17.—Globicephala melaena, dissections of nasal musculature: «, superficial musculature,

oblique postcrodorsal view; b, deep dissection, fasciculi of pi on its posteromedial surface

dorsal view. (ae = pars anteroexternus, fb = fat body, i = pa rs intermedius, pe = pars posteroexternus, pi = pars posterointernus, sc = spiracular cavity, v = vertex.)
NUMBER 207 27

a

NASAL PASSAGE AND DIVERTICULA.—There was a

small sacculation on the anterior end of the right

premaxillary sac in the specimen when I dissected,

but none on the left. This was not mentioned in

Purves' (1967) account, and I suspect that it was a

developmental anomoly. Otherwise the premaxillary sacs present no unusual features.

The accessory sacs were similar to those of most

of the other delphinids, the right being about 2.4

cm long by 1 cm wide, while the left was only

about half that size. In both the text and his

a

m

FIGURE 18.—Globicephala melaena, sections of rostral structures: a, oblique view of transverse section 20 cm posterior

to tip of rostrum; b, sagittal sections; c, parasagittal section,

10 cm lateral to above section. (bv = blood vessels, dct =

dermal connective tissue, m = melon, npm = nasal plug muscle, rm = rostral muscle).

FIGURE 19.—Globicephala melaena, lateral views of the external appearance of the heads, showing the degree of sexual

dimorphism in external head shape: a, female; b, male.
28

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

figures, Purves (1967) indicated that the accessory

sacs formed a communication between the premaxillary and nasofrontal sacs. There has been

consistent confusion in the literature over the relationship of these diverticula, and this mistake

apparently derives from a misunderstanding of the

descriptions of Lawrence and Schevill (1956).

The nasofrontal sacs are similar to those of

Tursiops, although the angles of both sacs were

more lobulated in Steno, reminiscent of the condition seen in Globicephala melaena, though not

nearly as well developed as in that species. The

lobulations of the nasofrontal sac were slightly

trabeculate when opened, and a few muscle fibers

were seen in the larger trabeculae.

The vestibular sacs were subequal, the right

being slightly larger than the left, and were somewhat smaller than in most delphinids. There were

no indications of anterior lobes on either of the

vestibular sacs.

MUSCULATURE.—The nasal musculature of S.

bredanensis is quite similar to that of Tursiops,

with only a few minor differences seen in the single

specimen examined. Pe was very thin and difficult

to define, and there was no trace of i. Both of

these, however, are variable in other delphinids.

The rest of the nasal musculature presented no

differences from the condition seen in Tursiops.

Purves (1967) illustrated the nasal musculature,

but did not describe it in any detail. However, his

illustrations are in agreement with my dissections.

OTHER STRUCTURES.—The melon was similar in

development to that of Tursiops, and, as in most

of the delphinids, entered asymmterically into the

right nasal plug. Purves (1967) described an intrinsic muscle of the premaxillary sac, which I was

unable to separate from the nasal plug muscle.

The diagonal membrane was similar to that of

other delphinids, with a moderately developed

diagonal membrane muscle which did not appear

to enter the free portion of the membrane. The

deep structures associated with the blowhole ligament were similar to those of Tursiops.

Sotalia

Schenkkan (1972, figs. 1, 2) illustrated the nasal

diverticula in Sotalia guianensis, and later (Schenkkan, 1973) gave a brief decription of the facial

anatomy of this species. The following discussion

is based primarily upon his illustrations in the

earlier paper.

NASAL PASSAGE AND DIVERTICULA.TIIC degree of

asymmetry seen in the premaxillary sacs as shown

in Schenkkan's (1972) figure is comparable to that

of Grampus, and is greater than that seen in other

delphinids. The accessory sacs are moderately

developed and situated similar to those of other

delphinids, as are the nasofrontal sacs. The vestibular sacs, as shown in the earlier paper, are remarkably large, particularly the right sac, which appears

to be between two and three times as large as the

left. However, in a later paper (Schenkkan, 1973)

they are shown as much smaller and nearly

symmetrical.

Schenkkan's (1972, fig. 2) mesial view of the nasal

diverticula of the right side shows a peculiarity not

seen in any other odontocete. This illustration

clearly shows a passage originating from the posterolateral edge of the premaxillary sac, just anterior to the accessory sac, and running dorsally to

connect with the medial side of the vestibular sac.

Unfortunately the text of this paper contains no

reference to the nasal diverticula of this species, no

information on this structure is given in the labeling of the figure, and the brief description in his

later paper (Schenkkan, 1973) contains no information on this structure, so one is at a loss to interpret its significance.

MUSCULATURE.—Schenkkan's (1973) comment that

the nasal musculature in Sotalia guianensis "was

comparable with the situation found in Delphinus

delphis" does not provide a basis for comparison,

but gives no reason to believe that it is any different from the situation seen in Steno.

OTHER STRUCTURES.—No data are available for

other features of the facial anatomy of Sotalia.

CEPHALORHYNCHINAE

Cephalorhynchus

MATERIALS.—A young male (110 cm) Cephalorhynchus hectori was dissected. Schenkkan (1973)

described a dissection of another male (118 cm) of

the same species.

NASAL PASSAGE AND DIVERTICULA.—The premaxillary sacs were relatively short as compared to

Tursiops. The dorsomedial wall of the left premaxillary sac was produced into a saccular fold,
NUMBER 207 29

which may have been an individual abnormality,

as Schenkkan (1973) noted nothing unusual in this

area on his specimen.

The diagonal membranes were small and about

the same size on both sides. The accessory sacs, as

noted by Schenkkan (1973), were relatively large,

with the right sac approximately twice the size of

the left (2.6 cm long as opposed to 1.4 cm on the

left). There was a small posterior branch of the

blowhole ligament passing dorsal to the accessory

sacs on both sides.

The anterior portions of the nasofrontal sacs

were well developed and were unique among delphinids in that the left sac was much larger than

the right. Approximately half of the anterior portion of the left nasofrontal sac extended across the

midline, where it was partly overlain by the right.

In their relaxed condition in this frozen specimen,

the left sac appeared to occupy about twice the

area of the right. The angles of both sacs were

faintly sacculated, reminiscent of the situation

seen in many other delphinids and found in Globicephala melaena to an extreme degree. Schenkkan

(1973) also noted the reverse asymmetry of the

anterior portions of the nasofrontal sacs.

The vestibular sacs were superficially symmetrical and not unusual in size. They lay posterior to

the blowhole, similar to the condition seen in

Orcinus. There walls were heavily wrinkled, indicating considerable distensibility, as in other delphinids. There was a pronounced anterior lobe

of the vestibular sac on the left and a somewhat

smaller one on the right. The left anterior lobe

entered the main portion of the vestibular sacs

through a slit just dorsal to the anterior fold,

while the right appeared to be an extension of the

anterior fold itself. A small, shallow fold just

dorsal to the right anterior fold may be the actual

homologue of the left anterior lobe of the vestibular sac. Schenkkan (1973) did not note these lobes

of the vestibular sacs in his specimen. A similar,

though much less pronounced, situation was seen

in Tursiops and some of the Stenella, where there

was a slight development of an anterior lobe on

the left.

MUSCULATURE.—In general the musculature was

similar to that of other delphinids. There was a

well-developed pe, but no indication of i on either

side. The portion of ae overlying the vestibular

sacs was thinner than in Tursiops or Stenella, but

was otherwise similar. The intrinsic musculature

of the nasofrontal sacs gave more appearance of

being continuous with the nasal plug muscle than

it did in Tursiops or Stenella.

The diagonal membrane muscle was difficult to

define, but appeared to enter the membrane to a

slight extent. The lateral and medial rostral muscles differed in fiber orientation more than in

Tursiops or Stenella.

OTHER STRUCTURES.—The melon was of moderate

size, and was unusual in not extending into the

right nasal plug as in most delphinids. The nasal

plugs were remarkably asymmetrical, the lateral

lip of the right nasal plug being twice as wide

(6 mm) as the left (3 mm).

Schenkkan (1973) described a "small bulbous,

translucent structure (diameter about y4 cm) consisting of a tough, unstructurated gelatinous substance" between the medial terminations of the

caudal portions of the nasofrontal sacs. I found no

trace of such a structure and suppose that this was

an individual abnormality, possibly a parasitic

cyst, such as the cestode cysts sometimes encountered in small odontocetes.

LISSODELPHINAE

Lissodelphis

Schenkkan (1973) provided a description of the

facial anatomy of Lissodelphis borealis, upon which

the following discussion is based.

NASAL PASSAGE AND DIVERTICULA.—The premaxillary sacs were relatively small, but presented no

notable peculiarities. The accessory sacs were well

developed and the right sac had a posteriorly

directed extension. The nasofrontal sacs were illustrated as being substantially larger than in Tursiops, and the angles of the nasofrontal sacs were

sacculated, though it is not clear to what extent.

The vestibular sacs appear to be relatively larger

than in any of the other delphinids, and are situated posterior to the blowhole. Schenkkan's (1974)

observation that the nasal passages were displaced

caudally as a result of extensive development of

the melon is difficult to visualize, and is not supported by his illustrations.

MUSCULATURE.—Schenkkan (1973) commented

that "Due to the caudad displacement of the nasal

passage, the direction of all muscle fibers was
30

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

nearly vertical and separation into various layers

was therefore fairly difficult." If this is in fact the

case, it seems very different from the other

delphinids.

OTHER STRUCTURES.—Schenkkan (1973) stated

that the melon was relatively large in L. borealis,

though this is difficult to imagine when considering

the external shape of the head.

PHOCOENIDAE

Phocoena, Phocoenoides, Neophocaena

The members of the family Phocoenidae present

a number of consistent differences from the Delphinidae, and appear to constitute a very distinct

group on the basis of facial anatomy. The nasal

apparatus of Phocoena phocoena has been described

more frequently than that of any other cetacean

(von Baer, 1826; Sibson, 1848; Rawitz, 1900; Gruhl,

1911; Moris, 1969; Schenkkan, 1973). Howell (1927)

gave a brief description of the nasal complex in

Neophocaena, and Ridgway (1966) described the

vestibular sacs in Phocoenoides dalli. Yet it still

remains to be described in detail as a functional

system. I do not intend to do so at this point, but

rather to present a brief description for comparison with the delphinid nasal system. This is based

upon the extensive literature listed above and upon

my own limited dissections of Phocoena and

Phocoenoides.

MATERIALS.—One adult of Phocoena phocoena

and one of Phocoenoides dalli were dissected.

NASAL PASSAGE AND DIVERTICULA.—The premaxillary sac is relatively small in the phocoenids, as

indicated both by my dissections and the literature

accounts. The prenasal area of the skull differs

markedly from that of the delphinids, in the presence of a strong premaxillary emminence, upon

which the premaxillary sac lies.

Schenkkan (1971) found that the accessory sac

was small or lacking in the specimens of Phocoena

phocoena which he examined. This sac had not

been reported in the earlier literature, and I was

able to find only a very small one on the right side

in Phocoenoides dalli.

The deep portions of the phocoenid nasal apparatus are more complicated than those of the

delphinids, and warrant much more study.

The nasofrontal sacs are large in the phocoenids

(Gruhl, 1911; Gallardo, 1913; Howell, 1927; Schenkkan, 1973) and are situated as in the delphinids. I

found the anterior portion of the nasofrontal sac

in Phocoenoides dalli to be lined with a thick,

nonpigmented, trabeculate epithelium. This had a

glandular appearance, but has not been examined

histologically. The illustrations of Gruhl (1911)

and Moris (1969) suggest that this condition is also

present in Phocoena phocoena.

The posterior portion of the deep nasal apparatus is complicated by a diverticulum which arises

from the inferior vestibule and passes dorsally,

posterior to the nasofrontal sac. This is the "hintere

hohle" of Gruhl (1911), the "sac nasal posterieur"

of Moris (1969), and the "hinter unter hohle" of

von Baer (1826). Schenkkan (1973) refers to this

diverticulum as part of the nasofrontal sac, but

does not describe it in detail.

The most striking feature of the phocoenid nasal

apparatus is the large vestibular sac, which has

been thoroughly described in the literature cited

above. This diverticulum is on the order of twice

the size of those seen in the delphinids. The ventral wall is thrown into a series of folds, 0.5 to 1.0

cm wide, aligned perpendicular to the long axis of

the body. The walls of these folds are composed

of a thick layer of connective tissue, fixing them in

place and precluding distension of the ventral wall.

The middle fold of this series is the deepest, clearly

dividing the ventral wall into two halves. This

fold also appears to form the principal communication with the nasal passage. The vestibular sac

is completely enclosed by an intrinsic muscle, and

is free to move within the layers of the pars anteroexternus. This situation appears to be common to

all three of the phocoenid genera, and is not

aproached by any other cetacean.

MUSCULATURE.—The nasal musculature of phocoenids is somewhat different from that of

delphinids when examined in detail, yet is still

arranged according to the same general plan. The

pars posteroexternus appeared to be absent in my

dissections. Gruhl's (1911) account of this musculature indicated a similar condition in Phocoena

phocoena. The pars anteroexternus is arranged in

essentially the same manner as in the delphinids.

Within this layer, however, a very distinct difference is seen in the structure of the vestibular sac,

as described above. The fibers of the musculature

of the vestibular sac are oriented perpendicular to
NUMBER 207 31

those of ae. The muscle of the vestibular sac is

attached to the maxilla anteriorly, above the surface of the vestibular sac, becoming tendinous on

the ventromedial portion of the sac. I have been

unable to confirm this in Gruhl's (1911) account,

but the illustrations of Gallardo (1913) suggest

that this holds for Phocoena dioptrica. Howell's

account of Neophocaena (1927) indicates a similar

condition in that genus.

Beneath the level of the vestibular sac, the muscular arrangement is similar to the delphinids. The

general impression, however, is that the deeper

muscles are relatively smaller in the phocoenids.

Unfortunately, I was unable to determine the

arrangement of the deep musculature around the

vertex (intrinsic muscle, diagonal membrane muscle) in my dissections, and there is no information

available from the literature.

MONODONTIDAE

Monodon

Huber (1934) described the facial structures in

a large fetal narwhal (Monodon monoceros) in

sufficient detail to allow comparison with the

delphinids.

NASAL PASSAGE AND DIVERTICULA.—It is in the

nasal passage itself (rather, the spiracular cavity)

that Monodon appears to be most specialized.

Instead of the slitlike passageway seen in delphinids and phocoenids, Monodon has a large, spherical cavity. The blowhole opens directly into this

cavity on its dorsal surface, and the nasal plugs

open from its ventral surface.

Unfortunately, Huber's description was published posthumously, and Howell, who edited it,

expressed some doubt as to the exact relationship

of the apertures of the diverticula to the spiracular

cavity. It appears that the vestibular sac ("lateral

sac") opens laterally from this cavity. Huber's figures indicate a complicated nasofrontal sac, opening both into the inferior vestibule and into the

spiracular cavity dorsal to the nasal plugs. He also

indicates that the anterior portion of the nasofrontal sac opens into the spiracular cavity, just

ventral to the opening of the vestibular sac. Schenkkan (1973) found similarities between Huber's

descriptions of Monodon and his own dissections

of Phocoena. The degree of complexity of the

nasofrontal sac is similar, but more definite comparisons require clarification of some of the

uncertainties in Huber's description. There is no

indication of an accessory sac.

Scoresby (1823), in his brief description of the

nasal passages of the narwhal, illustrated the

vestibular sacs, but did not menton any other

diverticula.

MUSCULATURE.—Huber (1934) concluded, based

upon a comparison with Tursiops, that the nasal

musculature of Monodon was derived from the

same general plan as that of the delphinids, but

differed in detail. The differences appear to be

largely due to the extreme modification of the

structures with which the musculature is associated.

Although Huber did not attempt to define separate layers of the nasal musculature, examination

of his illustrations suggest that the same layers as

in Tursiops can probably be recognized.

The most superficial of these layers of musculature appears to correspond to the pars posteroexternus, but has its origin much more posteromedially than in the delphinids. The configuration

of the remaining nasal musculature is more similar

to that of the delphinids, at least in terms of origin

and general area of insertion. None of Huber's

illustrations show the details of insertion of pi or

ai, both of which must differ from the delphinid

condition as a result of the modifications in the

spiracular cavity of Monodon.

Huber's (1934) illustrations give the impression

that the nasal plug muscle ("retractor muscle") is

continuous with musculature originating from the

maxilla to the spiracular cavity (at?). The nasal

plugs seem to have a lateral lip, as in delphinids.

OTHER STRUCTURES.—Due to the expansion of the

spiracular cavity and the unusual condition of the

nasal plug muscle, the relationship of the melon

to the nasal plugs must be very different from what

is seen in the delphinids. The melon, as indicated

by the illustration of Raven and Gregory (1933),

is quite large. All told, Monodon is a very unusual

animal, and certainly warrants detailed investigation.

Delphinapterus

The nasal apparatus of Delphinapterus leucas

was briefly described by Watson and Young (1879).

Their specimen, unfortunately, was in an advanced
32

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

state of decomposition, and the description suffered

accordingly. A more detailed description has been

given by Kleinenberg, et al. (1969) in their monograph on this species.

NASAL PASSAGE AND DIVERTICULA.—Watson and

Young (1879) were only able to find one pair of

nasal diverticula, the premaxillary sacs, which were

relatively small. They were familiar with the work

of Murie (1870, 1871, 1873) and appear to have

spent some time trying to locate all of the delphinid

diverticula. The illustration given of the spiracular

cavity gives the impression that it is large, as in

Monodon, but no mention of this was made in the

text. The muscles were unsuitable for dissection.

One interesting finding was the presence of numerous openings in the walls of the spiracular

cavity, which they took to be glandular orifices.

Unfortunately, the condition of their specimen

renders this suspect.

Kleinenberg, et al. (1969) described the system

of nasal diverticula in D. leucas in more detail.

The vestibular sacs, premaxillary sacs, and nasofrontal sacs are similar to those of delphinids. In

addition to these, there is a posterior extension of

the inferior vestibule, along the posterodorsal

aspect of the nasofrontal sacs, reminiscent of the

condition seen in Phocoena. These diverticula

were termed the accessory cavities of the nasofrontal

sacs by Kleinenberg, et al. (1969). No accessory sacs

proper were found. In most respects, their description indicates a greater similarity to the delphinid

condition than is seen in Monodon. In their figure

51, however, which illustrates the possible action

of the diverticula during ventilation, they show a

large spiracular cavity immediately dorsal to the

nasal plugs. This would correspond to the expansion of the spiracular cavity described in Monodon.

The other figures of Kleinenberg, et al. do not,

however, support this idea. No mention is made of

any glandular structures similar to those described

by Watson and Young (1870), nor are the diverticula described as being asymmetrical.

MUSCULATURE.—No data is available on the musculature of D. leucas.

OTHER STRUCTURES.—The melon in D. leucas

appears to be quite large, judging from the external appearance of the head, but no descriptions of

its structure are available.

PLATANISTIDAE

Platanista

The anatomy of the nasal complex in this interesting cetacean was briefly described by Anderson

(1878), and has been more recently covered in

detail by Purves and Pilleri (1973). The blowhole

of Platanista is unusual in being a longitudinal slit

instead of the transverse crescent seen in the delphinids. The mechanics of such a structure are

very different from those of the delphinid nose, and

the anatomy differs accordingly. There are no

vestibular sacs, a condition otherwise seen only in

Hyperoodon (Schenkkan, 1973; Purves and Pilleri,

1973) (excluding the Physeteridae in which structural homologies are unclear). The "maxillary"

sacs described by Anderson (1878) are not homologous to the maxillary sacs ( = vestibular sacs) of

Murie (1870), but to one of the deeper diverticula.

The nasofrontal sacs in Platanista are grossly similar in form to those of delphinids, but differ

markedly in that the distal portion (comparable

to the anterior portion of delphinids) extends dorsally rather than anteriorly. Purves and Piller

(1973) described an additional diverticulum originating from the area of the inferior vestibule

(which appears to be reduced in Platanista) and

lying posterodorsal to the nasofrontal sacs. They

treated it as a branch of the nasofrontal sac and

did not assign it a separate name. Although the

relationship is far from clear, this condition seems

comparable to that seen in Phocoena, where there

also was a diverticulum lying posterodorsal to the

nasofrontal sacs. The accessory sacs are absent and

the premaxillary sacs are relatively small.

The most striking features of the facial region in

Platanista are the extensive maxillary crests. Purves

and Pilleri (1973) described these in detail and

demonstrated that they contain an extensive system

of air cavities derived from the pterygoid air sinus

system. In this respect Platanista is remarkably

different from any other cetacean.

The nasal musculature is quite different from

that of the delphinids, as necessitated by the

extreme modification of the other facial structures,

making comparison with that group difficult and

beyond the scope of this paper.

Purves and Pilleri (1973) described the topographic homologue of the melon as a dense mass
NUMBER 207 33

of fibrous tissue. This seems quite different from

the condition seen in other odontocetes. However,

they ascribe a similar condition to Inia and Pontoporia, both of which I have examined and found

to have considerable fatty differentiation in this

area. I suspect the differences are partly due to

their using formalin fixed material, in which the

connective tissue becomes more conspicuous, partly

to actual difference in relative amount of fat and

connective tissue, and partly to semantic differences

in usage of descriptive terms.

The nasal plugs lack a lateral lip, as seems to be

the general situation in the platanistids. An item

of some interest is Anderson's (1878) mention of a

glandular recess around the ventral portion of the

nasofrontal sac. I have seen such a structure in

Inia, which may well be homologous to the glandular structures described by Evans and Maderson

(1973) in Tursiops.

Lipotes

The anatomy of the nasal region in the Chinese

river dolphin, Lipotes velixifer, has been very

briefly commented upon by Hinton and Pycraft

(1922) and Hinton (1936). The blowhole is peculiar

in being a longitudinal rectangular opening. In the

lateral margins of the blowhole are two small bones,

one on either side. Various slips of musculature are

attached to these, and Hinton and Pycraft (1922)

felt that the bones were instrumental in effecting

blowhole closure. Hinton (1936) mentions that

they also occur in Pontoporia, the La Plata river

dolphin, though Schenkkan (1972) does not mention them in his description of this species, and I

did not find them in the fetus which I dissected.

Hinton and Pycraft (1922) described two pairs of

superficial diverticula, an anterior one dorsal to

the bones, and a posterior one ventral to them.

The posterior one is of considerable extent on the

right side, covering the whole of the "dilator

naris," while that of the left side is concealed

beneath the small bone. Both of these diverticula

are at the level of the vestibular sac, and one of

them (probably the posterior) is homologous to it.

Hinton (1936) said that the same configuration of

diverticula was found in Pontoporia, but that the

degree of asymmetry was less. None of the other

facial structures were described in the above works.

Pontoporia

Burmeister (1867) briefly described parts of the

nasal system in Pontoporia blainvillei, while more

recently, Schenkkan (1972) described the nasal

complex in some detail. The discussion of this

species is primarily based on the latter work. In

addition, I have made a preliminary dissection of

a near-term fetus of this species, confirming much

of Schenkkan's description.

As opposed to the two preceding genera, the

blowhole is a crescentic slit, as in delphinids. The

deeper nasal diverticula in this species, as apparently in all of the platanistids, are relatively small.

The premaxillary sacs are comparable to those of

delphinids, differing primarily in size, while the

accessory sacs are absent. A small caudal portion

of the nasofrontal sac is present, but the anterior

portion is missing. The vestibular sacs, in striking

contrast to the other diverticula, are extremely

large and complex, covering much of the dorsal

and lateral surface of the facial region. As in most

of the delphinids, the right vestibular sac was larger

than the left, though to a much greater degree.

The nasal musculature appears to be more comparable to delphinids than that of Platanista, but

detailed comparisons remain to be made. The

melon is moderately developed and situated similar

to that of delphinids. Schenkkan (1973) indicated

that the nasal plugs were relatively simple, without

lateral lips.

Inia

I have made some preliminary dissections of the

facial region of Inia geoffrensis, which are of use

in comparing it to the other river dolphins. The

blowhole is of the type normally seen in delphinids,

crescentic with the concavity facing anteriorly.

There were no bony elements in the margins of

the blowhole, nor did I find two pairs of superficial

diverticula. The vestibular sac is extremely large,

much more so on the right, and covers the whole

of the posterolateral portion of the nasal musculature. The nasofrontal sacs are moderately developed and, as in Platanista, are associated with a

glandular structure, the exact nature of which has

yet to be determined. The anterior portions of the

nasofrontal sacs are lacking, the posterior portion

extending to a point just lateral to the nasal pass-
34

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

age. The accessory sacs are well developed, and

situated as in delphinids. I have not attempted to

work out the pattern of the musculature in Inia,

which appears to be very different from that of the

delphinids. The melon is well developed, though

it appears to contain a greater amount of connective tissue than any of the delphinids examined.

Summary of Descriptive Anatomy

NASAL PASSAGE AND DIVERTICULA

DELPHINIDAE.—This is the most variable portion

of the delphinid nasal complex. Of the delphinines,

the group comprised of the genera Tursiops, Stenella, and Delphinus appears to represent the most

generalized condition and the included forms show

few differences among themselves.

Lagenorhynchus albirostris differs from this group

of genera in the extreme expansion of the nasofrontal sacs and the development of a lateral diverticulum from the right premaxillary sacs. Lagenodelphis is similar to Lagenorhynchus albirostris in

having a lateral diverticulum from the premaxillary sac, but does not show any expansion of the

nasofrontal sacs.

Grampus is also distinctive in the morphology

of its nasofrontal sacs. The anterior portion is

absent on the left side and is greatly enlarged on

the right.

Of the orcinines, only Globicephala shows any

notable modifications of the diverticula. Again, it

is the nasofrontal sac which is specialized, having

an unusual trabeculate sacculation on the angle of

the right sac.

The Steninae and the Lissodelphinae show no

outstanding modifications of the nasal diverticula,

while the only member of the Cephalorhynchinae

examined, Cephalorhynchus hectori, shows a striking enlargement of the anterior portions of the

nasofrontal sacs, and is further unusual in that the

left sac is larger than the right.

The vestibular, accessory, and premaxillary sacs

are relatively conservative in the delphinids, the

nasofrontal sac being the most variable portion of

the system.

OTHER FAMILIES.—The nasal diverticula are extremely variable in the other odontocete families.

The vestibular sacs in the phocoenids have rigid,

heavily folded ventral walls. In some of the platanistids these sacs are extremely large, covering most

of the posterior facial region. They appear to be

relatively small in the monodontids.

The nasofrontal sacs of the phocoenids are more

complicated than those of the delphinids, and possess a trabeculate anterior portion. The posterior

portion is also more complicated, with an additional diverticulum arising from the inferior vestibule and lying posterior to the nasofrontal sac. In

the monodontids, the nasofrontal sacs are relatively complex, and are in some ways reminiscent

of those of the phocoenids. These diverticula are

relatively small in the platanistids, most of whom

appear to lack an anterior portion. They are somewhat more complicated in Platanista, which has a

diverticulum lying posterodorsal to the nasofrontal

sacs, somewhat similar to the condition seen in

phocoenids.

MUSCULATURE

DELPHINIDAE.—Within the delphinids the nasal

musculature is relatively conservative. Pe and i are

the most variable elements, the former being particularly so in the Orcininae. The deeper portions

of the musculature are more constant.

OTHER FAMILIES.—Outside of the Delphinidae,

this portion of the anatomy shows considerable

variation. The phocoenids are probably closest to

the delphinid pattern, differing mainly in the

arrangement of the superficial portions of the musculature. The reverse seems to be true in Monodon,

where the deep musculature is most divergent from

the delphinid pattern. None of the other odontocetes have been examined in sufficient detail to

draw comparisons.

MELON

DELPHINIDAE.—In most of the delphinines, the

melon is relatively small. In Grampus, however, it

becomes quite large, but without the proliferation

of dermal connective tissue seen in some other

delphinids.

In the orcinines this structure is more variable.

In Orcinus and Pseudorca it is relatively small. In

the latter, however, the dermal connective tissue
NUMBER 207 35

superficial to the melon has become thick, giving a

bulbous appearance to the forehead, particularly

in the male. In Globicephala both the melon and

the connective tissue have hypertrophied, again,

more so in the male than in the female. The

bulbous-headed genera Grampus, Pseudorca, and

Globicephala are compared in more detail in a

later section.

OTHER FAMILIES.—In the phocoenids the melon

is relatively small, with the possible exception of

Neophocaena, which has a bulbous forehead. In

the monodontids the melon is relatively large,

apparently without a thickening of the dermal

connective tissue. The melon in the platanistids is

relatively small.

OTHER STRUCTURES

The rest of the nasal complex shows little variation in the delphinidae. The platanistids stand out

as an unusual group in many ways, one of the

more important of which may be the lack of lateral lips on the nasal plugs in this group. Glandular structures are apparently present in all of the

families, but are not well enough known to permit

general comparisons.

FUNCTION OF THE FACIAL COMPLEX

Introduction

The facial complex is potentially involved in a

variety of functions. This complex has differentiated

around the external nasal passages, and most of

its possible functions involve movement of air in

these passages. The functions can be broken down

into two general categories, those associated with

respiration and those associated with sound production. Respiratory functions are of undoubted

importance, but do not account for the degree of

morphologic specialization seen in this area, suggesting that sound production may be of considerable importance in this region. In this context

sound production is meant to include not only the

generation of acoustic energy, but also modification

of that energy, such as modulation, reflection, and

refraction.

In this chapter the possible roles of the facial

structures in respiration are considered first. The

facial structures are discussed in the same order as

in the descriptive section, and the possible function of each element is considered separately. Following this, the questions of sound production are

considered in detail, with a review of the literature

pertinent to this problem. In the next section of

this chapter, the functional significance of cranial

asymmetry is gone into in a similar manner. Finally, a summary section is given, presenting the

most likely of the functions in which this region is

involved.

Respiratory Considerations

One of the general functions proposed for the

elaborate nasal apparatus of odontocetes has been

the exclusion of water. While this is of undoubted

importance to a diving animal, I believe that it

has been overemphasized with respect to odontocetes. It has been commonly thought that the

deeper an animal dives, the greater will be the

tendency for water to enter the nares or for air to

be lost. This would only be the case if a pressure

differential existed at the point of closure of the

nasal system. In general, it can be assumed that

the air within the respiratory system of a diving

animal will be compressed by collapse of the lungs,

thus equalizing the internal and external pressures

upon the system. A problem exists only if the air

available in the collapsible portions of the respiratory system is not sufficient to raise the pressure

within the noncollapsible portions of the system to

a level equal to that of the external pressure. It

has been suggested that this is compensated for in

cetaceans by expansion of vascular tissues into the

rigid air spaces (e.g., the middle ear), thus reducing

their volume and equalizing the pressure. In any

event, this is only a problem in structures deep to

the fleshy nasal passages, as this sort of pressure

differential would tend to force the nasal plugs

more firmly into the bony nares, effectively tightening the seal. Pinnipeds, with relatively simple

nasal passages, have been reported to dive to depths
SMITHSONIAN CONTR1BU I IONS TO ZOOLOGY

of 600 meters (Kooyman and Anderson, 1969), substantiating the idea that deep-diving does not

demand an extremely specialized nasal apparatus.

A different sort of question involving the entry

of water into the nasal passages has also been

raised. This is the possibility of water entering the

passages during breathing. Cuvier (1797) thought

that the diverticula in the delphinid nose served as

traps to prevent inspiration of water. Lawrence

and Schevill (1956) noted that water frequently

entered the vestibular sac if the animal started to

submerge with the blowhole partially open. This

appeared to present no problems to the animal, and

the water was expelled in the next breathing cycle.

They also noted that one of their experimental

subjects experienced no difficulty if the blowhole

was manually forced open underwater. Consequently they suggested that the vestibular sacs

function as a water trap. This would, however, be

effective only if the nasal plugs were seated and

water penetrated no farther than the spiracular

cavity. If, however, the vestibular sacs were absent,

water would merely be forced out by closure of the

nasal passage. Thus, although the vestibular sacs

will hold water, this ability seems to be merely a

consequence of their presence and does not provide

any particular advantage to the animal.

Lawrence and Schevill (1956) were of the opinion that there is no mechanism for removing water

once it got into the deeper portion of the respiratory system. The normal respiratory cycle of these

animals, however, is sufficiently rapid that every

expiration is essentially a cough, and should be

sufficient to clear small amounts of water from the

passages. Tomilin (1967) described a series of

experiments in which water was introduced into

the respiratory passages of dolphins, sometimes in

considerable quantity. This seemed to present no

problem to the animals and was expelled in subsequent expirations.

Schenkkan (1973) suggested that the vestibular

sacs were filled with air from the nasofrontal sacs

immediately before surfacing to breathe, and that

this provides a "pneumatic cushion beneath the

superficial fascia of the vestibular sections of the

m. maxillonasalis, facilitating the rapid opening

of the blowhole. . . ." It is not clear how this would

facilitate opening of the blowhole, nor is it evident

that it actually occurs. Blockage of the entrance of

water to the nasal passage by the initial outflow

of air from the vestibular sacs, as suggested by

Schenkkan (1973), would seem to be of negligible

importance when compared to the outflow of

respiratory air from the lungs. Water may, in fact,

enter the vestibular sacs, but it is difficult to see

how the "small particles enclosed in the epithelial

lining of the vestibular sacs in some species" relates

to this question. Much of Schenkkan's material was

derived from stranded animals, as was mine, in

which it is not uncommon to find sand and detritus

as far back in the respiratory tract as the terminal

bronchioles, either washed in post mortem, or, in

the more extreme cases, inspired when the animals

were thrashing about in the surf.

The observation that "in general a living dolphin

seems to be unable to open its blowhole unless the

vestibular sacs have been previously expanded" is

apparently based upon a misunderstanding of the

observation by Anderson (in Purves, 1967) on a

dead Phocoena. Schenkkan (1973) interpreted the

statement to mean that "when the air was expressed

from the (vestibular) sacs of a specimen, it died in

a motionless condition as the head and indeed the

entire animal sank beneath the surface." The statement in Purves (1967) is as follows: "Recently dead

animals have been observed to sink below the surface when the vestibular sacs have been punctured."

This observation does relate to Purves' (1967) discussion of the vestibular sac as a buoyancy regulator, but not to Schekkan's (1973) speculations.

Thus, the complexity of the odontocete nose

cannot be accounted for by the obvious demands

of an aquatic existence. Movement of air during

sound production, however, may require particularly tight closure of the nasal passages. It may also

be advantageous to be able to control the passages

at different level, isolating some of the diverticula.

The layered structure of the nasal musculature

supports such an idea.

Nasal Passage and Diverticula

A great variety of suggestions have arisen for the

functioning of the nasal diverticula. It was first

suggested (Ray, 1671) that they were part of the

olfactory system, later (Sibson, 1848) that they were

filled with air to maintain the head of the animal

near the surface while it was sleeping. The olfactory hypothesis has long been abandoned in view

of the lack of olfactory innervation in these ani-
NUMBER 207 37

mals. The idea of buoyancy regulation by the

diverticula appears in a number of later papers

(e.g., Purves, 1967), but has not been demonstrated

experimentally.

Norris (1964) suggested that the vestibular sacs

serve as reflective elements, directing sound emitted

from the region of the external bony nares anteriorly. If these sacs are air-filled during vocalization,

then they would certainly be effective reflectors of

sound energy. Their situation with respect to the

surrounding muscles allows them to expand primarily in a horizontal plane, increasing their reflective surface. As these sacs are capable of distension,

the area of reflective surface could be modified, thus

altering the shape of the emitted sound field. The

variation in morphology of these diverticula suggests that there may be considerable variation in

the shape of the sound field between different

species.

The anterior folds, as pointed out by Lawrence

and Schevill (1956), provide a tight closure of the

nasal passage at the level of the vestibular sacs.

Lawrence and Schevill (1956) proposed that the

nasofrontal sacs formed a pneumatic seal around

the nasal passage. This certainly appears to be the

mechanism functioning to produce closure of the

nasal passage in a dead animal when air is introduced into the nasal system through the larynx,

not action of the lateral lips of the nasal plugs as

stated by Schenkkan (1973). While this is a possible function for the nasofrontal sacs, it is also

possible to achieve the same end with the two large

muscle masses, pi and ai, which encircle the passage at this level. In Grampus the anterior portion

of the left nasofrontal sac is absent, precluding

pneumatic closure of that side. In Lagenorhynchus

the nasofrontal sacs have been greatly enlarged,

beyond what would seem to be useful for pneumatic closure. These modifications suggest a role in

addition to or other than closure of the nasal

passage.

At the moment, however, it is difficult to assign

a primary function to these sacs. Certainly any

cavities connected with the nasal passage can serve

as reservoirs for recycling of air during phonation.

If they contain air, they are going to be effective

reflectors of sound. The large nasofrontal sacs of

some species suggest that one of these functions

might be relatively important.

The accessory sacs are more of a puzzle than are

the nasofrontal sacs. Lawrence and Schevill (1956)

proposed that they served to conduct air from the

posterolateral edge of the premaxillary sacs into the

nasofrontal sacs. But as Schenkkan (1971) has

pointed out, the accessory sacs are blind diverticula,

unsuited for the conduction of air between other

cavities. He also noted that they are extremely

variable and suggested an inverse relationship

between their size and that of the posterior portion

of the nasofrontal sacs. As with any of the diverticula, air storage and sound reflection are likely

possibilities. Air can pass into them without passing

through many other structures, arguing for their

usefulness as reservoirs in laryngeal sound production. The intrinsic musculature surrounding them

would be able to return the air to the respiratory

passages without involving manipulations of the

rest of the nasal complex. Their small size, of

course, is a point against their being effective in

this role.

Of all of the diverticula, the premaxillary sacs

are probably the best situated for storage and

recycling of air for sound production (particularly

for laryngeal sound production). They are larger

than the other diverticula, and open directly into

the bony nasal passage. Fibers of ai which run from

the maxilla over the nasal plug mass could easily

provide the compression necessary to recycle air

back into the nasal passage. At the same time this

would firmly seat the nasal plugs posteriorly and

block the escape of air into the dorsal parts of the

nasal tract. Purves (1967) is a strong proponent of

this view and thinks that the premaxillary sacs are

the primary reservoirs of air during phonation.

They are also effectively situated to contribute to

reflection of sound anteriorly.

Musculature

The pars posteroexternus (pe) of the nasal musculature, as defined in this paper, appears to be a

compressor of the underlying structures (Figure

20). This is certainly the case where its insertion

is upon the vertex, and thus fixed with respect to

its origin. Compression would limit vertical expansion of the vestibular sacs, and in so doing would

serve to increase lateral expansion. The same function could be performed by the pars anteroexternus, but since it also has a large insertion upon
38

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

the nasal passage, its contraction might produce

other, possibly undesirable, effects.

The pars intermedius (i) has no immediately

obvious function. Lying as it does, it could produce

compression as well as posterior displacement of

the structures deep to it. These functions could

also be performed by the pars anteroexternus (ae)

(Figure 20). The functional differentiation between

i and ae will have to await experimental evidence.

The most posterior of the superficial fibers of the

pars anteroexternus (ae), which insert upon the

posterior wall of the blowhole, act to draw the

posterior lip backward, facilitating opening of the

blowhole aperture. The superficial fibers originating just anterior to this, however, run from an

origin posterior to the nasal passage to an insertion

anterior to it. These perform the antagonistic function of drawing the anterior lip posteriorly, thus

acting to close the blowhole aperture. As the

anterior lip is more mobile than the posterior,

simultaneous contraction of all the superficial fibers

of ae would probably result in maintaining blowhole closure, drawing the aperture slightly posteriorly and compressing the underlying structures.

The fibers of ae which lie adjacent to the vestibular

sacs are loosely attached to them and could posFICIRF. 20.—Diagramatic view of the actions of the layers of

the nasal musculature. (ae = pars anteroexternus; ae-a = pars

anteroexternus, anterior fibers; ae-p = pars anteroexternus,

posterior fibers; ai = pars anterointernus; i = pars intermedius; npm = nasal plug muscle; pe = pars posteroexternus;

pi = pars posterinternus).

sibly serve to draw the sacs {posteriorly. The greater

part of ae passes beneath the vestibular sacs, where

its fibers converge radially upon the walls of the

nasal passage. At this level ae is a strong dilator of

the nasal passage.

The pars posterointernus (pi), inserting via a

tendinous sling around the posterior wall of the

nasal passage, draws the posterior wall anteroventrally, opposing the action of the posterior fibers

of ae (Figure 20). Pi is certainly one of the main

agents of passage closure at this level. In drawing

the posterior wall ventrally it also serves to bring

the blowhole ligament to bear upon the lip of the

nasal plug, facilitating closure of the bony nasal

aperture.

The pars anterointernus (ai) is the largest and

the most powerful of the nasal muscles. Its principal function is closure of the nasal passages, both

by drawing the anterior wall posteriorly and by

compressing the nasal plug mass, forcing the plugs

back over the bony nares (Figure 20). The anterior

portions of ai, which insert upon the nasal passage

could, however, be functional in dilation of the

passage. As suggested by Purves (1967), ai could

also compress the premaxillary sac and recycle air

from that sac to other parts of the system. In addition, Purves suggested that ai compresses the accessory sac, a function which may be better performed

by parts of the intrinsic musculature.

Purves (1967) contended that the separate layers

of nasal musculature (ae, pi, etc.) could not operate independently, owing to the disposition of the

nerves and blood vessels among them. His observations were based on studies of specimens in which

the vasculature had been injected with latex or

polyester resin. He found that the innervation and

vasculature "which supply the major groups of

muscles spring each from a separate main trunk

and pass from layer to layer within the group,

branching only within the 'layer' of the muscle."

He concluded that shearing stresses produced by

independent action on the muscle layers could

cause ruptures of the vessels. I found the same

distribution of vessels and nerves in my dissections,

and did not consider it remarkable, as it is the

normal pattern for innervation and vascularization

of skeletal musculature. One has only to examine

an injected preparation of the human forearm,

where the same pattern can be seen in the musculature controlling the fingers, to realize that this
NUMBER 207 39

arrangement can permit considerable independence

of muscle action.

It is difficult to assign a discrete function to the

intrinsic musculature of the nasofrontal sac. Its

disposition along the posterior portion of this diverticulum, around the communication of the nasofrontal sac with the inferior vestibule, and around

the accessory sac puts it in a position to produce a

variety of actions upon these structures. It probably

provides partial isolation of these diverticula, allowing independent emptying and filling of their

cavities. It can also provide constriction of these

diverticula, altering their shape and capacity.

Purves (1967) suggested that it draws the nasofrontal sacs laterally, assisting in pneumatic closure

of the nasal passage. I do not see how this would

work and think that it must be a minor function

at best.

As pointed out by Lawrence and Schevill (1956),

the nasal plug muscle withdraws the nasal plugs

from the bony nares. This muscle may also be

involved in complex movements of the nasal plugs

during phonation.

The rostral musculature is difficult to interpret

functionally. Lawrence and Schevill's (1956) contention that it serves to "keep the melon under

tension and makes a strong connection between it

and the rostrum" is difficult to accept. This could

lie performed equally well by the connective tissue

of the rostrum.

The melon is known to have considerable mobility in the beluga (Delphinapterus leucas). This

has not been demonstrated in any other odontocetes, and the relationship of the beluga to the

delphinids is not well understood. It is possible,

nevertheless, that the rostral musculature may produce slight changes in the shape of the melon in

delphinids.

There is a possibility that the rostral musculature may play a role in sound projection. Recent

work by Norris and Harvey (1974) has demonstrated gradients in sound velocity in the melon,

which they feel may be of importance in shaping

the sound field. The rostral musculature, lying

immediately adjacent to the melon, may be

involved in this system, and may be capable of

altering its effect upon the sound field through

changes in its acoustic properties upon contraction.

The lateral portion of the rostral musculature is

partly associated with the upper lip. The lips of

cetacea are generally considered to be immobile,

but in view of the great expanse of lip surface in

animals such as Globicephala and Grampus and

the relatively large mass of muscle inserting into

the connective tissue of the lips in these forms, a

certain amount of mobility may be present and

may be important in feeding. It is interesting to

note that a greater portion of the rostral musculature was concerned with the lips in Orcinus and

Pseudorca than in other delphinids. This may be

part of their specialization for feeding on large

prey.

At least one of the functions of the nasal plugs,

that of closing the nasal passage at the level of the

bony nares, seems relatively clear. These plugs fit

tightly over the surface of the premaxillae, sealing

the nasal passage at that point. It is possible, as

suggested by Lawrence and Schevill (1956), that

air could be forced arovind the plugs from below.

This would involve unseating the plugs at some

point determined by the pattern of compression of

the muscles dorsal to the plugs, and could allow

air to flow into either the premaxillary sacs or the

inferior vestibule. From the inferior vestibule air

would be free to enter both the accessory and nasofrontal sacs.

Evans (1973) provided a new suggestion on the

role of the nasal plugs in sound production.

According to his theory, movement of the plugs

against the margin of the bony nares would set up

relaxation oscillations, "much the same mechanism

that causes chalk to screech when pushed across a

blackboard." This hypothesis was later amplified

(Evans and Maderson, 1973), taking more anatomical details into consideration.

The lips of the nasal plugs have been implicated

in sound production, a function which will be

discussed in detail later in this paper. They also

appear to provide a more effective seal over the

bony nares by projecting posteriorly beneath the

blowhole ligament.

The function of the diagonal membrane is probably more complex than has been suggested.

Lawrence and Schevill (1956) thought that it facilitated closure of the nasal passage by the nasal

plugs. Norris (1969) suggested that it may form

part of an air metering system for sound production. It is also possible that these membranes may

be directly involved in sound production. Now that

it is known that they are under muscular control,
40

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

it seems likely that they play a more active role

than was previously thought.

The blowhole ligament and the fat body associated with it maintain stability in the complex

area around the inferior vestibule. The blowhole

ligament prevents the mouths of the accessory and

nasofrontal sacs from collapsing, and provides a

surface against which the nasal plugs fit in closing

the nasal passage. The fat body maintains the shape

of the posterior fold.

Melon

The melon has constituted one of the most enigmatic portions of the nasal complex. One suggestion as to its function was that of Howell (1930),

who thought it might be a buffer to reduce the

effect of water pressure on the skull. While the

role of water pressure in influencing the shape of

the cetacean head has been exaggerated, the idea

of the melon as a buffer is fairly plausible. It is

suitably constructed for such a purpose, having a

soft, almost fluid core contained within a tough

sheath of dermal connective tissue. It seems likely

that in some of the bulbous-headed delphinids

(particularly Globicephala) the melon actually

serves this purpose. It seems less likely, however,

that this is of primary importance in other, less

specialized delphinids.

Huber (1934) was of the opinion that the melon

serves as a special sensory organ to detect changes

in pressure "when the animal accelerates, when it

dives to greater depths, or approaches unyielding

objects. . . ." This seems to have been based on its

presumed rich innervation. I attempted to follow

this innervation, and believe that most of it runs

to the area around the nasal passages and to the

skin. The skin is known to be highly innervated

(Palmer and Wenddell, 1964) and could better

accomplish some of the functions suggested by

Huber. The detection of changes in hydrostatic

pressure requires a different sort of mechanism.

Since animal tissues are relatively incompressible,

this function is likely to be performed by sensors

in air-containing structures which are subject to

compression with changes in depth.

Another group of suggestions has been that the

melon served as a reservoir for dissolved gases.

Howell (1930) suggested that the melon and other

fatty structures might absorb carbon dioxide, but

felt that this was more possible than probable.

Kooyman and Andersen (1969) suggested that fatty

structures in diving mammals might serve as nitrogen buffers during serial deep dives. The lack of

vascularity in the melon makes it unlikely that it

is involved in any sort of gas exchange.

Raven and Gregory (1933) thought that the

lesser density of the melon served to buoy up the

anterior end of the animal, making breathing

easier. This has been recently revived by Clarke

(1970), with respect to the extreme situation seen

in the sperm whale. In the case of the sperm

whale, as in the bulbous-headed delphinids, the

amount of energy required to push this structure

through the water is likely to more than make up

for the small advantage conferred in raising the

head to the surface. It must also be borne in mind

that, while a slightly positive buoyancy may be of

some advantage in rising to the surface to breathe,

it is of a corresponding disadvantage in diving.

Clarke (1970) has hypothesized that the spermaceti

organ in Physeter is cooled by drawing water into

the nasal passage, thus altering the density of this

mass when the animal is ready to dive. Lawrence

and Schevill (1956), however, note that cetaceans

seem to be able to rapidly alter their buoyancy,

probably through altering lung displacement.

Ridgway (1971) further discussed Clarke's hypothesis from a physiological standpoint and concluded

that it was unlikely.

Raven (1942) thought that the melon served as

a cushion upon which the nasal musculature acted

to compress the nasal plugs against the bony nares.

While this may occur in the most posterior portions of the melon, the greater portion of it lies

anterior to the insertion of this musculature.

Recently, with the increased knowledge of echolocation in delphinids, the melon has been examined with respect to possible acoustic roles. The

shape and position of the melon led to the suggestion (Lilly, 1961) that it is an acoustic lens, a

theory which has received considerable acceptance.

The principal objections to this theory have been

that the melon is not shaped like a lens and that

there was no evidence that its acoustic properties

differ sufficiently from those of the surrounding

tissues to make it effective as an acoustic refractor.

Kleinenberg et al. (1969) subscribed to the idea

of the melon as an acoustic lens, although with no

new evidence along this line. They also suggested
NUMBER 207 41

that the melon may be able to focus sufficient acoustic power to enable prey to be stunned at a "considerable distance." It seems highly unlikely that

the animals would be capable of generating enough

power to do this without disrupting their own

tissues.

Norris (1968) has suggested that the melon

serves as an acoustic waveguide, offering a path of

minimum resistance through the forehead tissues.

This, of course, can be countered by the suggestion

that there would be even less acoustic resistance if

there were no tissue there at all. However, assuming that the elevated vertex and the posterior nasal

apparatus are important to the animal, removing

the tissue of the melon would result in a concave

forehead, producing more drag than a convex forehead as the animal moves through the water. The

conclusion from this line of reasoning is that the

melon is merely filler to produce a particular external form. While this may have been important in

the early evolution of the melon, it is probable

that other functions are presently more important.

The work of Bullock et al. (1968), in which

areas of sensitivity to sound were mapped on the

head of a live animal, suggested that the melon

might be involved in acoustic reception. They

found two general areas of sensitivity: a ventral

one over the posterior end of the lower jaw and a

dorsal one anterolateral to the blowhole. Norris

(1968) suggested that an acoustic waveguide may

extend from the dorsal area through the antorbital

notch to the lower jaw and thence to the ear. The

antorbital notch is occupied by dense connective

tissue through which the facial nerve runs and

seems unlikely as a route for sound conduction.

Experimental work by Norris and Harvey (1974)

did not demonstrate acoustic transmission in this

area. The alternative is conduction through the

bones of the skull, which is contrary to the present

theories of cetacean hearing. However, of these two

alternatives, I would tend to support the latter

theory, rather than the idea of an antorbital waveguide. More work needs to be done to demonstrate

the paths of sound reception, and to clarify the

possible role of bone conduction in hearing.

Ackman et al. (1971) noted that the lipids of

the melon and mandibular fat bodies (which are

suspected of playing a role in sound transmission)

were similar and that they differed from the lipid

content of the blubber. They speculated that these

differences may reflect differing physical properties

advantageous for high frequency sound transmission.

Recent experiments by Norris and Harvey (1974),

utilizing tissues from freshly dead specimens, have

demonstrated a gradient in sound velocity in the

melon tissues. They found that the center of the

melon possessed relatively slow transmission velocities, while peripheral areas were somewhat faster

(ca. 10%). These differences may be due to variations in lipid composition or lipid content, as

described by Litchfield et al. (1973). Unfortunately,

it is not possible to make a precise comparison

between Norris' sound velocity data and Litchfield's lipid data, as the exact correspondence

between the sites measured cannot be determined.

This would be of great interest, as the greatest

velocity difference (in Norris' section C, about

30%) does not appear to correspond to any of the

lipid differences described by Litchfield, nor to any

anatomical differences known to me.

Unfortunately, no data is available on the in

vivo acoustic properties of any of the tissues of the

facial complex. Until this is available, the acoustic

functioning of the structures will remain unclear.

Glandular Structures

Glandular structures have been described in the

nasal passages of Delphinapterus leucas (Watson

and Young, 1879), Platanista gangetica Anderson

(1878), and Tursiops truncatus (Maderson, 1968).

I have found tissue which appeared to be glandular

in Phocoenoides dalli and Inia geoffrensis. The

observation of Watson and Young (1879) may be

in error, as their specimen was in an advanced state

of decomposition. Such structures were not mentioned by Kleinenberg et al. (1969) in their extensive monograph on D. leucas.

Glandular tissue in /. geoffrensis and P. gangetica

was located around the nasofrontal and accessory

sacs and the inferior vestibule. I could not discern

any ducts or openings into the nasal passage, leaving the functional relationships of the glands

unclear.

In P. dalli the anatomical situation is much

different. Here the anterior portion of the nasofrontal sac itself is modified into what appears to

be a glandular structure.

Glandular tissues have recently been discovered

in the area of the inferior vestibule in T. truncatus
42

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

(Maderson, 1968; Evans and Maderson, 1973). They

are described as compound acinar, exocrine glands,

opening onto the surface via small crescentic pores.

The secretion of these glands is not mucinous and

is suggested to contain a lipid, possibly for lubrication of adjacent structures.

Functional Basis of Sound Production

REVIEW

Odontocetes have long been known to produce

sounds and there is a relatively voluminous literature dealing with this subject. With the discovery

of echolocation in odontocetes, there has been a

tremendous increase of activity relative to cetacean

sound production. In the last ten years, by far the

bulk of the literature dealing with odontocetes has

been concerned with acoustic problems. Unfortunately the problems are complex and much remains

to be resolved.

The mechanism of sound production in Cetacea

is poorly understood and the literature pertaining

to it is full of confusion, errors, and misunderstanding. Norris (1969) lists the following as being

the only definitely known sources of sound production in odontocetes: the lips of the blowhole (external), movements of the jaws, and slaps of the

body, flippers, or flukes against the water. None

of these mechanisms accounts for the variety of

complex sounds which these animals have been

observed to produce.

In the following pages I will review first the

nature of the sounds and the sound field, then the

theories of the site and mechanism of sound production. Following this, I will consider these problems in the light of the present study.

The nature of the sounds themselves has received

the greatest attention, as this has been the most

accessible part of the problem. Norris (1969) and

Evans (1973) have provided summaries of the

descriptive information on odontocete sounds. Unfortunately the state of our knowledge is not such

that detailed comparisons of delphinid sounds can

be made. An extremely wide variety of equipment

has been used to record these sounds, limiting the

frequencies which could be analyzed in many cases.

The relatively recent discovery that the sound field

is highly structured (Evans and Prescott, 1962;

Norris and Evans, 1967; Schevill and Watkins,

1966; Evans, 1973) has made it imperative that the

orientation of the animal with respect to the receiving apparatus be precisely known. This has seldom

been the case. Norris (1969) presented evidence

that there may be considerable individual variation

in echolocation, further complicating the situation.

Caldwell et al. (1965) have demonstrated individual variation in the low frequency components of

delphinid vocalizations. Thus it is impossible at

present to make any correlations between anatomical differences and differences in sound production.

Odontocetes are known to produce sounds from

within the audible range of humans to over 250

kHz (Norris and Evans, 1967). Within this frequency range there is a variety of sound types. Two

general types of sounds are important for consideration of sound production mechanisms: (1)

whistles or squeals, which are within the audible

range of man and which seem to be primarily

communication signals; and (2) clicks, which are

broad-band pulsed sounds extending well above

the audible range. The latter are usually considered to be primarily important for echolocation.

As noted above, the sound field produced by

delphinids has been shown to be highly directional.

The shape of this field has been described for a

few animals and had been shown to vary with the

frequency of the emitted sound. Most measurements of this field have been made in the horizontal plane and indicate an asymmetry in the shape

of the field. In general, the greatest amount of

energy is radiated directly anterior to the animal,

with the field strength dropping laterally and posteriorly. This is particularly true of the higher

frequencies. Norris and Evans (1967) presented

data based upon work with live animals (Steno).

Their data indicate that the sound intensity 20

degrees to the left of the midline is 1-2 db greater

than that 20 degrees to the right of the midline

(frequency unspecified). Evans et al. (1964) obtained

essentially the same results with an artificial sound

source implanted "in the area of the nasal sacs" in

an infant Stenella microps ( = S. longirostris) cadaver. Their tests ranged from 20 to 60 kHz and

indicated that the asymmetry increased with an

increase in frequency. The sound field observed by

these workers was less directional than that measured by Norris and Evans (1967) with live Steno.
NUMBER 207 43

Evans et al. (1964) also measured the sound field

in the vertical plane (under the same conditions)

and found slightly more energy dorsally in the low

range, changing to ventrally at 60 kHz. Evans

(1973) presented further data based upon work

with a live Tursiops truncatus. He noted a double

pulse waveform with maximum energy at 30 kHz

and a striking right-left asymmetry in relative

strength of the two pulses. Measurements of the

shape of the sound field indicated a rapid loss of

energy below the horizontal plane of the animal.

These measurements were apparently based on the

30 kHz pulses, although the frequency or bandwidth of the measurements is not given.

Evans et al. (1964) conducted tests on dry skulls

of Tursiops and found that for the lower portion

of the range (20-40 kHz) more energy was radiated

laterally than anteriorly. At 60 kHz, however, this

changed and the anterior portion of the sound field

was about 10 db above the lateral portion. Their

data also indicated that for the skull alone, the

asymmetry becomes less at higher frequencies.

Evans and Prescott (1962) produced sounds by

forcing air through the upper respiratory system

(including larynx) of a severed head of Stenella

grafjmani (= S. attenuata), as well as by forcing air

through the excised larynx alone. They stated that

the sounds produced in both cases were similar,

although the production of "echolocation clicks"

was dependent upon inflation of the nasal sacs.

They measured the sound field around the head

(all frequencies) and found that it was stronger on

the right side in both the horizontal and vertical

planes. They also found a substantial ventral element to the sound field.

The statement that there is no significant ventral

portion of the emitted sound field (i.e., that sound

is emitted "above the level of the mouth") has

appeared in the literature as an argument against

the larynx as a sound source (Norris, 1968). This

is based upon the findings of Norris et al. (1961),

who stated that when their experimental animal

presented the ventral surface of the head to the

hydrophone, "the volume decreased markedly." No

frequency specific measurements were made and

the type of sound (whistle or click) was not specified. The text implies that this concerned the

audible sound range only. Since the data of Evans

et al. (1964) indicate that the strength of the ventral portion of the sound field increases with frequency, the implications of Norris et al. (1964)

may not hold for the higher frequencies of the

echolocation sounds.

At this point I would like to review the arguments concerning the site of sound generation in

odontocetes. These are concerned with two areas,

the larynx (which is somewhat removed from the

area of my work) and the upper portion of the

nasal passage.

At the moment there is no direct evidence relating to the mechanism of sound production, and

relatively little indirect evidence.

The diverticula of the nasal passage have frequently been implicated in sound production (Lilly

and Miller, 1961; Lilly, 1961, 1962; Evans and

Prescott, 1962; Norris, 1964, 1968; Norris and

Evans, 1967), a possibility originally suggested by

Lawrence and Schevill (1956). Lilly and Miller

(1961) speculated that the cavities of the nasal tract

are "shock excited." I have trouble following their

arguments, but it seems that shock excitation is by

means of sound (specifically, clicks) produced elsewhere. This is in accordance with the view expressed by Lilly (1961) that the clicks were produced

by the larynx. He does, however, state that the

nasal plugs and sacs are used to produce sound, but

does not produce any evidence for this statement.

Lilly's other work (1962) merely contains a reference to his book (1961). Thus, the work of Lilly,

which is frequently cited as supportive of nasal sac

x

sound production, contains no evidence and, in

fact, expresses the view that the larynx is the source

of the "echolocation clicks."

In their work on severed heads of Stenella graffmani (= S. attenuata), Evans and Prescott (1962)

noted that production of "echolocation clicks"

ceased if the nasal diverticula were deflated by

depressing the anterior surface of the head (over

the melon). This could be interpreted as evidence

that the nasal sacs were involved in sound production (as the authors suggested). It is also possible

that such manipulation more firmly seats the nasal

plugs, slowing the flow of air through the entire

system.

Another line of evidence which has been brought

forward as implicating the nasal diverticula is that

the sound field is stronger on the dorsal surface of

the animal. As noted earlier, the evidence for this

is scanty and indicates that this is true principally

for low frequencies. Even if this were demonstrably
44

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

the case, it does not preclude laryngeal sound

production.

One of the underlying problems of this question

concerns the anatomy of the nasal diverticula.

Lawrence and Schevill (1956:114) described the

accessory sac (connecting sac) in such a way that

it is possible to get the impression that it has two

openings, one into the nasal passage and one into

the nasofrontal sac. This is further implied by the

name ("connecting sac") which they used for this

diverticulum. Their illustrations, however, do not

show this to be the case. I think that this has

resulted in a number of people believing that the

accessory sac forms an alternate pathway for air to

reach the nasofrontal sac. This view is implicit in

several papers of Norris (1964, 1969) and is explicit in van Heel's (1970) illustration of the nasal

passages. Norris (1964) postulated that air is forced

from the vestibular sacs into the nasofrontal sacs,

passing around the lateral lips of the nasal plugs

and producing clicks. According to him the air

passes from the nasofrontal sacs through the accessory sacs to the nasal passage below the level of the

nasal plugs. The plugs remain seated throughout

this procedure. When the supply of air in the

vestibular sacs is depleted the nasal plugs withdraw

from the nares and air is passed to the vestibular

sacs, allowing a new cycle to start. Neither Schenkkan (1971) nor I have found any anatomical basis

for the idea of a continuous passage for air past

the lateral lips of the nasal plug.

The lateral lips of the nasal plugs rest within

the common orifice of the accessory and nasofrontal

sacs (the inferior vestibule), but both of these sacs

(as described by von Baer, 1826; Gruhl, 1911; and

Lawrence and Schevill, 1956) are in fact blind.

This limits the amount of air which can be passed

through this system without pausing for recycling.

Kleinenberg et al. (1969) discussed the role of

the nasal diverticula in sound production, basing

their observations on the beluga. According to

them, the sound source could be located by ear in

the upper part of the nasal passages of belugas

examined on land. Tampering with the nasal

apparatus by hand affected sound production.

These observations, of course, dealt with sound in

the human audible range, apparently of the whistle

type. They suggested that sound is produced by

the movement of air between the diverticula (with

the nasal plugs seated). This general idea has

appeared in the work of many people, usually,

however, involving recycling of the air between the

upper and lower respiratory passages. The explanation of Kleinenberg et al. (1969) involves only the

supracranial portion of the respiratory system. The

details concerning the operation of this mechanism

were not discussed.

Purves (1967) discussed sound production in

cetaceans at great length and concluded that the

larynx is capable of producing the sounds used for

echolocation by odontocetes. His initial argument

is that of Occam's Razor, whereby the larynx

should be assumed to be used in sound production

unless there is some compelling reason to believe

otherwise. He eliminated the lack of "true vocal

chords" as an argument against laryngeal sound

source in cetaceans by noting their absence in most

mammals other than man. Mammals generally

employ modifications of the thyroarytenoid fold,

artiodactyls utilizing the aryepiglottic folds (Negus,

1949). Purves carried out a series of experimental

investigations on the larynx and concluded that it

was capable of producing the sounds recorded from

odontocetes. He also concluded that coupling of

sound to the skull via the palatopharyngeal muscles would result in the observed pattern of the

emitted sound field. His data do not, however,

eliminate the possibility of nonlaryngeal sound

production, as he did not investigate this aspect

of the problem in his experiments.

Evans (1973) argued against Purves' theories of

laryngeal sound production on a variety of points.

His observation that a "closed tube" model could

not produce the observed sounds may be correct,

but probably does not apply to the cetacean larynx,

which is a complex, flexible structure, nor does

the argument that the lack of demonstrated differences in the laryngeal anatomy of whistling and

nonwhistling species carry much force. The observed differences in sound production may be

limited by behavior rather than anatomy, and,

definitive anatomical studies of the larynx remain

to be done.

The hypothesis proposed by Evans (1973), that

sound is produced by movement of the nasal plugs

against the edge of the bony nares and not through

airflow past apposed surfaces, has several advantages. It removes the questions of complex airflow

and the problem of sound production at great

depth, where the air volume is very limited. Al-
NUMBER 207 45

though it is not explicit in his papers (Evans, 1973:

Evans and Maderson, 1973), it is presumed that

this explanation is meant to cover production of

high-frequency clicks and not the lower frequency

whistles.

Recently Norris et al. (1971) have presented an

analysis of low frequency "chirp" production based

upon cineradiography of the head of a live Stenella

longirostris. They demonstrated complex movements in the nasopharynx and nasal diverticula

concurrent with production of squeals or chirps,

and concluded that the most probable site for production of these sounds was the left nasal plug.

Briefly, the sequence of events described by them

consisted of movement of air (recycling) from the

nasal diverticula into the nasopharynx, closure of

the nasal plugs and posterior nasopharynx, movement of air past the nasal plugs into the premaxillary sacs, then pulsation of the tissues around the

left nasal plug, with air movement into the spaces

above the plug. The last part of this sequence was

correlated with production of squeals. This activity

was observed only in the left naris.

One of the critical factors in this experiment was

the determination that there was no airflow through

the larynx during sound production. Although

their arguments are convincing, the question may

be raised of the adequacy of the resolution of the

cineradiography equipment to demonstrate this

conclusively. If there remains a possibility of air

movement through the larynx, the events observed

above may be correlated with movement of air into

reservoir space rather than sound production per se.

As noted by the authors, their evidence relates to

production of low-frequency squeals and not to

clicks.

Schenkkan (1973) raised a series of objections to

the hypothesis of Norris et al. (1971). His statement that "no one has disputed that dolphins can

produce sounds with their nasal passages when the

head is above water" is irrelevant, as the authors

were not dealing with the familiar noises produced

by trained animals with their blowholes open, but

rather with sounds apparently identical to the

squeals produced underwater with the blowhole

closed. The nasal plugs are not essential to preclude water from being taken into the internal

nares, as stated by Schenkkan (1973), since closure

can be effected both by the blowhole and between

the level of the vestibular sacs and the nasal plugs

by tissue elasticity and muscular control. The nasopalatine sphincter is capable of movement anterodorsally, contra Schenkkan's statement, as can be

readily demonstrated by manual pressure in a fresh

specimen. This muscle is very loosely attached to

the periosteum of the nasal passage and moves

quite readily over it. Schenkkan's (1973) views concerning the loss of any air which passes distal to

the nasal plugs is based upon the assumption that

the nasal plugs cannot be unseated underwater,

which has been partly discussed above. Anatomically the plugs appear capable of complex movements, and there is no reason to assume that air

cannot be moved around them without losing it

out the blowhole or allowing water to enter.

Schenkkan (1973) presented a rather elaborate

description of the functions of the nasal diverticula

and associated structures during phonation. Unfortunately he appears to have adopted fairly rigid

ideas of the possible relative movements of air and

of the anatomical structures, without sufficient

allowance for the complexity of the system. His

functional observations are further clouded by the

derivation of a sequence for the evolution of the

cetacean nasal complex based upon an arrangement of the highly specialized living forms into a

supposedly phylogenetic series.

Schenkkan (1973) argued heavily against many

of the current theories of sound production. His

observation that ziphiids produce echolocation

clicks but do not possess lateral lips on the nasal

plugs is certainly an argument against those structures being used for sound production in that

group, and clearly suggests that echolocation clicks

can be produced by some other mechanism. It does

not necessarily apply, however, to the somewhat

distantly related and structurally different delphinids. Nor would it be necessary, as he postulates, for the entire nasal plug mass to vibrate in

order to produce sound in the absence of lateral

lips. His argument that air expanded in vibrating

the lateral lips of the nasal plug could not be

recovered is unlikely and is in contradiction to

most of his earlier statements about airflow, particularly in and out of the nasofrontal sacs. The

further argument that clicks would be confined to

the right side and as such could not be produced

into a beamed transmission, since such transmissions are only produced through interference

between two or more sources, is incorrect. This is
46

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

indeed one way to produce a beamed pattern,

which can also be produced by reflection, refraction, attenuation, or any combination of these.

Schenkkan's arguments for laryngeal sound production suffer similar deficiencies. As stated in his

paper, production of relaxation oscillations through

a constricted aperture is efficient, but can be applied

equally to all of the suggested sites of sound production, not just the larynx. His concept of

"matched loads" equally fits all other areas of the

system. The fact that the lips of the nasal plugs

are nonmuscular has no bearing on the theories

involving their action in sound production, all of

which postulate vibration between apposed surfaces, not freely in an air cavity as stated by Schenkkan. His calculations of the potential power output

of this musculature (based upon Gray's (1936)

estimate of the power output of dolphin axial musculature) suffers from the consideration that the

visceral musculature associated with the larynx

probably differs considerably in physiological characteristics from the skeletal muscles used in locomotion.

In short, Schenkkan's (1973) functional discussions of sound production seem to have little actual

bearing on the problems involved.

The fact that odontocetes can produce both

"whistles and clicks" simultaneously, starting and

stopping one without affecting the other, and with

no indication of one modulating the other, has

been cited as an indication that two separate sound

sources were active (Lilly and Miller, 1961). This

is circumstantial evidence for both the larynx and

the nasal apparatus being active in sound production. Following the suggestions of Evans (1967)

and Schevill (1964), among others, that the larynx

is responsible for whistles, this would leave the

nasal apparatus responsible for the "echolocation

clicks." It is also possible, as suggested by Norris

et al. (1971), that the left nasal plug produces

whistles while the rigTit produces clicks.

One thing which must be borne in mind in any

discussion of sound production is the possible differences between apparent and actual sources of

sound. Sound may be conducted from its actual

source to another point at which it becomes apparent to the observer. The evidence to date suggests

that sound radiates from a point external to the

skull, but deep within the facial complex. This

does not, however, preclude a laryngeal sound

source, as sound could easily be conducted from

the larynx to the external bony nares.

ANATOMICAL CONSIDERATIONS

Purves (1967) discussed the nature of the sounds

produced by odontocetes and concluded that they

were of the relaxation oscillation type, produced

by the approximation of the walls of some portion

of the nasal passage, forming an aperture through

which air is forced. This mode of sound production

has also been variously referred to as "raspberry"

or "Bronx cheer" sound production. If this is the

case, only those portions of the nasal apparatus

which can be approximated to form suitable apertures are likely to be involved in sound production.

Unfortunately, there are a great many structures

of this description within the nasal passages and

diverticula. Thus, while it is not possible to conclusively delimit the site of sound production on

an anatomical basis, it may be possible to decide

which structures are most likely to be involved and

which are least likely. In production of sounds of

this sort, it would seem that relatively small apertures would be advantageous, as they would permit

higher velocities of airflow with the restricted

amount of air available. For the same reason,

structures which can be tightly appressed are more

suitable than those which can only be loosely

approximated. It is also advantageous to have a

large reserve volume on either side of the site of

sound production to minimize the necessity for

recycling the air.

The juncture of the spiracular cavity with the

vestibular sacs, while under considerable muscular

control, is quite wide and thus probably not

involved in sound production. The apertures of

both the nasofrontal and accessory sacs are held

open by the blowhole ligament and are thus

incapable of sound production by themselves. The

lateral lip of the nasal plug, however, may be

inserted into the apertures of these diverticula to

form an appropriate mechanism for sound production. This is the prevalent theory at the present

time. The principal objection to this theory is that

in most species the volume of the nasofrontal and

accessory sacs is quite small. There is not, as was

sometimes supposed, a connection between the

distal portion of the nasofrontal sacs and the rest

of the nasal passage via the accessory sac. This
NUMBER 207 47

limited volume would impose serious limitations

on the duration of individual cycles of phonation.

The nasal plugs are capable of being apposed to

a great variety of surrounding surfaces to create

apertures, some of which are suitable for sound

production. These include the bony aperture of

the nasal passages, the posterior wall of the spiracular cavity, and the diagonal membrane. If air is

passing from the bony nasal passages into the distal

portion of the nasal system, the nasal plugs must

be partly unseated. Depending upon the movements of the nasal plugs, air could escape upward

via several routes. It could pass anteriorly into the

premaxillary sacs, but the surface between the

nasal plugs and the anterior edge of the bony nares

does not seem particularly suitable for sound production. Air could also pass between the nasal plug

and the diagonal membrane, entering anteriorly

where the membrane slopes ventrally into the bony

nasal passage. It could then pass posterolaterally

into the inferior vestibule, and from there into the

accessory and nasofrontal sacs. If the nasal plugs

were not closely appressed to the posterior wall of

the nasal passage, air could then pass dorsally into

the vestibular sacs. Along this route are several

structures which seem capable of sound production.

The most likely of these are the diagonal membrane, where it lies against the nasal plug, and the

lateral lip of the nasal plug, where it is in contact

ventrally with the wall of the inferior vestibule.

Either of these sites would probably allow passage

of air into the spiracular cavity and vestibular sacs.

The above ideas have presumed movement of

air from the bony nasal passage into the supracranial portion of the nasal system. There is also

the possibility of involvement within the supracranial system between the diverticula or movement from the supracranial system ventrally into

the bony nares.

If the vestibular sacs are involved in the movement of air during sound production, it is most

likely that they serve as reservoirs to receive air,

rather than as sources of air. This is due to the

arrangement of the anterior fold, which would

probably not allow passage of air toward the deeper

structures without the spiracular cavity being

opened fairly widely.

The premaxillary sacs are better suited to serve

as sources for air during phonation. With the nasal

plugs seated, air could pass from the premaxillary

sacs posterolaterally, ventral to the lateral lips.

The insertion of ai is suitably placed to compress

the premaxillary sacs, providing the pressure necessary for high air velocity.

An interesting possibility is the movement of air

from the premaxillary sacs into the bony nasal

passage past the apposed surfaces of the nasal plug

and diagonal membrane. This seems like an admirable site for sound production, except that air

movement in this direction would probably interfere with production of sound by the larynx. It

might, however, be possible for air to flow between

the nasal plug and the posterior wall of the nasal

passage. The arrangement of musculature within

the nasal plug is reminiscent of the intrinsic musculature of the tongue, suggesting that it might be

capable of complex movements.

A principal consideration in the functioning of

the nasal structures is the levels at which the

various portions of the system can be isolated. The

vestibular sacs can certainly be isolated from structures ventral to them through the combined actions

of the anterior folds and the nasal musculature.

The interaction of the deeper structures is more

complex. As noted earlier, the apertures of the

accessory and nasofrontal sacs are held open by

the blowhole ligament, and it is only through

movements of the lateral lip of the nasal plug that

these diverticula might be closed. The nasal plugs

would also be the critical factor in isolation of the

premaxillary sacs. In view of their possible plasticity, it is possible that they may be able to isolate

many of the deeper structures, allowing complicated airflow in this area.

As noted above, the nasal plugs are capable of

being apposed to a variety of structures, and are

probably capable of complex muscular activity.

This agrees well with Evans' (1973) theory of

sound production by movements of the nasal plugs

independent of any airflow. As he noted (Evans

and Maderson, 1973), the premaxillary sacs may

function as clefts allowing free anteroposterior

movement of the nasal plugs for this type of sound

production.

In summary, it appears that the structures most

likely to be involved in sound production are those

in the vicinity of the nasal plugs. The discovery

of musculature associated with the diagonal membrane renders it more likely than previously sup

posed that it is involved in sound production. All
48

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

of the available evidence, particularly that of the

asymmetry (to be discussed later), implicates the

nasal plugs in sound production.

Functional Aspects of Cranial Asymmetry

REVIEW

One of the striking peculiarities of the delphinid

skull is the asymmetry of the facial elements. The

entire area of the external nares is shifted slightly

to the left. This primarily involves the elements

bordering the nares, the premaxillae and the nasals.

The frontals and the maxillae are distorted to a

lesser degree. This sinistral displacement is most

pronounced along the median sutures between the

premaxillae, nasals, and the posterior portion of

the frontals. The lateral sutures, between the premaxillae and maxillae, and the maxillae and frontals are much less affected (Figure t). The rostrum

is usually free from this distortion. Correlated with

the displacement of the bones bordering the nares

is an enlargement of the right-hand elements. This

is most pronounced in the premaxillae, where the

ascending process of the right premaxilla is sometimes half again as wide as that of the left. Only

the facial elements are involved in this asymmetry.

The internal nares and nasal passages are symmetrical.

All living odontocetes show this cranial asymmetry to one degree or another. It seems to be least

in some of the river dolphins and is greatest in the

sperm whale (Ness, 1967). Mysticetes, however, are

completely unaffected by this phenomenon.

The question of the origin and functional significance of this asymmetry has been treated extensively in the earlier literature, which is reviewed

in the following pages.

Pouchet (1886) ascribed the cranial asymmetry

in odontocetes to a process which he termed "pleuronectism," derived from a comparison with the

flatfish, Pleuronectes. This term was applied to

symmetry modifications resulting from swimming

on one side. Pouchet pointed out the advantages of

the dorsal situation of the blowhole, arriving at the

conclusion that the blowhole will tend to seek the

dorsal surface. Thus, if the animal preferentially

swims on one side, the blowhole will migrate to

the other side. He presented very little evidence for

the relevance of this theory to odontocetes, merely

citing the old tale of handedness in the sperm

whale (see Scammon, 1874). He did note that

mysticetes swim on their sides as well, and attributed the asymmetrical pigmentation of Balaenoptera physalus to pleuronectism. He did not, however, explain why this had no effect on the

blowholes of mysticetes.

Weber (1886) briefly mentioned the cranial

asymmetry of odontocetes and considered it in

comparison with asymmetric variation seen in

pinniped crania without arriving at any conclusions.

Beddard (1900) discussed the phenomenon of

asymmetry in odontocete crania. He correlated it

with the presence of a specialized nasal apparatus,

but was unable to proceed further.

Abel (1902a, 1902b) provided one of the more

extensive overlooks of the question of odontocete

cranial asymmetry. Noting the fundamental differences between mysticetes and odontocetes in the

narial region, Abel correlated cranial asymmetry

in the latter with posterodorsal displacement of

the nares. He ascribed the immediate cause of the

asymmetry to the development of the nasal and

interparietal bones during ontogeny, but was unable to arrive at any functional or phyletic conclusions. He did state that the asymmetric pigmentation of the finwhale was not related to the cranial

asymmetry of the odontocetes, thus implicitly contradicting Pouchet's (1886) theory of pleuronectism. He also felt that Kiikenthal's (1893) ideas

about the relationship of the flukes to cranial

asymmetry were incorrect.

Lahille (1908) examined a skull of Balaenoptera

acutorostrata in which there was a slight asymmetry

of the nasal bones. He correlated this with lack of

a hypoglossal canal on one side, which he felt

might have produced a physiologic asymmetry, and

suggested that cranial asymmetry in cetaceans in

general might be connected with similar asymmetries in soft structures. The lack of a hypoglossal

canal on one side (the hypoglossal nerve then

exiting through the posterior lacerate foramen) is

relatively common and not connected with any

other manifestations of asymmetry. The cranial

asymmetry of odontocetes is certainly correlated

with soft part asymmetries, but not as far removed

as the ventral surface of the head.

Kiikenthal (1908) was of the opinion that Cetacea progressed through the water with a spiral

motion of the flukes. This was based partly on the
NUMBER 207 49

observations of earlier writers (Beddard, 1900) of

animals at sea, where the motion of the flukes

seemed more complex than a simple up and down

stroke. It was also based on Kiikenthal's own observations on fetal material (1893), where the flukes

are folded in a spiral fashion. Kukenthal felt that

this mode of locomotion produced a torque, bending the head to the left, and that the cranial asymmetry was produced by the difference in water

pressure on the two sides of the head as the animal

swam.

The principal defect in Kiikesthal's theory is that

the evidence applies equally to mysticetes, in which

there is no cranial asymmetry. Slijper (1936) suggested that the folding of the flukes in the fetus

may play a role in the uterus. The question of

movements of the flukes in locomotion is very complex. However, there is no sound evidence for any

asymmetry in their movements (Parry, 1949).

Lillie (1910) noticed that the larynx in two

specimens of Physeter examined at a whaling station was situated on the left side of the pharynx.

He concluded that this had developed to facilitate

passage of food through the gullet and that it has

resulted in asymmetric development of the nares

(the idea being implicit that differential use of

the nares in respiration resulted in the asymmetry).

One would expect on the basis of his hypothesis

that the left naris would be the larger of the two.

This, however, is the opposite of what actually

occurs. Lillie noted that Pouchet and Beauregard

(1892) found the larynx to be situated on the right

in Physeter. I would suspect that the larynx is

mobile, and that the position in which it lies

depends upon postmortem manipulation of the

carcass. Purves (1967:299) commented further on

this:

To complete the general description of the nasopharynx,

it must be stated, that, as with the larynx, this part of the

respiratory tract is perfectly bilaterally symmetrical and in

marked contrast with the upper narial region, which in the

odontocete is noted for its asymmetry. Even in the sperm

whale Physeter catodon, in which one of the upper nares is

from five to seven times greater in diameter than the other,

there is not the least trace of asymmetry in the posterior

narial region.

I would agree with this. However, on page 259 of

the same paper Purves stated:

In most odontocetes the left bony narial aperture is larger

than the right and the naris follows a more vertical course.

The epiglottic spout is bent slightly to the left (markedly so

in the Ziphiidae and Physeterida) and when the larynx is

pushed upward into the nasopharynx the glottis moves

towards the left posterior naris.

It is difficult to decide what Purves had in mind.

The narial passages of the odontocetes which I

have examined were symmetrical, except for the

area immediately adjacent to their exit from the

skull. As for Physeter, the narial asymmetry is considerable and apparently extends well down the

bony nasal passage. Hosakawa (1950) noted that

one of the intrinsic laryngeal muscles was asymmetrical in Physeter, as was the relationship of the

esophagus to the larynx. He did not, however,

mention that the larynx itself was asymmetrical.

Houssay (1912) agreed with Kiikenthal's correlation of cranial and caudal asymmetry, but thought

that the cause and effect were somewhat different.

According to his theory, the early cetacea were

unstable, tending to capsize. This resulted in the

cranial asymmetry. Subsequently the caudal asymmetry developed to correct for the instability

problem.

Steinmann (1912) followed the theory of Kiikenthal (1908), but went beyond it in attempting to

explain the origin of the asymmetry in the flukes.

According to this theory, cetaceans are descended

from ichthyosaurs and the horizontal flukes of the

former are derived from the vertical tail of the

latter. He noted that the vertebral column of

ichthyosaurs extended only into the lower lobe of

the tail, which is larger than the upper lobe. As

the tail rotated to assume a horizontal position, the

vertebral column regressed, but the former lower

lobe remained larger and the flukes retained an

ontogenetic vestige of this rotation in the form of

the spiral folding observed by Kiikenthal.

Howell (1925) discussed cranial asymmetry only

in noncetaceans and concluded that, when developed to an appreciable extent, it was due to disease

or injury.

Howell (1930) reviewed a few of the early

theories on cranial asymmetry and dismissed them

as unconvincing. He stated that he and Ernst Huber

had suspected the nasal musculature, but upon

examining it found it to be symmetrical, and was

unable to shed further light on the question.

Richard (1930) described an asymmetrical bending of the hemal arches in several specimens of

the sperm whale. From this he concluded that
50

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

unequal forces were being applied by the caudal

musculature originating from them, and that these

were producing the asymmetry of the skull. He

applied this theory to cetaceans in general, and

suggested that cranial asymmetry was not produced

in the mysticetes because the elastic jaw joints and

the large mass of the tongue acted as cushions

to absorb the forces applied by the tail. Slijper

(1936), however, stated that he could not find the

consistent caudal asymmetry upon which Richard

based his theory.

Slijper (1936), in his monograph on cetacean

anatomy, gave considerable attention to the question of cranial asymmetry. Building upon the

wealth of theories advanced by earlier workers

(largely Abel, 1902b; Houssay, 1912; and Pouchet,

1886), Slijper arrived at a phyletic and functional

interpretation of odontocete cranial asymmetry.

He accepted Pouchet's (1886) pleuronectism theory

as the immediate cause of the cranial asymmetry,

and looked for the cause of the swimming instability postulated by that author. Slijper's extensive

examination of the relationships of the viscera

(which are normally asymmetrically disposed in

vertebrates) resulted in the observation that the

Cetacea were uncommonly symmetrical in this area.

He countered this observation by supposing that,

in the transition from terrestrial forms, there must

have been an ancestral form which had the viscera

(mainly the lungs) asymmetrically arranged, and

that the cranial asymmetry became fixed during

that stage of phylogenetic development. Subsequently Slijper (1958) discovered that the apparent

organ symmetry documented earlier (Slijper, 1936)

was in error, and that the viscera of cetaceans are

as asymmetrically disposed as those of terrestrial

mammals.

Sleptsov (1939) investigated the state of cranial

asymmetry in fetal specimens of Delphinus, Delphinaptents, and Phocoena with regard to Kiikenthal's (1908) theory. Sleptsov found asymmetry to

be present at an early stage and strongly criticized

Kukenthal's ideas. He also measured a series of

flukes and found no consistent asymmetry. Sleptsov

suggested that the cranial asymmetry resulted from

more rapid ontogenetic reduction of the olfactory

nerve on the left. He also suggested that the asymmetry is useful in breathing without, however,

providing any basis for this.

Purves (1967) presented the most recent discussion of the problem of cranial asymmetry in odontocetes. He considered asymmetry of the narial

diverticula to be related to hydrostatic problems.

This was based on the argument that lateral displacement of the blowhole is advantageous during

ventilation, to reduce the amount of expired air

and water vapor taken in on inspiration. It is

difficult to imagine that the observed displacement

of the blowhole laterally (on the order of 1 to 2

cm in a large Tursiops) has an appreciable effect

on the pattern of flow of air and water vapor during expiration. At any rate, one might expect the

pattern of flow in expiration and inspiration to be

similar (i.e., if expired air is expelled laterally,

then inspired air should be drawn from that direction as well).

Displacement of the blowhole, along with the

associated diverticula would, according to Purves

(1967), result in a shift in the center of buoyancy

of the head, tending to return the blowhole to a

middorsal position. In order to counteract this, the

diverticula have become larger on the right. This

disparity of size in the diverticula is true for the

deeper diverticula, but not for the vestibular sac,

to which Purves assigns a particular hydrostatic

importance. The vestibular sac is slightly larger on

the right in some animals, equal in others, and

larger on the left in some. In some genera, such as

Stenella, this sac is consistently larger on the left

than on the right.

Purves (1967) further argued that paired nasal

passages of equal size are less efficient (in terms of

airflow) than if one is increased in size and the

other correspondingly decreased. His argument in

terms of surface/volume ratio is quite plausible.

However, it also follows that efficiency would be

even more drastically improved if both nasal passages were increased in size, and thus is not an

argument in favor of asymmetry, but of increased

diameter alone. It would seem that if the factors

controlling the diameter of the nasal passages would

allow an increase in the size of one, then they

might also allow an increase in the other. The

same net increase in efficiency gained by increasing

the size of one passage, while decreasing the size

of the other, could be gained by a relatively small

increase in the size of both passages. The above

arguments aside, it does not appear that the bony

nasal passages, in delphinids at least, differ in

diameter at any point other than their immediate
NUMBER 207 51

exit from the skull. As for the fleshy portion of the

passages, the right is much larger than the left,

contra Purves' arguments.

To summarize the discussion thus far, the early

theories attempting to explain the functional basis

of the cranial asymmetry fall largely into two categories: (1) those based upon the assumption of

asymmetrical locomotory forces (Kiikenthal, 1908;

Steinmann, 1912; Richard, 1930; Borri, 1931) produced by a screwlike movement of the flukes; and

(2) those based upon a buoyancy-related instability

or some unspecified lopsidedness (Pouchet, 1886;

Houssay, 1912; Slijper, 1936). Slijper (1936, 1961)

presented anatomical and observational data sufficient to indicate that the first group of theories has

no basis in fact and concluded that the folding of

the flukes observed in fetal material could be related

to problems of gestation and birth. He also concluded that the axial musculature showed no

asymmetrical development and that there was no

observational basis for asymmetrical movements in

swimming. In addition, it is obvious that those

theories apply equally well to the mysticetes. Richard (1930) had countered this argument by suggesting asymmetrical forces were absorbed by the elastic

joints and tongue of mysticetes. But, according to

this reasoning, Physeter, with its enormous mass of

connective tissue and fat on its head, should be the

least affected of all whales, whereas it is the most

asymmetrical in its facial anatomy.

The second group of theories can also be criticized on the basis that it applies equally well to

both suborders (as well as to other aquatic mammals) and, in fact, would apply most strongly to

archaeocetes, which show no signs of cranial asymmetry. In addition, these theories rest upon Pouchet's (1886) hypothesis that the blowhole will tend

to migrate dorsally. Thus, it would be expected

that the blowhole would be the most asymmetrically situated element in the system. While the

blowhole is placed slightly laterally, its relations

are not nearly as asymmetrical as those of the

deeper elements.

This brings us to the observation (Howell, 1930;

Abel, 1902; Beddard, 1900) that asymmetry of the

skull is correlated with the development of a complex nasal apparatus. This is based upon the facts

that (1) the blowhole apparatus is more complex

in all odontocetes than it is in any mysticete, and

(2) that the most complicated nasal complexes,

those of the physeterids, are associated with the

most asymmetrical skulls.

Norris (1964) discussed cranial asymmetry as it

might relate to sound production and suggested

that it might be instrumental in producing the

observed asymmetrical sound fields. He also suggested that the sound field asymmetry might be

more complicated than it seems, particularly with

respect to frequency distribution. In a later paper

(Norris, 1968), he noticed that the melon entered

only the right nasal plug in Delphinns, but did not

seem to connect this with the rest of the cranial

asymmetry.

Wood (1967), in a discussion of the nasal passages of Kogia, made the following observation:

"I think this asymmetry in the skull reflects the

evolutionary development of sound producing

mechanisms and the utilization of one narial passage primarily for sound production, and the other

for breathing."

This is the conclusion at which I have arrived

through examination of the delphinids, and which

I think can be applied to odontocetes in general.

ANATOMICAL CONSIDERATIONS

I have approached the problem of cranial asymmetry by first assuming that it is probably not the

bones which are primarily asymmetrical, but the

soft tissues associated with them. This working

hypothesis is based upon the generalization that

bony elements of a complex system are likely to

be more strongly influenced by the soft tissues

which they support than the other way around

(Moss and Salentijn, 1969). Accordingly, I have

attempted to ascertain which soft structures exhibited the greatest degree of asymmetry, as an indication of where the primary source of asymmetry

might lie.

This approach was largely confined to specimens

of Stenella, which provided the only sample large

enough to take individual variation and dissecting

errors into account. The small amount of data

collected from other genera show the same trends

as the Stenella data. My data on muscle weights

confirms the observation of Howell (1930) that the

musculature is relatively symmetrical (Table 3).

While a number of the weights of individual muscles were markedly asymmetrical in some of the

specimens, the combined weights of all of the
52

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

muscles for the specimens were less so. There is

considerable variation in the muscle weight ratios,

some of which is, no doubt, due to factors of dissection. These factors are substantially reduced by

lumping the weights for all the muscles on each

side of a specimen (total muscle weight ratio). This

ratio shows a consistent asymmetry, on the order

of 5 to 10 percent. If anything, I feel that this is

due to inclusion of more connective tissue in the

muscle samples from the right sides. The tendon

of insertion of these muscles is larger and, even

though I attempted to remove it consistently on

both sides, probably accounts for some of the asymmetry. At any rate, this asymmetry is much less

than that seen in the relative widths of the nasal

passages, which is on the order of 50 percent. The

asymmetry of the deep diverticula, as estimated

visually, is on this order as well, as is the width of

the lateral lip of the nasal plug. -The vestibular sac

did not appear to fit into this pattern, so it was

dissected and the epithelium of the sac weighed

to obtain relative size. The data of Table 3 indicate

that for the Stenella sample, the vestibular sacs

are equal in size, or slightly larger on the left, in

contrast to the deeper diverticula, which are larger

on the right. As with many other characters, Stenella coeruleoalba was an exception, the right vestibular sac being 50 percent larger than the left.

Having seen that the primary asymmetry probably lies in the fleshy portion of the nasal complex

between the levels of the premaxillary and vestibular sacs, we can attempt to interpret it functionally.

As discussed earlier in this paper, these structures

are apparently concerned with the production and/

or manipulation of sound.

Since the larynx normally occupies an intranarial position, all of the theories of sound production necessitate movement of air through the

cranial portions of the respiratory tract. Observations on living animals indicate that most sounds

are produced without loss of air from the system,

the advantages of which are obvious to a diving

animal. This means that air must be stored in the

distal portions of the system and recycled for sound

production. Since the diverticula are larger on the

right, it may be suggested that more air is cycled

through the right-hand portions of the system. This

is equally applicable, whether the sound is produced by the larynx, around the nasal plugs, or in

both places. In any case, it suggests that greater

acoustic activity takes place on the right side. The

same logic applies if the diverticula are considered

as reflective structures.

If the melon functions as an acoustic pathway,

then its posterior extension into the right nasal

plug supports both the idea of the nasal plug as a

sound source and the idea of greater acoustic activity on the right side.

As noted above, these arguments work equally

well for laryngeal or nasal sound production. If,

however, sound production by the lateral lip of the

nasal plug is considered separately, some interesting

possibilities appear. The lip of the nasal plug and

the adjacent structures are larger on the right,

which might render them more suitable for sound

production.

Lawrence and Schevill (1956) presented some

interesting data relevant to the functioning of the

large nasal plug on the right side. They observed

an asymmetry in the opening and closing of the

blowhole, with the left side opening earlier than

the right. Their sequential photographs of blowhole movements also indicate that the left passage

opens wider than the right. In some of their photos

it is possible to see straight down into the bony

nasal passage on the left side, while the right side

is always slightly occluded by the nasal plugs. I

would suggest that this is due both to the greater

size of the lips of the nasal plug on the right, and

to the invasion of the nasal plug muscle by the

melon on that side, rendering it less effective as a

retractor of the plugs. It does seem clear that the

right nasal passage is less effective than the left

during ventilation. This implies that the modifications on the right side must be of sufficient functional importance to offset the respiratory disadvantage incurred.

Norris et al. (1971) noted asymmetric activity in

the blowhole during production of squeals in

Stenella longirostris. In this case, the left side was

active, while the right side appeared quiet. They

suggested the possibility that the left side is primarily involved in low-frequency sound production, while the right side may be specialized for the

production of clicks. However, if movement of air

through the larynx is involved in low-frequency

sound production, as suggested by several workers,

it would be reasonable to expect movement of air

primarily through the less specialized left naris, as

in respiration.
NUMBER 207 53

Taking all of the preceding arguments into

account, I believe that at some point in cetacean

evolution, the nasal plugs, which probably originally developed as valves, became involved in

sound production. As a result of the mechanism of

sound production it became advantageous to increase their size. This, however, had an adverse

effect on ventilation, so that one passage became

specialized for vocalization, while the other remained as a respiratory pathway. Consequently the

blowhole was shifted slightly, to lie more directly

over the respiratory side.

A larger nasal plug requires a larger posterolateral area in the premaxillary sac to accommodate

it. As the premaxillary sac is intimately related to

the ascending process of the premaxilla, this

accounts for that portion of the bony asymmetry.

This also explains the shift to the left in the aperture of the bony nasal passage. The increase in the

size of the other deep diverticula may be related

to their function as air reservoirs, reflecting elements, or to direct involvement in sound production.

It must be borne in mind that the acoustic functioning of the structures in the odontocete head is

still poorly understood. While I have emphasized

the possible role of asymmetry in differences in

sound quantity, it may equally well be involved in

differences in sound quality (e.g., sound of a higher

frequency may be differentially produced on one

side, or the asymmetry may affect generation of

harmonics).

Summary of Facial Complex Function

NASAL DIVERTICULA

The nasal diverticula probably function both as

air reservoirs during phonation and as sound

reflectors serving to direct the sound field anteriorly. The exact relationships of these functions

are not known, but it seems likely that the vestibular sac serves as both a receptable for air and

as one of the principal reflectors. The premaxillary

sac may serve as a source of air during phonation.

The nasofrontal sac is more of a problem. In

most delphinids it appears to be too small to be

particularly important as either a reservoir or a

reflector. In these animals its primary function may

be that suggested by Lawrence and Schevill (1956),

as a partial pneumatic seal of the nasal passage

above the level of the nasal plugs. In Lagenorhynchus this diverticulum has been greatly enlarged

and may be of considerable importance as both a

reservoir and a reflector. In Grampus, where the

anterior portion of the nasofrontal sac is absent

on the left, its effectiveness as a pneumatic seal is

impaired. The enlarged right-hand portion, however, may be more effective as a reservoir or

reflector.

The function of the accessory sac is difficult to

ascertain, as it appears to be inconsequential due

to its small size. If the source of sound is close to

this diverticulum, as is hypothesized, then it may

be important as a reflector of sound which would

otherwise radiate laterally.

The lateral premaxillary diverticulum of Lagenorhynchus and Lagenodelphis probably serves

principally to increase the volume of the premaxillary sac, substantiating the role of the latter as an

air reservoir.

The pronounced directionality observed in the

delphinid sound field necessitates the presence of

an effective focusing mechanism. At the moment

it seems likely that this is accomplished at least in

part by reflection from the nasal diverticula.

NASAL MUSCULATURE

The larger nasal muscles (pe, i, ae, pi, and ai)

open and close the nasal passage at various levels,

a function important both in respiration and sound

production. The more superficial of these muscles

(pe, i, ae, and to a certain extent pi) effect closure

above the level of the nasal plug. Pi and at also

serve to seat the nasal plugs in the orifice of the

bony nasal passage. Ae and a small anterior portion of at are functional in opening the nasal

passage. This is in marked contrast to the interpretation of Schenkkan (1973), that the musculature

functions only to open the nasal passages.

The nasal plug muscle serves both to withdraw

the nasal plugs from the aperture of the bony nasal

passage during respiration and possibly to effect

complex movements of the nasal plugs during

phonation.

The role of the intrinsic musculature is very

poorly understood. It is capable of altering the

configuration of the posterior portion of the nasofrontal sac, but in which functions this would be

important is unknown. The diagonal membrane
54

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

muscle is possibly active during phonation, serving

to change the tension of the diagonal membrane

and thus to alter its contact with the nasal plug.

OTHER STRUCTURES

Both the nasal plug and the diagonal membrane

have been implicated in sound production. They

also serve to close the nasal passage at the lower of

the bony nares. The blowhole ligament provides

stability in the relationships of the deep structures,

principally the apertures of the nasofrontal and

accessory sacs. It is also important in providing a

surface against which the nasal plug fits to close

the nasal passages.

The melon is probably an acoustic channel, providing a path of minimum resistance for sound

passing in an anterior direction. The rostral musculature may be involved in movements of the lips

or may be related in some obscure way to sound

transmission.

Experimental Approaches

As stated earlier in this paper, none of the

experimental data currently available allows correlations to be made between structure and function.

It is most important to obtain comparative data

which will allow such parameters as shape of the

sound field to be correlated with differences in

anatomy of the facial complex. This will provide

information of the structures important in shaping

the sound field. It should also be ascertained

whether the shape of the sound field is capable of

being actively altered by the animal. To a lesser

extent, comparative data on the frequency range

of sound production may allow correlations to be

made with anatomical differences.

The nasal complex appears to be suitable for

investigation by electromyography. Simultaneous

synchronized recording of muscular activity and

both vocalization and respiratory movements

would provide evidence on the function of the

various components of this complex. These techniques could also be useful coupled with cineradiography, such as used by Norris et al. (1971).

To a lesser extent, the nasal structures may be

modified experimentally in order to see what effect

this would have on sound production. Perhaps the

most useful approach here would be to fill the

various diverticula with some inert substance, such

as silicone rubber, which would alter both their

functioning as reservoirs and reflectors. Surgical

alteration of these elements has the drawback of

introducing the element of trauma and thus rendering the conclusions suspect.

In any of these approaches it would be useful

to obtain information from as wide a morphologic

range as possible. Data on the phocoenids would

be of particular interest, as their nasal structure is

considerably different from that of the delphinids.

PHYLETIC RELATIONS OF THE DELPHINIDAE

Relationships within the Delphinidae

The classification of odontocetes used in this

paper is essentially that of Simpson (1945), with

the suprageneric groupings of Fraser and Purves

(1960). Peponocephala has been placed in the Delphininae on the basis of osteological resemblances

of Lagenorhynchus, but its position here is still

subject to question. Peponocephala electra was formerly placed in the genus Lagenorhynchus (True,

1889). Within the family Delphinidae, as used here,

there are five subfamilies: Delphininae, Orcininae,

Lissodelphinae, Cephalorhynchinae, and Steninae.

On the basis of osteological characters the Delphinidae is generally felt to constitute a coherent assemblage. The arrangement of Delphinids into subfamilial groups is a fairly recent development.

Slijper (1936) made one of the better attempts to

establish groups of genera within the Delphinidae,

and recognized that a distinction needed to be

made between the delphinines and the orcinines.

Fraser and Purves (1960) provided the most wellfounded grouping of delphinid genera, based upon

characters of the ventral portion of the skull.
NUMBER 207 55

I have found that, in general, the delphinids are

fairly conservative in their facial anatomy. Thus, I

have found no characters which consistently separate the Orcininae and the Delphininae, the only

two subfamilies for which I have had extensive

material. Nor do the subfamilies Steninae and

Lissodelphinae, for which there is comparative

data, present any major differences from these

delphinids. The Cephalorhynchinae, as represented

by Cephalorhynchus hectori, seem quite distinct

from the other delphinids in terms of facial morphology. In the following discussions involving the

relationships of various genera, it must be borne

in mind that in some of these all of the species

have not been examined and the conclusions are

therefore somewhat tentative.

Within the Delphinidae, Tursiops appears to be

a conservative, generalized animal, and can be

related with equal facility to all but the most divergent species. Within the subfamily Delphininae it

is structurally most similar to Stenella and DelFIGURE 21.—Phyletic relationships of the delphinid genera

examined in this study, based upon both data from the

facial anatomy and from the literature.

phinus. The relationships of the species in this

group of three genera have been examined by

Fraser and Purves (1960) and Mitchell (1970).

They agree that Tursiops is the most generalized

of this series, and Delphinus is the most specialized.

The interrelationships of the numerous species of

Stenella are uncertain at this time. Mitchell (1970)

has suggested that S. attenuata and S. longirostris

are the most generalized of this group, so far as

external pigmentation is concerned, and that the

other species may represent divergent specializations. The data from facial anatomy indicate that

the Stenella species form a closely related group,

with only one of the species examined being unusual. Stenella coeruleoalba differs from the other

Stenella species in a number of features of the

nasal diverticula. It thus appears to be the

only member of the Tursiops-Stenella-Delphinus

group which has diverged on the basis of nasal

specializations.

In addition to the Stenella species group, there

is a large group of species gathered into the genus

Lagenorhynchus. Of the four species for which

information is available, three (L. acutus, L. obliquidens, and L. obscurus) are essentially similar to

Tursiops in facial morphology, while the fourth

(L. albirostris) differs in development of the nasal

diverticula. A number of authors (True, 1889;

Fraser, 1966; Fraser and Purves, 1960; Mitchell,

1970) have suggested that L. obscurus is similar in

many ways to Stenella, and it may be the most

generalized of the Lagenorhynchus species, while

L. albirostris may be the most specialized.

Lagenodelphis should probably be grouped with

the Lagenorhynchus species, as it shows a resemblance to L. albirostris in its facial anatomy, and

differs from the rest of the delphinids in this point.

Fraser (1956), in the initial description of Lagenodelphis, suggested not only a relationship to

Lagenorhynchus, but also to Delphinus and

Stenella.

Grampus seems to be closely related to Tursiops

in osteological characters, structure of the pterygoid air sinuses (Fraser and Purves, 1960), and the

existence of possible hybrids (Fraser, 1940). It is

quite different from Tursiops in its facial anatomy,

and I would be tempted to put it in a subfamily

by itself if not for the data relating it to Tursiops.

There is no anatomical information available

for Peponocephala, which seems to represent a
56 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

development toward a bulbous-headed form from

the Lagenorhynchus group.

The Orcininae appear to form a natural group

on the basis of development of the pterygoid air

sinuses (Fraser and Purves, 1960), but specific relationships within this subfamily are not clear. Fraser

and Purves suggested that Pseudorca, Orcinus, and

Orcaella formed a "natural sequence of specialization," while Feresa and Globicephala showed certain resemblances to one another and to Orcinus.

Mitchell (1970) suggested a slightly different

arrangement, with Feresa and Orcinus forming one

group, Globicephala, Orcaella, and Pseudorca

forming another. Anatomical data is available only

for the three genera which I dissected, Orcinus,

Pseudorca, and Globicephala. Orcinus appears to

be a very generalized delphinid, which has attained

a large size and has become specialized for feeding

on large prey. The melon is relatively small and

structures posterior to it show no specializations.

Pseudorca is similar to Orcinus (and to Tursiops,

for that matter), except in the development of a

large, elongate connective tissue mass on the forehead external to the melon. As described earlier,

there is no increase in the size of the melon, and it

is thus quite different from both Grampus and

Globicephala. Globicephala has developed a similar layer of thick dermal connective tissue, but

has greatly enlarged the melon as well. In addition,

Globicephala shows some specializations in the

nasal diverticula, separating it from the rest of the

orcinines.

Information is available for only one species of

the Cephalorhynchinae, Cephalorhynchus hectori.

The anterior portions of the nasofrontal sacs are

extremely large, somewhat similar to the condition

seen in the Lagenorhynchus albirostris specimen

which I dissected. Cephalorhynchus hectori differs

markedly, however, in that the left nasofrontal sac

is by far the larger, whereas the right is larger in

all other delphinids for which there is information.

Cephalorhynchus hectori was also unusual in that

the fatty tissue of the melon did not penetrate the

right nasal plug as it does in most delphinids.

Cephalorhynchus is clearly different from the

other delphinids in a number of other characters,

such as details of the skull, postcranial skeleton,

and external body form. In some of these it shows

resemblances to phocoenids, and may in fact be

somewhat convergent upon them.

The Lissodelphinae (consisting only of the two

species of Lissodelphis) show no particular specializations from the general delphinid facial morphology and are separated on the basis of their peculiar

elongate body form. In general cranial characters

they are perhaps most similar to Lagenorhynchus

and may represent a locomotory specialization from

an origin near that genus.

The data available for the Steninae indicate a

generalized facial morphology, essentially similar

to that of Tursiops. Dohl et al. (1974) reported a

viable hybrid between Tursiops sp. and Steno

bredanensis, suggesting a fairly close genetic relationship between these genera.

Relationships to Other Families

In the structure of the face the Phocoenidae are

as different from the delphinids as are any of the

nonphyseteroid odontocetes. This is manifest in the

form of the vestibular sac and the greater complication of structures around the inferior vestibule.

The Monodontidae also represent a divergent

group, with Monodon appearing to be more specialized facially than Delphinapterus. In some

respects the monodontids resemble the phocoenids,

and may actually be more closely related to that

group than to the delphinids. The details are

unclear, however, and more work is needed to

establish the degree of relationship of these two

genera to one another and to the other delphinoid

families.

The data available for the Platanistidae suggest

that this is a very heterogeneous grouping of

genera. They have been grouped in a variety of

ways in different systems of classification, perhaps

the most soundly based being that of Fraser and

Purves (1960) in which Inia and Lipotes are

grouped together. There is some indication, however, that Lipotes and Pontoporia are related in

facial structure (Hinton, 1936). There seems to be

general agreement that Platanista is not particularly related to the other genera, largely on the

basis of facial characters. The relationship of the

Platanistidae to the Delphinidae is uncertain, but

does not appear to be very close.

Very little data is available for the Physeteridae,

and that which exists is sometimes contradictory.

Physeter and Kogia are very different from one
NUMBER 207

57

Relationships of Bulbous-headed Delphinids

GENERAL CONSIDERATIONS

Bulbous-headed species have developed independently in a number of odontocete groups. In

these animals some portion of the facial apparatus

has become hypertrophied, resulting in a bulbous

appearance of the forehead.

In the delphinines, Grampus represents an extreme development of this type, while Peponocephala shows a slight hypertrophy of this area.

Hypertrophy of the facial structures is common in

the orciniines, all members of this subfamily except

Orcinus showing it to a certain extent. In none of

the other delphinids, however, is this condition

developed.

Among the nondelphinid odontocetes, several

groups show hypertrophy of the facial elements.

The monodontids are quite bulbous-headed, as are

some of the ziphiids (Hyperoodon and Berardius).

Although facial structures in the platanistids

appear to be extremely complicated, none of them

have developed a bulbous forehead. One phocoenid, Neophocaena, should probably be included in

the category of bulbous-headed animals. Both of

the physeterid genera show extreme hypertrophy

of this area, but in a manner totally unlike that of

the other odontocetes.

FIGURE 22.—Phyletic relationships of the suprageneric groups

of odontocetes. (Based upon both data from the facial anatomy and from the literature.)

another, but appear to be even more different from

the rest of the odontocetes, and bear no particular

relationship to the delphinids.

The Ziphiidae are another unusual group whose

relationships are not clear. They are commonly

grouped with the Physeteridae, though the evidence

for this relationship is tenuous. The scanty information on ziphiid facial anatomy (Schenkkan,

1973) indicates a morphology more comparable to

delphinids than to physeterids, but still quite different from either. Relationships within the

Ziphiidae are equally unclear.

Globicephala

Tursiops

most othe

delphinids

small large

Melon Size

FIGURE 23.—Structural relationship of the bulbous-headed

delphinids, according to which portion of the rostral tissues

has become hypertrophied.
58

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Of the bulbous-headed odontocetes, I have

examined material of three of the delphinids,

Grampus, Globicephala, and Pseudorca.

If the structures of the facial region are examined, two principal elements are seen to be involved

in this hypertrophy: (1) the melon and (2) the

dermal connective tissue overlying the melon. A

coordinate system can be devised, as in Figure 23,

in which the relative degree of hypertrophy of

these elements can be presented graphically. In

this graphic system the bulk of the delphinids, in

which the facial structures are not hypertrophied,

fall near the origins of the axes. Any displacement

in a positive direction along these axes represents

development toward bulbous-headedness. It can be

seen from this graph that the three animals examined represent the three possible extremes of development of these characters. Presumably, when the

other bulbous-headed odontocetes are examined

they will occupy intermediate positions in this

system. Physeterids must be excluded from these

considerations, as they do not appear to be comparable to other odontocetes in these characters.

COMPARISON OF Pseudorca, Globicephala, AND

Grampus

The general shape of the head differs considerably among these animals. In Pseudorca (Figure

26) the facial mass is enlarged anteriorly, retaining

a more or less streamlined configuration. In Globicephala (Figures 18, 26) the enlargement takes

place both anteriorly and dorsally, producing an

extremely protuberant forehead (hence the common name "pot-head," which is sometimes applied

to this animal). In Grampus (Figures 12, 25),

enlargement is mainly in a dorsal direction, resulting in a high forehead, which slopes steeply down

to the tip of the rostrum. In addition, there is a

median sulcus on the anterior portion of the forehead of Grampus (Figure 12), resulting in a distinctly bilobed external surface.

As is indicated in Figure 23, the relative degree

of hypertrophy of the anterior facial elements differs among these three animals. In Pseudorca only

the dermal connective tissue is hypertrophied,

while in Grampus only the melon is involved. In

Globicephala, which has by far the largest forehead

mass, both of these elements have increased in size.

As a result, the consistency of the forehead is different in these animals. In Pseudorca and Globicephala, in which the dermal connective tissue is

very thick, the forehead mass is extremely firm and

resilient. In Grampus, on the other hand, the

forehead is quite soft. In this connection it is

interesting to note that a prominent feature of the

behavior of Globicephala is head-butting (Kritzler,

1952; Brown, 1962). This appears to be connected

with mating behavior. Comparable data are not

available for Pseudorca and Grampus, but it might

be expected on the basis of anatomical similarities

that Pseudorca would engage in this behavior,

while Grampus would not.

The nasal diverticula present some interesting

modifications in these animals. The vestibular sacs

are not remarkably different from those of the

other delphinids, but lie consistently somewhat

more posterior to the nasal passage. The nasofrontal

sacs of Pseudorca are similar to those of Tursiops,

while Grampus and Globicephala are markedly

different. In Grampus the anterior portion of the

right nasofrontal sac is extremely large, while that

of the left is absent. In Globicephala the general

size and shape are not peculiar, but there is an

unusual trabeculate sacculation on the angle of the

right sac. None of these modifications of the nasofrontal sac, however, appear to be related to the

hypertrophy of the anterior structures. The remainder of the diverticula in all three animals are

not notably different from those of Tursiops.

In the musculature, as in the diverticula, Pseudorca is similar to Tursiops, while Grampus and

Globicephala present what appear to be independent specializations. In Grampus, pe is different

from the condition seen in Tursiops, while in Globicephala it is pi which has been modified.

The degree of cranial asymmetry does not appear

to be related to development of a bulbous forehead.

In fact, Globicephala is unusual in being one of

the two known delphinids in which the melon does

not invade the right nasal plug.

These three animals clearly represent independent developments of enlarged facial structures

In most respects Pseudorca is conservative, while

Grampus and Globicephala represent extreme conditions. Very little information is available on the

natural history of these animals, making it difficult

to correlate facial hypertrophy with behavior or

ecology. It is interesting to note that both Globi-
NUMBER 207

59

dct

a Tursiops

ct

Stenella

d c t

Lagenorhynchus

FIGURE 24.—Diagrammatic views of the nasal diverticula and melon. Tursiops truncatus: a,

lateral view; b, dorsal view. Stenella attenuata: c, lateral view; d, dorsal view. Lagenorhynchus

albirostris: e, lateral view; /, dorsal view, (as = accessory sac, dct=dermal connective tissue, lps =

lateral premaxillary sac, m = melon, npm = nasal plug muscle, ns = nasofrontal sac, ps = premaxillary sac, vs = vestibular sac).
60

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

dct

Lagenodelphis

dct

Grampus

dct

Orcinus

FIGURE 25.—Diagrammatic views of the nasal diverticula and melon. Lagenodelphis hosei: a,

lateral view; b, dorsal view. Grampus griseus: c, lateral view; d, dorsal view. Orcinus orca:

e, lateral view; /, dorsal view. (as=accessory sac, dct=dermal connective tissue, lps=lateral

premaxillary sac, m=melon, npm = nasal plug muscle, ns=nasofrontal sac, ps=premaxillary

sac, v = vestibular sac.)
NUMBER 207 61

Pseudorca

Globicephala

FIGURE 26.—Diagrammatic views of the nasal diverticula and melon. Pseudorca crassidens: a,

lateral view; b, dorsal view. Globicephala melaena: c, lateral view; d, dorsal view. (as=accessory sac, dct=dermal connective tissue, lps=lateral premaxiliary sac, m=melon, npm=nasal

plug muscle, ns=nasofrontal sac, ps=premaxiliary sac, vs=vestibular sac.)

cephala and Grampus feed preferentially on squid,

as do a number of other bulbous-headed animals

(ziphiids, physeterids, and Monodon) (Tomilin,

1967). Pseudorca frequently feeds on cephalopods,

but it also takes large quantities of fish, while

Delphinapterus differs from the above forms in

feeding predominantly on fish. The extreme hypertrophy of the anterior facial elements may be in

some way correlated with a cephalopod diet, or it

may merely be due to coincidence.

ORIGIN OF THE ODONTOCETE NASAL APPARATUS

The nose of most mammals is a relatively complex organ, and there is no reason to assume that

the nose of the terrestrial ancestor of the cetaceans

was any less complex than that of an ordinary dog

or cat. It was probably provided with a series of

muscles (of the maxillonasolabialis group) capable

of constriction and dilation of its orifice according

to the ordinary needs of terrestrial animals. During

the course of evolution from such a terrestrial

ancestor to the completely aquatic Cetacea, there
62

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

should have been little difficulty in adapting the

nose to fit the altered needs of an aquatic existence.

Mere exclusion of water from the nasal passages

appears to present very little problem, and has been

accomplished many times by aquatic and semiaquatic vertebrates. The skull of the early archaeocetes does not indicate any special modifications in

the nasal apparatus.

Elaboration of the soft tissues of the nose in

cetaceans seems to have occurred after the separation of the lines leading to mysticetes and odontocetes. As noted in the introduction, the nose of the

former is relatively simple and presents little in

the way of modification from what was probably

the primordial mammalian plan. Odontocetes, however, have drastically modified the structure of the

nose. If such modifications are not necessary to

exclude water from the nasal passages, as is evident

from their absence in other aquatic mammals, then

they are connected with some other function of

the respiratory passages, in this case probably

sound production.

The production of sound in mammals normally

involves movement of air through the larynx. If

this takes place underwater, where the animal cannot replenish its air supply, provisions must be

made to prevent the loss of air through the nostrils.

This movement of air results in an increase of

pressure in that portion of the respiratory system

distal to the larynx, proportional to the ratio of the

volume of air used in phonation to the volume of

the distal portion of the respiratory system. The

pressure thus produced tends to force air through

the nostrils, and poses a problem entirely different

from that of excluding water from the nasal passages. One approach to this problem is to increase

the capability of the nostrils to retain air under

pressure, the other is to increase the volume of the

distal air reservoir (assuming that the means of

sound production has not altered in order to

utilize a smaller volume of air in the production

of sound).

Odontocetes appear to have approached this

problem from both ways. The nasal musculature

has greatly increased in size, making it possible for

the animal to close the nasal passages effectively,

and at several different levels. They have also

developed a series of diverticula, expanding the

volume of the reservoir available for storage of air.

The mammalian nose seems to readily develop such

diverticula in response to changing needs of the

animal, as they are seen in a great variety of modern mammals. Anthony (1926) discussed the question of the homology of the nasal diverticula in

cetaceans with those of other mammals, and concluded that they are most comparable to those of

perissodactyls. Cetacea, however, seem to bear no

other particular resemblance to perissodactyls, and

there seems to be no reason to assume that the

odontocete nasal diverticula were not developed

de novo (particularly in consideration of their

absence in mysticetes). It is easy to imagine that

any increase in the volume of the distal portion of

the nasal passage would prove of value to the early

odontocetes and might lead to the development of

a diverticulum. Norris (1968) has also suggested

that the diverticula were an early development

related to sound production.

The point might be raised that, since mysticetes

are known to utilize underwater sound production,

such a system would be advantageous to them, but

is seen to be lacking. The difference between the

two major divisions of living whales, in the structure of the noses and the larynx, suggest that

specialized underwater phonation was probably

developed independently by each. Mysticetes have

always been large animals, and it may well be that

the initial volume of the nasal passage was sufficient for retention of air during vocalization.

Once the nasal diverticula have developed, for

whatever initial reasons, they will become effective

reflectors of sound when filled with air. It seems

likely that this has been utilized to some advantage

by the odontocetes, and may now be one of the

principal functions of these diverticula. This same

line of reasoning is applicable to the possible function of the nasofrontal sac in pneumatic closure

of the nasal passage.

The origin of the melon is a more difficult problem. Schenkkan (1972) stated that the melon is a

"degenerate, hypertrophied part of the musculus

maxillolabialis." Purves and Pilleri (1973) elaborated this view somewhat, suggesting that the

melon was initially a fibrous structure derived by

"hypertrophy of the tendinous origin of the maxillolabialis," and that the fatty melon seen in most

odontocetes represents a degeneration of this

condition.

One of the critical problems in understanding

the origin of the melon is our lack of understand-
NUMBER 207 63

ing of its function. It seems clear that it is structurally related to the insertion of the medial

portion of the rostral muscle (which is equivalent

to part of the m. maxillolabialis as used by the

above authors), but its functional relationship to

this muscle is uncertain. At this point it is not

possible to decide whether the musculature as such

was once more extensive and the melon developed

through fibrous or fatty degeneration of the muscle,

whether it developed as a fibrous or fatty addition

to the muscle, or whether in fact the medial portion of the rostral muscle was absent primitively

and developed along with a fibrous or fatty structure in this area.

The possible relation of cranial asymmetry to

sound production raises some interesting evolutionary possibilities. If extra-laryngeal sound production in modern odontocetes is connected with

cranial asymmetry, as suggested earlier in this

paper, this gives us a functional character which

can be traced back into the fossil record. A cursory

examination of the data available for fossil odontocetes indicates that many of the Miocene forms

show cranial asymmetry similar to that of the

living delphinids, and they may therefore have

possessed a similar acoustic system. The nature of

the fossil material is such, however, that a detailed

study is necessary to demonstrate the extent of the

cranial asymmetry in the early forms.

There is, however, a comparative anatomical

approach to the question of the origin of the modern odontocete acoustical system. The fact that the

cranial asymmetry in all of the odontocetes involves

a displacement of the nares to the left suggests

that this cranial asymmetry was present in a common ancestor. This raises the possibility that some

of the very early odontocetes utilized the nasal

apparatus for sound production and had reached

a level of specialization where one passage was

dominant in this role. Whether or not echolocation

was involved is something which we probably can

never determine. It does suggest, however, that

sound production was important and formed one

of the bases for the differentiation of the odontocetes from the mysticetes and from the more archaic

cetaceans.
Appendix 1

CLASSIFICATION OF THE ODONTOCETES (TOOTHED WHALES)

Order Cetacea Brisson, 1762

Suborder Odontoceti Flower, 1867

Superfamily Physeteroidea Gill, 1872

Family Physeteridae Gray, 1821

Subfamily Physeterinae Flower, 1867

Physeter Linnaenus, 1758 [sperm whale]

Subfamily Kogiinae Gill, 1871

Kogia Gray, 1846 [pigmy sperm whales]

Family Ziphiidae Gray, 1865

Mesoplodon Gervais, 1850 [beaked whales]

Ziphius Cuvier, 1823 [Cuvier's beaked whale]

Tasmacetus Oliver, 1937 [Shepherd's beaked whale]

Berardius Duvernoy, 1851 [giant bottlenose whales]

Hyperoodon Lacepede, 1804 [bottlenose whales]

Superfamily Platanistoidea Simpson, 1945

Family Platanistidae Gray, 1863

Subfamily Platanistinae Flower, 1867

Platanista Wagler, 1830 [Susu]

Subfamily Iniinae Flower, 1867

Inia D'Orbigny, 1834 [Boutu]

Lipotes Miller, 1918 [white flag dolphin]

Subfamily Stenodelphininae Miller, 1923

Pontoporia Gray, 1846 [franciscana]

Superfamily Delphinoidea Flower, 1864

Family Monodontidae Gray, 1821

Monodon Linnaeus, 1758 [narwhal]

Delphinapterus Lacepede, 1804 [beluga]

Family Phocoenidae Bravard, 1885

Phocoena Cuvier, 1817 [harbor porpoises]

Phocoenoides Andrews, 1911 [Dall's porpoise]

Neophocaena Palmer, 1899 [finless porpoise]

Family Delphinidae Gray, 1821

Subfamily Delphininae Slijper, 1936

Delphinus Linnaeus, 1758 [common dolphin]

Stenella Gray, 1866

Grampus Gray, 1828 [Risso's dolphin]

Tursiops Gervais, 1855 [bottlenose dolphin]

Lagenorhynchus Gray, 1846

Lagenodelphis Fraser, 1956 [Fraser's dolphin]

Peponocephala Nishiwaki and Norris, 1966 [melonheaded whale]

Subfamily Orcininae Sliiper. 1936

Orcinus Fitzinger, 1860 [killer whale]

Pseudorca Reinhardt, 1862 [false kiler whale]

Globicephala Lesson, 1828 [pilot whale]

Orcaella Gray, 1866 [Irrawaddy dolphin]

Teresa Gray, 1870 [pygmy killer whale]

Subfamily Steninae Fraser and Purves, 1964

Steno Gray, 1846 [rough-toothed dolphin]

Sotalia Gray, 1866 [tucuxi]

Subfamily Lissodelphinae Fraser and Purves, 1964

Lissodelphis Gloger, 1841 [right whale dolphins]

Subfamily Cephalorhynchinae Fraser and Purves, 1964

Cephalorhynchus Gray, 1846

64
Appendix 2

TABLES

TABLE 1.—Nomenclature of nasal structures

Present

study

Lawrence and

Schevill, 1956

von Baer,

1826

Murie,

1870, 71, 73

Gruhl, 1911 Anthony, 1926 Huber, 1934 Moris, 1969

vestibular

sac

nasofrontal

sac

accessory

sac

premaxillary

sac

Inferior

vestibule

spiracular

cavity

pe

1

vestibular

sac

tubular

sac

connecting

sac

premaxillary

sar

nasal passage

(constriction

slit)

pe

1

ae, pi

a i , pr

spritzsacke

hintere obere

hflhle; vordere

obere hBhle

vordere

untere hBhle

gemeinschSftliche hBhle

— -

maxillary

sac

nasofrontal

sac

premaxillary

sac

nasal passage

occipitofrontal is

several

?pyranidal1s

depressor

all nasi

spritzsacke

haupthflhle

blind sicke

vorderd

untere hUhle

pars

superficial

pars

profunda

diverticule

lateral

diverticule

diverticule

anterleur

lateral sac

nasofrontal

premaxillary

sac

sac paranasal

superieur

sac paranasal

sac paranasal

moyen?

sac nasal

anterleur

sac paranasal

moyen?

pars nasal is

muscle evental,

plan superieur

muscle evental,

plan moyen

'Levator labii superioris alaeque nasi, zygoraaticus, levator superioris

proprius.

TABLE 2.—Muscle weight ratios (right/left) for species of Stenella (pe = pars

posteroexternus; ae = pars anteroexternus; pi = pars posterointernus; ai = pars

anterointernus; vest, sac = vestibular sac; total muse. = total musculature;

x = mean)

s.

s.

s.

s.

£•

s.

Species

attenuata

attenuata

lonairostris

longirostris

plagiodon

caeruleoalba

Sex

H

n

H

>t

H

M

M

M

F

F

F

F

F

M

F

F

F

F

F

F

M

M

Specimen

No.

WFP 48

WFP 49

WFP 51

WFP 56

WFP 77

WFP 81

JSL 91

JSL 92

X =

WFP 55

WFP 66

WFP 73

WFP 78

JSL 96

X =

WFP 47

WFP 54

WFP 57

WFP 58

WFP 74

WFP 79

WFP 80

X -

EOM 844

EDM 845

WFP 50

Pe

0.87

1.37

1.17

1.31

1.10

1.18

0.96

1.11

1.13

1.37

1.24

1.54

2.09

1.42

1.53

0.78

0.72

1.19

1.44

1.22

0.97

0.99

1.09

-

0.91

0.86

Ae

_

0.92

0.94

0.82

0.86

0.82

0.94

1.07

0.91

1.08

0.93

0.85

0.79

1.14

0.96

0.94

1.00

1.08

1.08

0.95

0.91

0.87

fl.98

0.95

1.01

1.23

Pi

.

0.72

1.31

2.34

1.22

1.44

0.82

1.04

1.27

1.08

0.92

1.09

1.55

0.71

1.07

1.27

0.70

1.35

2.63

0.66

1.14

0.78

1.21

1.55

1.21

0.64

Ai

.

1.24

1.09

1.15

1.01

1.18

0.97

1.08

1.10

1.03

1.12

1.03

1.09

0.86

1.03

1.08

1.26

1.10

0.96

1.18

1.22

1.20

1.15

1.03

0.88

1.23

Vest.

Sac.

1.0

0.83

0.86

0.82

1.04

0.94

0.95

0.89

0.92

0.85

0.95

0.93

1.02

1.02

0.95

1.22

0.87

1.00

1.11

1.12

0.96

0.93

1.00

1.03

1.47

1.93

Nasal

Passage

1.47

1.26

1.38

1.68

1.56

1.47

1.50

1.47

1.67

1.26

-

1.37

1.43

-

1.38

1.64

1.47

1.50

1.28

1.51

-

total

%iSC.

.32

.07

.05

.08

3.99

.08

).95

.08

.08

.07

.09

.04

.07

1.98

.05

.01

.04

.10

.13

.03

.08

.02

.07

.04

.90

.13
66

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

TABLE 3.—Data on specimens examined (measurements in size column

are total lengths; specimen catalog numbers are from collection of

Division of Mammals, National Museum of Natural History)

Species

Cephalorhynchus hectori

Globicephala neiaena

Grampus griseus

In1a geoffrensis

Laqenodelphis hosei

Lagenorhynchus acutus

Laqenorhynchus albirostris

Orcinus orca

Phocoena phocoena

Phocoenoides dalU

Pontoporia blainvillei

Pstfudorca crassidens

•

Steneiia attenuata

•

" *

* *

Sex

m

•

f

•

f

m

f

in

f

f

.

f

•

m

HI

m

.

•

•

m

•

in

•

n

m

m

•

f

f

Size

110 cm

near-term fetus

575 cm

335 cm

adult

110 cm

adult

198 cm

177 cm

755 en

618 an

adult

adult

near-term fetus

adult

adult

128 cm

145 cm

146 cm

156 cm

157 cm

160 cm

163 cm

165 en

167 en

168 cm

172 cm

186 cm

190 cm

192 cm

197 cm

105 cm

l i e ca

Field Number

WAW 142

D180-71

Dl60-71

LR23

0119-71

Dl18-71

A0 42

JSL 87

JSL 88

JSL 91

WFP 59

UFP 81

UFP 77

JSL 92

JSL 94

UFP 56

UFP 62

JSL 90

JSL 93

UFP 48

UFP 51

UFP 49

JSL 86

JSL 97

USNM

Catalo q Number

500864

396079

485827

501200

396037

396175

396171

396034

396038

396027

396029

396028

Species

Stenella attenuata

»

„

Stenella coeruleoalba

Stenella lonqirostHs

Stenella plagiodon

Steno bredanensis

Tursiops truncatus

Sex

f

f

f

f

f

f

f

f

f

f

f

m

m

m

n

m

m

m

•

m

m

f

f

f

f

f

f

f

m

m

m

f

f

Size

122 cm

138 cm

145 cm

161 cm

165 cm

167 cm

179 en

185 cm

191 cm

200 cm

201 cm

214 en

236 cm

136 cm

154 cm

164 en

166 cm

Ifi9 cm

174 cm

175 cm

177 cm

129 cm

149 cm

163 cm

169 cm

178 cm

178 cm

179 cm

179 cm

189 cm

54 cm

adult

270 cm

Field Number

WFP 63

JSL 95

WFP 72

UFP 66

WFP 73

WFP 78

WFP 67

JSL 96

JSL 89

WFP 55

WFP 70

UFP 50

EDM 845

UFP 75

WFP 68

UFP 65

HFP 71

WFP 53

WFP 76

WFP 47

WFP 52

WFP 58

HFP 69

HFP 57

UFP 80

WFP 74

UFP 54

WFP 79

EDM 844

UFP 466

(fetus)

EDM 846

USiM

Catalog Nunber

396024

396018

396025

396172

396019

396033

396022

396169

396020

396017

396023

396031

396170

396026

396030

396036

396021

396035

396174

396168

396032

396173

504089
Literature Cited

Abel, O.

1902a. Les dauphins longirostres du Bolderien. Memoires

de Musee Royal d' Histoire Naturelle de Belgique,

2:97-199, 8 plates.

1902b. Die Ursache der Asymmetrie des Zahnwalschadels.

Sitzungsberichte der Kaiserliche Akademie der

Wissenschaften in Wein, Mathematische—naturwissenshaftliche classc, 3:510-526, 1 plate.

Ackman, R. G., C. A. Eaton, and C. Litchfield

1971. Composition of Wax Esters, Triglycerides and

Diacyl Glyceryl Ethers in the Jaw and Blubber Fats

of the Amazon River Dolphin (Inia geofjrensis).

Lipids, 6(2):69-77.

Allen, G. M.

1923. The Black Finless Porpoise, Meomeris. Bulletin of

The Museum of Comparative Zoology, 65 (7):233-

256, 3 plates.

Anderson, H. T. (Ed.)

1969. The Biology of Marine Mammals. 511 pages. New

York: Academic Press.

Anderson, J.

1878. Anatomical and Zoological Researches: Comprising

an Account of the Zoological Results of the Two

Expeditions to Western Yunnan in 1868 and 1875;

and a Monograph of the Two Cetacean Genera,

Platanista and Orcella. 985 pages, 85 plates. London: B. Quaritch.

Anthony, R.

1926. Les affinites des ce'tace's. Annales de I' Institut

Oceanographique, new series, 3(2):93-133, 1 plate.

Baer, K. E. von

1826. Die Nase der Cetacean erlautert durch Untersuchung der Nase des Braunfisches (Delphinus phocaena). Isis von Oken, 19:811-847, 2 plates.

Beddard, F. E.

1900. A Book of Whales. 320 pages. New York: G. P.

Putnam's Sons.

Benham, W.

1901. On the Anatomy of Cogia breviceps. Proceedings

of the Zoological Society of London, 2 (I):107-134,

4 plates, 2 figures.

Boas, J. E. von, and S. Paulli

1908. The Elephant's Head: Studies in the Comparative

Anatomy of the Organs of the Head of the Indian

Elephant and Other Mammals, Part I: The Facial

Muscles and the Proboscis. 38 pages, 19 plates.

Jena: Gustav Fischer.

Borri, C.

1931. L'asimmetria del cranio dei cetacei. Archivio Zoologico Italiano, 16:751-759, 4 figures.

Bouvier, E.

1889. Les ce'tace's souffleurs. 218 pages. These pre"sente"e

au concours d'aggre"gation, £cole Supe"rieure de

Pharmacie de Paris.

Brown, D. H.

1962. Further Observations in the Pilot Whale in Captivity. Zoologica, 47 (l):59-64, 2 plates.

Bullock, T. H., A. D. Grinnell, E. Ikenzono, K. Kameda,

Y. Katsuki, M. Nomoto, O. Sato, N. Suga, and K.

Yanagisawa

1968. Electrophysiological Studies of Central Auditory

Mechanisms in Cetaceans. Zietschrift fur Vergleichende Physiologie, 59(2): 117-156, 15 figures.

Burmeister, G.

1867. Descripcion de cuatro especies de Delfinides de la

costa Argentina en el Oceano Atlantico. Annales de

Museo Publico de Buenos Aires (Museo Argentino

de Ciencias Naturales), 1:367-445, 8 plates.

Caldwell, M. C, and D. K. Caldwell

1965. Individualized Whistle Contours in Bottle-nosed

Dolphins (Tursiops truncatus). Nature, 207(4995):

434-435.

Camper, D., and A. G. Camper

1820. Observations anatomiques sur la structure interieure

et le squelette de plusieurs especes de Cetaces. 218

pages, 2 figures, 53 plates. Paris: Dufour.

Carlsson, A.

1888. Zur Anatomie des Hyperoodon diodon. Kungliga

Svenska Vetenskapsakadamiens handlingar, 13(4):

3-25, 3 plates.

Carte, A., and A. Macalister

1868. On the Anatomy of Balaenoptera rostrata. Philosophical Transactions of the Royal Society of

London, 158:201-261, 4 plates.

Clarke, M. R.

1970. Function of the Spermaceti Organ of the Sperm

Whale. Nature, 228:873-874.

Cuvier, F.

1835-1836. Cetacea. Pages 562-594 in volume 1 of Todd's

Cyclopedia of Anatomy and Physiology.

Cuvier, G.

1797. Sur les narines des c<kace"s. Bulletin des Sciences,

Societe Philomathique de Paris, 2:26-29, 3 figures.

Danois, E.

1910. Recherches sur l'anatomie de la tete de Kogia

breviceps Blainv. Archives de Zoologie Experimental et Generate, series 5, 6:149-174, 4 plates.

1911. Description d'un embryon de Grampus griseus Gray.

Archives de Zoologie Experimental et Generate,

series 5, 8:399-420, 2 plates.

Dohl, T. P., K. S. Norris, and I. Kang

1974. A Porpoise Hybrid: Tursiops X Steno. Journal of

Mammalogy, 55(1):217-221, 1 figure.

Edgeworth, F. H.

1935. The Cranial Muscles of Vertebrates. 493 pages, 841

figures. London: University Press.

67
68

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Edinger, T.

1955. Hearing and Smell in Cetacean History. Monatsschrift fur Psychiatrie und Neurologie, 129:37-58.

Evans, W. E.

1967. Special Acoustic Problems in Cetacean Research,

General Discussion. Pages 395-398 in volume 2 of

Tavolga, editor, Marine Bio-acoustics. New York:

Pergamon Press.

1973. Echolocation by Marine Delphinids and One Species of Fresh-water Dolphin. Journal of the Acoustical Society of America, 54(1): 191-199, 7 figures.

Evans, W. E., and P. F. A. Maderson

1973. Mechanisms of Sound Production in Delphinid

Cetaceans: A Review of Some Anatomical Considerations. American Zoologist, 13:1205-1213, 8 figures.

Evans, W. E., and J. H. Prescott

1962. Observations of the Sound Capabilities of the

Bottlenose Porpoise: a Study of Whistles and

Clicks. Zoologica, 47 (3): 121-126, 6 figures, 4 plates.

Evans, W. E., W. W. Sutherland, and R. G. Beil

1964. The Directional Characteristics of the Delphinid

Sounds. Pages 353-372 in volume 2 of Tavolga,

editor, Marine Bio-acoustics. New York: Pergamon

Press.

Fisher, M. P.

1881. C£tac£s du Sud-Ouest de la France. Actes de la

Societe Linneene de Bordeaux, 35:1-219, 8 plates.

Fraser, F. C.

1940. Three Anomalous Dolphins from Blacksod Bay,

Ireland. Proceedings of the Royal Irish Academy,

45 (17):413-455, 7 plates.

1956. A New Sarawak Dolphin. Sarawak Museum Journal,

7:478-503, 5 plates.

1966. Comments on the Delphinoidea. Pages 7-31 in

Norris, editor, Whales, Dolphins and Porpoises.

Berkeley: University of California Press.

Fraser, F. C, and P. E. Purves

1960. Hearing in Cetaceans: Evolution of the Accessory

Air Sacs and the Structure and Function of the

Outer and Middle Ear in Recent Cetaceans. Bulletin of the British Museum (Natural History),

Zoology, 7(l):l-14O, 53 plates.

Frechkop, S.

1944. Notes sur les mammiferes, xxviii: Essai d' interpretation biologiquc de la structure des c^tac^s.

Bulletin du Musee Royal d'Historie Naturelle de

Belgique. 20(13):l-28, 15 figures.

Gallardo. A.

1913. Notas sobre la anatomi'a del aparto espiracular,

laringc y hioides de dos delfines: Phocaena dioptrica

Lahillc y Lagenorhynchus fitzroyi (Waterhouse)

Flower. Annales de Museo Nacional de Historia

Xatural de Buenos Aires (Museo Argentino de

Ciencias Naturales), 24:235-246, 9 plates.

Gray, J.

1936. Studies in Animal Locomotion. VI: The Propulsive Powers of the Dolphin. Journal of Experimental Biology, 13:192-199, 3 figures.

Gruhl, K.

1911. Beitrage zur Anatomie und Physiologie der Cetaceennase. Jenaische Zeitschrift fur Naturwissenschaft, 47 (3):367-4l4, 21 figures.

Heel, D. van.

1970. Dolfijn, hoe doe je het? 158 pages, 8 plates. Amsterdam: Van Kampen & Zoon.

Hinton, M.

1936. Some Interesting Points in the Anatomy of the

Freshwater Dolphin Lipotes and Its Allies. Proceedings of the Linnean Society of London, 148(3):

183-185.

Hinton, M., and W. Pycraft

1922. Preliminary Note on the Affinites of the Genus

Lipotes. Annals and Magazine of Natural History,

10:232-234.

Hosakawa, H.

1950. On the Cetacean Larynx, with Special Remarks on

the Laryngeal Sacs of the Sei Whale and the

Aryteno-epiglottideal Tube of the Sperm Whale.

Scientific Reports of the Whales Research Institute,

3:23-62, 12 figures.

Houssay, F.

1912. L'asymetrie du crane chez les c£tac£s et ses rapports avec la loi de l'action et de la re-action.

Analomische Anzeiger, 36:12-17.

Howell, A. B.

1925. Asymmetry in the Skulls of Mammals. Proceedings

of the United States National Museum, 67 (27): 1-18,

8 plates.

1927. Contribution to the Anatomy of the Chinese Finless Porpoise, Neomeris phocaenoides. Proceedings

of the United States National Museum, 70(13):l-43,

14 figures, 1 plate.

1930. Aquatic Mammals: Their Adaptations to Life in

the Water. 338 pages, 53 figures. Baltimore: Charles

C. Thomas.

Huber, E.

1930. Evolution of Facial Musculature and Cutaneous

Field of Trigeminus. Quarterly Review of Biology,

5:133-187, 389-437, 46 figures.

1934. Anatomical Notes on Pinnipedia and Cetacea.

Pages 105-136 in E. L. Packard, R. Kellogg, and

E. Huber, Marine Mammals. Carnegie Institute of

Washington, Contributions to Paleontology, number 447.

Hunter, J.

1787. Observations on the Structure and Oeconomy of

Whales. Philosophical Transactions of the Royal

Society of London, 77:371-450, 8 plates.

1890. Observations on the Structure and Economy of

Whales. Philosophical Transactions of the Royal

Society of London, 15 (1785-1790):306-351, 1 plate.

[Abridged by Hutton, Shaw, and Pearson.]

Kellogg, A. R.

1928. The History of Whales: Their Adaptation to Life

in the Water. The Quarterly Review of Biology,

3(l,2):29-76, 174-208, 10 figures.
NUMBER 207 69

1938. Adaptation of Structure to Function in Whales.

Pages 649-682 in Cooperation in Research by Staff

Members and Research Associates of the Carnegie

Institute of Washington. Carnegie Institute of

Washington, Contributions to Paleontology, number

501.

Kellogg, W. N., R. Kohler, and H. N. Morris

1953. Porpoise Sounds as Sonar Signals. Science, 117

(3036): 239-243.

Kernan, J. D., Jr., and H. von W. Schulte

1918. Memoranda upon the Anatomy of the Respiratory

Tract, Foregut, and Thoracic Viscera of a Foetal

Kogia breviceps. Bulletin of the American Museum

of Natural History, 38 (3):231-267, 16 figures.

Khomenko, B. H.

1970. Pro gistotructuru ta innervatsiyu zbukovo aparatu

(nasalnikh mishkiv) dilfiniv (The Histostructure

and Innervation of the Sound Apparatus-Nasal

Sacs- in Dolphins). Dopovidi Akademiyi Nauk

Ukrayinskoyi RSR, 32(l):83-87, 4 figures.

Kleinenberg, S. E., and A. V. Yablokov

1958. O morfologii verkhnikh dykhatelnykn putei kitoobraznykh (Morphology of Upper Respiratory Passages in the Cetaceans). Zoologicheskii Zhurnal,

37 (7): 1091-1099, 10 figures.

Kleinenberg, S. E., A. V. Yablokov, B. M. Belkovich, and

M. N. Tarasevich

1969. Beluga (Delphinapterus leucas): Investigation of

the Species. 376 pages, 118 figures. Israel Program

for Scientific Translations. [Translated from

Russian.]

Kooyman, G. L., and H. T. Andersen

1969. Deep Diving. Pages 65-94 in Anderson, editor,

The Biology of Marine Mammals. New York: Academic Press.

Kritzler, H.

1952. Observations on the Pilot Whale in Captivity.

Journal of Mammalogy, 33:321-334.

Kiikenthal, W.

1893. Vergleichend-anatomische und entiwickelungsgeschichtliche Untersuchungen an Walthieren. Denkschriften der Medicinisch-Naturwissenschaftlichen

Gesellschaft zu Jena, 3(2):l-448, 25 plates.

1908. Ueber die Ursache der Asymmetrie des Walschadels.

Anatomische Anzeiger, 33:609-618.

Lahille, F.

1908. Notas sobre un ballenato de 2.10 metros de largo

(Balaenoptera acuto-rostrata Lac). Annales de

Museo Publico de Buenos Aires (Museo Argentino

de Ciencias Naturales), 16:375^101, 8 figures, 1

plate.

Lawrence, B., and W. E. Schevill

1956. The Functional Anatomy of the Delphinid Nose.

Bulletin of the Museum of Comparative Zoology,

114 (4): 103-151, 30 figures.

Lillie, D. G.

1910. Observations on the Anatomy and General Biology

of Some Members of the Larger Cetacea. Proceedings of the Zoological Society of London, 1910:769-

792, 10 figures, 1 plate.

Lilly, J. C.

1961. Man and Dolphin. 312 pages. Garden City: Doubleday & Co., Inc.

1962. Vocal Behavior of the Bottlenose Dolphin. Proceedings of the American Philosophical Society,

106 (6): 520-529, 11 figures.

Lilly, J. C, and A. M. Miller

1961. Sounds Emitted by the Bottlenose Dolphin. Science,

5:1689-1693,4 figures.

Litchfield, C, and A. Greenberg

1974. Comparative Lipid Patterns in the Melon Fats of

Dolphins, Porpoises, and Toothed Whales. Comparative Biochemistry and Physiology, 47B:401-407,

1 figure.

Litchfield, C, R. Karol, and A. Greenberg

1973. Compositional Topography of Dolphin Melon

Lipids: Implications for Echolocation. Marine

Biology, 23:165-169.

Macalister, A.

1867. On Some Points in the Anatomy of Globicephalus

svinval (Gray). Proceedings of the Zoological Society

of London, 1867:477^82.

Maderson, P. F. A.

1968. The Histology of the Nasal Epithelia of Tursiops

truncatus (Cetacea) with Preliminary Observations

on a Series of Glandular Structures. American

Zoologist, 8:810 (abstract).

Miller, G. S., Jr.

1923. The Telescoping of the Cetacean Skull. Smithsonian Miscellaneous Collections, 76(5):l-70, 8

plates.

Miller, M. E., G. C. Christensen, and H. E. Evans

1964. Anatomy of the Dog. 941 pages. New York: Saunders.

Mitchell, E. D.

1970. Pigmentation Pattern Evolution in Delphinid Cetaceans: An Essay in Adaptive Coloration. Canadian

Journal of Zoology, 48 (4):717-740, 15 plates.

Moris, F.

1969. £tude anatomique de la region cephalique du

marsouin, Phocaena phocaena L. (cetace odontocete). Mammalia, 33 (4):666-726, 27 figures, 4 plates.

Moss, M. L., and L. Salentijn

1969. The Primary Role of Functional Matrices in Facial

Growth. American Journal of Orthodontics, 55(6):

566-577, 5 figures.

Murie, J.

1870. On Risso's Grampus, G. rissoanus (Desm.). Journal

of Anatomy and Physiology, 5:118-138, 2 figures,

1 plate.

1871. Notes on the White-beaked Bottlenose, Lagenorhynchus albirostris Gray. Journal of the Linnean

Society, Zoology, 11:141-153, 1 plate.

1873. On the Organization of the Caaing Whale, Globiocephalas melas. Transactions of the Zoological

Society of London 8(4):235-301, 9 plates.
70

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Negus, V. E.

1949. The Comparative Anatomy and Physiology of the

Larynx. 230 pages. London: Heinemann.

Ness, A. R.

1967. A Measure of Asymmetry of the Skulls of Odontocete Whales. Journal of Zoology, 153:209-221, 4

figures.

Nishiwaki, M.

1963. Taxonomical Consideration on Genera of Delphinidae. Scientific Reports of the Whales Research

Institute, 17:93-103.

Norman, J. R., and F. C. Fraser

1937. Giant Fishes, Whales, and Dolphins. 376 pages, 8

plates. London: Putnam.

Norris, K. S.

1964. Some Problems of Echolocation in Cetaceans.

Pages 317-355 in volume 1 of Tavolga, editor,

Marine Bio-Acoustics. New York: Pergamon Press.

1968. The Evolution of Acoustic Mechanisms in Odontocete Cetaceans. Pages 297-324 in Drake, editor,

Evolution and Environment. New Haven: Yale

University Press.

1969. The Echolocation of Marine Mammals. Pages 391-

423 in Andersen, editor, The Biology of Marine

Mammals. New York: Academic Press.

Norris, K. S., and W. E. Evans

1967. Directionality of Echolocation Clicks in the Roughtooth Porpoise, Steno bredanensis (Lesson). Pages

305-316 in volume 2 of Tavolga, editor, Marine

Bio-Acoustics. New York: Pergamon Press.

Norris, K. S., J. H. Prescott, P. V. Asa-Dorian, and P. Perkins

1961. An Experimental Demonstration of Echolocation

Behavior in the Porpoise, Tursiops truncatus

(Montagu). Biological Bulletin, Woods Hole, 120(2):

163-176,4 figures.

Norris, K. S., K. J. Dormer, J. Pegg, and G. J. Liese

1971. The Mechanism of Sound Production and Air

Recycling in Porpoises: A Preliminary Report.

Proceedings of the Eighth Annual Conference on

Biological Sonar and Diving Mammals, Stanford

Research Institute, pages 113-129, 4 figures.

Norris, K. S., and G. W. Harvey

1974. Sound Transmission in the Porpoise Head. Journal

of the Acoustical Society of America, 56 (2):659-664,

4 figures.

Osburn, R. C.

1903. Adaptation to Aquatic, Arboreal, Fossorial, and

Cursorial Habits in Mammals, I: Aquatic Adaptations. American Naturalist, 37 (442):651-665.

Palmer. E.. and G. Weddell

1964. The Relationship between Structure, Innervation,

and Function of the Skin of the Bottlenose Dolphin

(Tursiops truncatus). Proceedings of the Zoological

Society of London, 143 (4):553-567, 7 plates.

Parry, D. A.

1949. The Anatomical Basis of Swimming in Whales.

Proceedings of the Zoological Society of London,

119:49-60, 5 figures.

Pouchet, M. G.

1886. De I'Asyme'trie de la face chez les Cetodontes. 16

pages. Paris: Libraire de l'Academie de Medicine.

Pouchet, M. G., and H. Beauregard

1885. Sur "l'organe des Spermaceti." Comptes Rendus de

Socie'te Biologique, 11:343-344.

1892. Recherches sur le cachalot. Nouvelle Archives du

Muse'e d' Histoire Naturelle, series 3, 4:1-90, 12

plates.

Purves, P. E.

1966. Anatomy and Physiology of the Outer and Middle

Ear in Cetaceans. Pages 320-380 in Norris, editor,

Whales, Dolphins and Porpoises. Berkeley: University of California Press.

1967. Anatomical and Experimental Observations on the

Cetacean Sonar System. Pages 197-270 in volume 1

of Busnel, editor, Animal Sonar Systems, Biology

and Bionics. GAP (Hautes-Alpes): Imprimerie

Louis-Jean.

Purves, P. E., and G. Pilleri

1973. Observations on the Ear, Nose, Throat, and Eye of

Platanista indi. Pages 13-57 in volume 5 of Pilleri,

editor, Investigations on Cetacea.

Raven, H. C.

1942. Some Morphological Adaptations of Cetaceans

(Whales and Porpoises) for Life in the Water.

Transactions of the New York Academy of Sciences,

second series 5(2):23-29.

Raven, H. C, and W. K. Gregory

1933. The Spermacetic Organ and Nasal Passages of the

Sperm Whale (Physeter catodon) and Other Odontocetes. Novitates, American Museum of Natural

History, 677:1-18, 9 figures.

Rawitz, B.

1900. Die Anatomie des Kehlkopfes und der Nase von

Phocaena communis Cuv. Internationale Monatsschrift fur Anatomie und Physiologie, 17:245-354.

Ray, J.

1671. An Account of the Dissection of a Porpess. Philosophical Transactions of the Royal Society of

London, 6(76):2274-2279.

Reysenbach de Haan, F. W.

1957. Hearing in Whales. Acta Oto-laryngologica, supplement 134, 114 pages, 41 figures.

Richard, C.

1930. Di una peculiare asimmetria dei fiseteridi (asimmetrie emapofisaria) e delle sue relazioni con

l'asimmetria cranica. Accademia Nazionale dei

Lincei, Rome, classe di Science Fisiche, Rendiconti,

series 6, 12:165-172, 2 figures.

Richard, J.

1936. Documents sur le Cetaces et Pinnipedes des Croisieres du Prince Albert ler de Monaco. Fascicule

XCIV in Resultats des Campagnes Scientifiques

Accomplies sur son Yacht ptr Albert ler, Prince

Souverain de Monaco. 72 pages, 8 plates.
NUMBER 207 71

Ridgway, S. H.

1966. Dall Porpoise, Phocoenoides dalli (True): Observations in Captivity and at Sea. Norsk HvalfangstTidende (Norwegian Whaling Gazette), 1966(5):97-

110, 11 figures.

1971. Buoyancy Regulation in Deep Diving Whales. Nature, 232(5306): 133-134.

Scammon, C. M.

1874. The Marine Mammals of the North-western Coast

of North America, Described and Illustrated: Together with an Account of the American WhaleFishery. 319 pages, 27 plates. San Francisco: John

H. Carmany & Co.

Schenkkan, E. J.

1971. The Occurrence and Position of the "Connecting

Sac" in the Nasal Tract Complex of Small Odontocetes (Mammalia, Cetacea). Beaufortia, 19(246):

37-43, 3 figures.

1972. On the Nasal Tract Complex of Pontoporia blainvillei Gervais and d'Orbigny 1844 (Cetacea, Platanistidae). Pages 83-90 in volume 4 of Pilleri, editor,

Investigations on Cetacea.

1973. On the Comparative Anatomy and Function of the

Nasal Tract in Odontocetes (Mammalia, Cetacea).

Bijdragen tot de Dierkunde, 43(2): 127-159, 16 figures.

Schenkkan, E. J., and P. E. Purves

1973. The Comparative Anatomy of the Nasal Tract and

the Function of the Spermaceti Organ in the Physeteridae (Mammalia, Odontoceti). Bijdragen tot de

Dierkunde, 43(1):93-112. 12 figures.

Schevill, W. E.

1964. General Discussion. Pages 395-398 in volume 1 of

Tavolga, editor, Marine Bio-Acoustics. New York'

Pergamon Press.

Schevill, W. E., and B. Lawrence

1956. Food-finding by a Captive Porpoise (Tursiops truncatus). Breviora of the Museum of Comparative

Zoology, 53:1-15.

Schevill,"W. E., and W. A. Watkins

1966. Sound Structure and Directionality in Orcinus

(killer whale). Zoologica, 519(6):71-76, 6 plates.

Schulte, H. von W.

1916. Anatomy of a Foetus of Balaenoptera borealis.

Memoirs of the American Museum of Natural History, new series, 1 (6):389-502, 15 plates.

Scoresby, W.

1823. Journal of a Voyage to the Northern Whalefishery:

Including Researches and Discoveries on the Eastern Coast of Greenland, Made in the Summer of

1822, in the Ship Baffin of Liverpool. 472 pages, 8

plates, London: Hurse, Robinson and Co.

Sibson, F.

1848. On the Blow-hole of the Porpoise. Philosophical

Transactions of the Royal Society of London, 1848:

117-123, 1 plate.

Simpson, G.

1945. The Principles of Classification and a Classification

of Mammals. Bulletin of the American Museum of

Natural History, 85:1-350.

Sleptsov, M. M.

1939. K voprosy ob asimmetrii cherepa u odontoceti

(On the Question of the Asymmetry of the Skull

in Odontoceti). Zoologicheskii Zhurnal, 18:367-386,

6 figures. [English summary.]

Slijper, E. J.

1936. Die Cetaceen, Vergleichend-anatomisch und systematisch. Capita Zoologica, 7:1-590, 251 figures.

1958. Organ Weights and Symmetry Problems in Porpoises and beals. Archives Neerlandaises de Zoologie,

supplement, 8(1):97-113, 5 figures.

1961. Locomotion and Locomotory Organs in Whales

and Dolphins (Cetacea). Symposia of the Zoological

Society of London, 5:77-94, 10 figures.

Stannius, H.

1849. Beschreibung der Muskeln des Tummlers (Delphinus phocaena). Archiv fur Anatomie, Physiologie

und wissenschaftliche Medicin, 1849:1-41.

Steinmann, G.

1912. Ueber die Ursache der Asymmetrie der Wale.

Anatomische Anzeiger, 42:45-54, 5 figures.

Sterling, S.

1910. O asymetryi czaszki wielorybow (On the Asymmetry

of the Skulls of Whales). Towarzystwo naukowe

warszawskie, Warsaw, sprawozdinia z posiedzen

(Comptes Rendus des Seances de la Societe scientifique de Varsovie), 3 (5):231-235, 2 figures.

Tomilin, A. G.

1967. Cetacea, Mammals of the U.S.S.R. and Adjacent

Countries, IX. 717 pages, 146 figures. Israel Program for Scientific Translations. [Translated from

Russian.]

True, F. W.

1889. Contributions to the Natural History of the Cetaceans, a Review of the Family Delphinidae. Bulletin of the United States National Museum, 36:1-

191, 47 plates.

Turner, W.

1867. A Contribution to the Anatomy of the Pilot Whale

(Globiocephalus svineval, Lacepede). Journal of

Anatomy and Physiology, 2:66-79.

Watson, M., and A. H. Young

1879. The Anatomy of the Northern Beluga (Beluga

catodon Gray; Delphinapterus leucas Pallas) Compared with That of Other Whales. Transactions

of the Royal Society of Edinburgh, 29(1):393-435,

2 plates.

Weber, M.

1886. Studien iiber Sdugethiere: Ein Beitrag zur Frage

nach dem Ursprung der Cetaceen. 252 pages, 4

plates. Jena: Gustav Fischer.

Wedmid, G., C. Litchfield, R. G. Ackman, and J. C. Sipos

1972. Heterogeneity of Lipid Composition within the

Cephalic Melon Tissue of the Pilot Whale. Journal

of the American Oil Chemists Society, 48:332 A

[abstract].
SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

72

WH" n S W Wood, F. G.

1902 On Certain Homoplastic Characters in Aquatic, 1964. General Discussion. Pages 395-398 in volume 1 of

Air-breathing Vertebrates. Kansas University Science Tavolga, editor, Marine Bio-Acoustics. New York:

Bulletin, 1:259-266. Pergamon Press.

T.V U.S. GOVERNMENT PRINTING OFFICE: 107S 586-382/39
Publication in Smithsonian Contributions to Zoology

Manuscripts for serial publications are accepted by the Smithsonian Institution Press, subject to substantive review, only through departments of the various Smithsonian museums. NonSmithsonian authors should address inquiries to the appropriate department. If submission is

invited, the following format requirements of the Press will govern the preparation of copy.

Copy must be typewritten, double-spaced, on one side of standard white bond paper, with

W2" top and left margins, submitted in ribbon copy with a carbon or duplicate, and accompanied by the original artwork. Duplicate copies of all material, including illustrations, should be

retained by the author. There may be several paragraphs to a page, but each page should begin

with a new paragraph. Number consecutively all pages, including title page, abstract, text, literature cited, legends, and tables. The minimum length is 30 pages, including typescript and illustrations.

The title should be complete and clear for easy indexing by abstracting services. Taxonomic

titles will carry a final line indicating the higher categories to which the taxon is referable:

"(Hymenoptera: Sphecidae)." Include an abstract as an introductory part of the text. Identify

the author on the first page of text with an unnumbered footnote that includes his professional

mailing address. A table of contents is optional. An index, if required, may be supplied by the

author when he returns page proof.

Two headings are used: (1) text heads (boldface in print) for major sections and chapters and (2) paragraph sideheads (caps and small caps in print) for subdivisions. Further

headings may be worked out with the editor.

In taxonomic keys, number only the first item of each couplet; if there is only one couplet,

omit the number. For easy reference, number also the taxa and their corresponding headings

throughout the text; do not incorporate page references in the key.

In synonymy, use the short form (taxon, author, date:page) with a full reference at the

end of the paper under "Literature Cited." Begin each taxon at the left margin with subsequent lines indented about three spaces. Within an entry, use a period-dash (.—) to separate

each reference. Enclose with square brackets any annotation in, or at the end of, the entry.

For references within the text, use the author-date system: "(Jones, 1910)" and "Jones

(1910)." If the reference is expanded, abbreviate the data: "Jones (1910:122, pi. 20: fig. 1)."

Simple tabulations in the text (e.g., columns of data) may carry headings or not, but they

should not contain rules. Formal tables must be submitted as pages separate from the text, and

each table, no matter how large, should be pasted up as a single sheet of copy.

Use the metric system instead of, or in addition to, the English system.

Illustrations (line drawings, maps, photographs, shaded drawings) can be intermixed

throughout the printed text. They will be termed Figures and should be numbered consecutively; however, if a group of figures is treated as a single figure, the components should be

indicated by lowercase italic letters on the illustration, in the legend, and in text references:

"Figure 9b." If illustrations (usually tone photographs) are printed separately from the text as

full pages on a different stock of paper, they will be termed Plates, and individual components

should be lettered (Plate 96) but may be numbered (Plate 9: figure 2). Never combine the

numbering system of text illustrations with that of plate illustrations. Submit all legends on

pages separate from the text and not attached to the artwork. An instruction booklet for the

preparation of illustrations is available from the Press on request.

In the bibliography (usually called "Literature Cited"), spell out book, journal, and

article titles, using initial caps with all words except minor terms such as "and, of, the." For

capitalization of titles in foreign languages, follow the national practice of each language.

Underscore (for italics) book and journal titles. Use the colon-parentheses system for volume,

number, and page citations: "10(2) :5-9." Spell out such words as "figures," "plates," "pages."

For free copies of his own paper, a Smithsonian author should indicate his requirements

on "Form 36" (submitted to the Press with the manuscript). A non-Smithsonian author will

receive 50 free copies; order forms for quantities above this amount with instructions for payment will be supplied when page proof is forwarded.
i