anatomy of the external nasal passages and facial complex

Anatomy of the ExternalNasal Passages and Facial Complex

in the Delphinidae(Mammalia: Cetacea)

JAMES G, MEAD

miut.

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S M I T H S O N I A N C O N T R I B U T I O N S T O Z O O L O G Y • N U M B E R 2 0 7


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 Complexin the Delphinidae (Mammalia: Cetacea). Smithsonian Contributions to Zoology,number 207, 72 pages, 26 figures, 3 tables, 1975.—This study is concerned withthe comparative anatomy of the external nasal passages and associated structuresin delphinid odontocetes. It has been possible to assemble detailed anatomicalinformation for nearly all of the delphinid genera. Comparative data for theother small toothed whales is considered in such detail as is available.

The function of the structures associated with the external nasal passages hasbeen 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 nasalpassage during respiration, and with movement of air between the nasal diver-ticula during sound production. The nasal diverticula are part of the acousticsystem of these animals, and function both as air reservoirs and as reflectiveelements to focus the emitted sound field. The potential area of sound produc-tion is limited to the deep structures around the external body nares. The melonprobably serves as an acoustic channel. Cranial asymmetry in odontocetes isrelated to specialized sound-producing mechanisms involving predominantly theright nasal passage.

The nasal structures have formed a very important functional complex in theevolution of odontocetes, and are important from a phyletic viewpoint. Thisstudy has shown that the genera Tursiops, Stenella, and Delphinus form a rela-tively generalized group within the Delphinidae. The bulbous-headed generaGrampus, Globicephala, and Pseudorca clearly represent independent specializa-tions. The other families of odontocetes differ considerably from the delphinidsin their facial anatomy.

The anatomical diversity in this region suggests an acoustic diversity whichremains to be demonstrated experimentally.

OFFICIAL PUBLICATION DATE is handstamped in a limited number of initial copies and is recordedin the Institution's annual report, Smithsonian Year. SI PRESS NUMBER 5387. SERIES COVERDESIGN: The coral Montastrea cavernosa (Linnaeus).

Library of Congress Cataloging in Publication DataMead, 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 1.27:2071. 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

PageIntroduction 1

Historical Review • 1General Aspects of the Facial Anatomy of Mammals 2Questions of Odontocete Facial Anatomy . 4Acknowledgments 5

Descriptive Anatomy 5Introduction 5Delphinidae 6

Delphininae . 6Tursiops 6Stenella 15Delphinus 17Lagenorhynchus 18Lagenodelphis 19Grampus 19

Orcininae 22Orcinus 22Pseudorca 23Globicephala 24

Steninae 26Steno 26Sotalia 28

Cephalorhynchinae • 28Cephalorhynchus 28

Lissodelphinae 29Lissodelphis 29

Phocoenidae 30Phocoena, Phocoenoides, Neophocaena 30

Monodontidae 31Monodon 31Delphinapterus 31

Platanistidae 32Platanista 32Lipotes 33Pontoporia 33Inia . 33

Summary of Descriptive Anatomy 34Nasal Passage and Diverticula . 34Musculature 34Melon 34Other Structures 35

j v SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

Page

Function of the Facial Complex 35Introduction 35Respiratory Considerations . 35Nasal Passage and Diverticula 36Musculature 37Melon 40Glandular Structures 41Functional Basis of Sound Production 42

Review 42Anatomical Considerations 46

Functional Aspects of Cranial Asymmetry 48Review 48Anatomical Considerations 51

Summary of Facial Complex Function 53Nasal Diverticula 53Nasal Musculature 53Other Structures 54

Experimental Approaches . 54Phyletic Relations of the Delphinidae 54

Relationships within the Delphinidae 54Relationships to Other Families 56Relationships of Bulbous-headed Delphinids 57

General Considerations 57Comparison of Pseudorca, Globicephala, and Grampus 58

Origin of the Odontocete Nasal Apparatus 61Appendix 1: Classification of the Odontocetes (Toothed Whales) 64Appendix 2: Tables 65Literature Cited 67


in the Delphinidae(Mammalia: Cetacea)

James G. Mead

INTRODUCTION

Historical Review

The structure of the Cetacea (whales, porpoises,and dolphins) has long fascinated anatomists andstudents of natural history in general. Many fea-tures of cetacean anatomy were familiar to theclassical natural historians, notably Pliny the Elderand Aristotle. During the middle ages, cetaceawere frequently treated in general works on nat-ural history (Olaus Magnus, Gesner, Rondeletius,and others), but emphasis was on the fabulousaspects of the larger members of the order. Thefirst work exclusively on the anatomy of a cetaceanis John Ray's "Account of the Dissection of aPorpess" (1671). This paper is particularly inter-esting, in that it contains a description of the nasalpassages and diverticula, as well as some specula-tions upon their function.

The peak of activity on cetacean anatomy oc-curred during the 19th century, when such workersas Turner, Flower, Murie, Rapp, Kukenthal, Stan-nius, and others produced thousands of pages ofdescriptive anatomy. During the 20th century thiswork was continued by Howell, Schulte, Beddard,Huber, Slijper, and others.

Of the smaller cetaceans, Phocoena phocoena

James G. Mead, Department of Vertebrate Zoology, NationalMuseum of Natural History, Smithsonian Institution, Wash-ington, D. C. 20560.

(the harbor porpoise) has been the most frequentlyand most thoroughly described (e.g., Ray, 1671;Stannius, 1849; von Baer, 1826; Rawitz, 1900), dueto its abundance along the European coast and itsconvenient size. The pilot whale (Globicephalamelaena) has also been the frequent subject ofanatomical investigations (Macalister, 1867; Tur-ner, 1867; and most notably Murie, 1873), due tothe frequency of its strandings along the Europeancoasts. Aside from these, the best descriptions ofthe anatomy of smaller cetaceans are usually ofrare and unusual animals (e.g., Neophocaena,Howell, 1927; Kogia, Danois, 1910; Kernan andSchulte, 1918; Monodon, Huber, 1934). Delphininecetaceans have received less attention, and verylittle published information exists for Tursiopstruncatus, the ubiquitous experimental animal ofthe present time.

Relatively few of the many hundreds of papersdealing with the anatomy of cetaceans containinformation on the structures of the facial region.Some of the early papers (Ray, 1671; Hunter, 1787;Cuvier, 1836) on general anatomy mention thestructure of the nasal passage, or comment brieflyon the musculature surrounding it. Von Baer(1826) appears to have been the first to focus onthe structure of the cetacean nose, based upon dis-sections of Phocoena. Sibson (1848) described thenasal apparatus in Phocoena and Murie (1870,

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

1873) went into some detail in discussing the facialstructures of a variety of odontocetes. Gruhl (1911)commented extensively on the diverticula in anumber of species. (Purves, 1967, and Moris, 1969,have given brief descriptions of the facial anatomyof Steno and Phocoena.)

The principal recent works dealing with theanatomy and function of the nasal apparatus arethose of Lawrence and Schevill (1956), who wereprimarily concerned with the respiratory functionsof these structures, Schenkkan (1971, 1972, 1973),and Schenkkan and Purves (1973). Schenkkan(1973) presented an extensive treatment of thecomparative functional anatomy of the nasal tractof odontocetes. His data filled in many of the gapsin my material and have been utilized extensivelyin the present paper. Many of the differences be-tween his work and mine probably stem from thefact that Phocoena formed the comparative frame-work of his study, whereas I used Stenella.

Since the discovery of the possibility of echoloca-tion in odontocetes in the early 1950s (Kellogg,et al., 1953; Schevill and Lawrence, 1956), and itsexperimental demonstration in 1961 (Norris et al.,1961), the anatomy of structures potentially in-volved in sound production and reception hasreceived considerable attention. The question ofsound reception has been treated by Reysenbachde Haan (1957) and Fraser and Purves (1960).Evans and Prescott (1962) and Norris (1964) haveconsidered the problems of sound production, whileNorris (1969) has provided the most recent generalsurvey of the problems of echolocation in cetaceans.

The structures comprising the facial region ofthe odontocetes, i.e., the nasal passages and theirdiverticula, the fatty melon, and the muscles asso-ciated with these, have frequently been implicatedin sound production (Lawrence and Schevill, 1956;Evans and Prescott, 1962; Norris, 1968). Questionsrelating to the mechanism of sound production,such as which structures are involved and how theacoustic energy is conducted from the soundsource (s), focused, modulated, and otherwisealtered, are still under debate.

General Aspects of the Facial Anatomy ofMammals

The face, as it is generally thought of in humanterms, consists of the anterior portion of the head,

containing the nose, mouth, and eyes. To a certainextent this area can be considered separate fromthe remainder of the head, or cranium. Thus con-ceived, the bony elements of the face are the max-illae, premaxillae, nasals, vomer, palatines, zygo-matics, and frontals. This division of the headcorresponds approximately with the distributionof motor elements associated with the facial nerve,and with the sensory distribution of the trigeminalnerve.

The anatomy of the mammalian face is complex(see Huber, 1930; Edgeworth, 1935; Miller et al,1964), and presumably has been throughout muchof its evolutionary history.

The soft tissues consist of a series of musclesdisposed about the orifices of the face and largelyconcerned with manipulation of these, the skin andvarious specialized portions of the skin (lips, eye-lids, etc.), and the vascular and nervous suppliesof these elements. The structures within the facialorifices (eyes, tongue, etc.) could logically beincluded in this group and would greatly expandthis list. However, these are extremely specializedand are better considered separately.

The nose is generally a complex structure inmammals, and even in terrestrial mammals it iscapable of being opened and closed to a consider-able extent. This is accomplished by various por-tions of the m. maxillonasolabialis acting upon thecartilages comprising the skeleton of the nasal aper-ture. In addition, the area of the nose is usuallyhighly sensitive and is abundantly supplied withnerves and blood vessels. The complexity of themammalian nose has provided the basis for a greatvariety of evolutionary modifications, exemplifiedby the noses of pigs, elephants, tapirs, bats, moles,and whales. Boas and Pauli (1908) give an excel-lent picture of the diversity of mammalian noses.

The cetacean face has become specialized as aresult of the demands of an aquatic existence, andpresents a number of differences from that of ter-restrial mammals. The nose occupies a dorsal ratherthan a terminal position on the rostrum, and thefacial musculature has become largely concernedwith opening and closing the nasal aperture. Ceta-cea are, in fact, one of the very few groups ofmammals incapable of facial expression, as theareas of the mouth and eyes are relativelyimmobile.

The orbit has moved laterally and ventrally and

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now bears a closer relationship to the base of thecranium than to the rest of the face. There hasbeen extensive alteration of the bones of the skull(Miller, 1923), differing in detail in the two sub-orders 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 ceta-cean skull (when viewed from above) is the flatexpanse of bone formed by the dorsal surface ofthe rostrum and cranium. This surface is boundedby the lateral edge of the rostrum, the supraorbitalprocess of the frontal, and the temporal and nuchalcrests (Figure 1). This area can be usefully definedas the face in this group of animals, as it forms anarea concerned with the operation of the highlymodified cetacean nose. The orbit, while still sur-rounded by what is technically facial musculature,does not fit into the functional area of the face in

pmx

sopFIGURE 1.—Skulls of modern cetaceans (after Kellogg, 1928):a, Tursiops truncatus, an odontocete, lateral view; b, T. trun-catus, dorsal view; c, Balaenoptera edeni, a mysticete, lateralview; 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 sec-tion; b, detail of the above. (af = anterior fold, bhl = blow-hole ligament, bnp = bony nasal passage, iv = inferior vesti-bule, lnp = lip of the nasal plug, m = melon, ns = nasofrontalsac, np = nasal plug, pf=posterior fold, ps = premaxillary sac,sc = spiracular cavity, vs = vestibular sac.)


the same manner that it does in terrestrial mam-mals, nor does the mouth.

The skull of mysticetes has been modified alongdifferent lines than that of the odontocetes, theprimary modification apparently being the development of a large rostrum as part of the feedingmechanism. If the braincase is taken as the pointof reference, the nasal passages have not been dis-placed posterodorsally, as they have in odontocetes.Carte and Macalister (1868) provide the bestdescription of the facial structures of a mysticete.The musculature associated with the nares is exten-sive, but there are no diverticula, nor is there any-thing comparable to the large melon of odonto-cetes. Viewed from the side, the facial region ofmysticetes appears very low and flat compared tothat of odontocetes.

In the odontocetes, the nasal aperture has mi-grated posterodorsally, and now opens on the dorsalsurface of the head. The musculature associatedwith the nasal passage has increased in size andcomplexity, as have the passages themselves. Insteadof a relatively simple passage, as in the mysticetes,there is a complicated series of diverticula andvalves within the nose of the toothed whales (Fig-ure 2). An accessory structure, the melon, hasdeveloped anterior to the nasal passage, greatlyincreasing the bulk of the facial apparatus. Theacme of these is seen in the nose of the spermwhale, which constitutes on the order of one-thirdof the weight of the entire animal.

The development of a complex nasal apparatus,particularly the elaboration of a fatty melon, isone of the principal distinctions between odonto-cetes and mysticetes. The differences in the struc-ture of the bony elements of the face can be fol-lowed well back into the fossil record (Kellogg,1928), suggesting that the adaptive aspects of theseformed one of the bases for differentiation of thetwo suborders. Mysticete differentiation appears tohave depended upon the development of a novelfeeding apparatus, while odontocetes remained rela-tively conservative in that aspect, and have elab-orated the nasal apparatus and associated structures.

Numerous anatomists have attempted to homolo-gize the structures of the cetacean nose with thoseof the other mammals (von Baer, 1826; Murie,1870, 1873; Anthony, 1926). The diverticula havebeen compared with the turbinals of other mam-mals and with the nasal sacs of the tapir, the saiga

antelope, and the horse. Murie (1870) attemptedto homologize the nasal musculature with the var-ious facial muscles of man. It is my belief, however,that the melon, nasal diverticula, and differentia-tion of the nasal musculature have been derivedindependently in cetaceans. Huber's (1934) briefhomology of the nasal musculature with the m.maxillonasolabialis appears to be the most rationalapproach to the question of muscle homologies.The archaeocetes do not appear to have possesseda specialized nasal apparatus, making it unlikelythat anything but the most generalized of mam-malian homologies is applicable to the modernCetacea.

Questions of Odontocete Facial Anatomy

A thorough understanding of the anatomy ofthis region is essential before we can hope to under-stand the functions in which it is involved. Thisis particularly true of a system like the odontocetenose, which does not appear to have an analoguein any other mammalian structure. I have describedthe components of the facial complex and theirrelationships to one another in order to see if theyform discernible functional systems. To an extentthis has been possible, particularly with simplermechanical functions, such as opening and closingof the blowhole and nasal passages.

Many of the potential functions of this regionare more subtle or complex and cannot be ap-proached in this manner. In order to elucidatethese, I have undertaken a comparative study,hoping to find structural differences which couldbe correlated with observed behavioral or ecologicdifferences.

This type of comparative approach is useful notonly in terms of the answers which it provides, butalso the questions which it poses. The range ofexternal morphology in the head of small odonto-cetes indicates the possibility of a wide range ofinternal structure. If such structural diversity isdemonstrated, it will suggest a functional diversitywhich must then be looked for in the livinganimals.

Specialization of the facial region of odontoceteshas probably been an important factor in theirevolution and is thus important phyletically aswell as functionally. Relationships among the livingodontocetes are poorly understood at present. An

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examination of one of their more important func-tional complexes will provide a new basis for inter-preting phyletic relationships in this group. Thisis particularly true where questions of possibleconvergence are involved, as in the bulbous-headeddelphinids.

The significance of the asymmetry of the skull inodontocetes has never been satisfactorily explained.This is because the relationship of the bony asym-metry to the soft tissues of the head has never beenexamined. Such an approach is essential to anunderstanding of the functional significance of thischaracter.

A detailed anatomical study will also provide abasis for experimental work on these animals,which has previously been hampered by a lack ofinformation on the structures involved.

The literature pertaining to these problems isvoluminous and somewhat confusing. I haveattempted to review much of this and to clarifysome of the points of confusion.

Acknowledgments

This work was begun and substantially com-pleted during my tenure as a graduate student atthe University of Chicago, and, as any dissertation,owes a great deal to many people. LeonardRadinsky, Charles Oxnard, George Rabb, LeighVan Valen, and Edward D. Mitchell served on thedissertation committee, read the manuscript at

various stages, and provided much valuable criti-cism. I would like to express particular apprecia-tion to James Hopson, my major professor, withoutwhose patience and assistance this work wouldnever have succeeded. I am also grateful to myfellow graduate students, particularly Timothy L.Strickler, who participated in many phases of thisstudy, and to my wife, Rebecca.

One of the greatest obstacles faced by a com-parative study of this sort is the availability ofspecimens. The material used in the studj wasprovided 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 Aqua-rium, Chicago; William F. Perrin, Southwest Fish-eries Center; Robert Jones, University of Californiaat Berkeley; Robert L. Brownell; Allen Wolmanand Dale Rice, Marine Mammal Biology Labora-tory, Seattle. I would also like to thank the people,too numerous to mention, who spent time unsuc-cessfully trying to obtain material for this study.I am particularly indebted to Edward D. Mitchell,not only for providing material, but also for theuse of his laboratory facilities and library, remu-nerative employment, the drawing used in Figure10, and a continuing flow of advice.

While I was at the University of Chicago, thiswork was supported by grants from the Hinds Fundand a fellowship from the Center for GraduateStudies in Systematic Zoology and Paleontology atthe Field Museum of Natural History.

DESCRIPTIVE ANATOMY

Introduction

I have dissected the facial region in a series ofdelphinids, consisting of members of the followinggenera: Tursiops, Stenella, Grampus, Lagenorhyn-chus, Lagenodelphis, Orcinus, Pseudorca, Globi-cephala, Steno, and Cephalorhynchus. In addition,I have dissected specimens of Phocoena, Phocoe-noides, Inia, and Pontoporia, and have compiledsuch comparative data as is available for othergenera. The families Physeteridae and Ziphiidaehave been deliberately omitted, as they appear to

be strikingly different and constitute a separateproblem.

The techniques employed consisted of gross dis-section, along with gross coronal and sagittal sec-tions of the soft structures of the facial region. Thedissections were limited to the area dorsal andmedial to the supraorbital process of the frontaland the temporal crest, and anterior to the nuchalcrest. Extensive photographs were taken as a recordof the dissections. A large series of specimens ofStenella, covering a wide size range, was dissected


and the nasal muscles fixed and weighed in orderto determine whether there was any asymmetry inthe 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 outstand-ing reasons for this choice. First, Tursiops appearsto be a relatively generalized delphinid, from whichthe conditions seen in the other genera could bereadily derived. Second, it has become the standardexperimental animal and, as such, there are dataavailable for it that are lacking for the less com-mon animals. Unfortunately, I found materialdifficult to obtain for Tursiops, and I have notbeen able to dissect enough animals to establishthe range of individual variation in this species.

The descriptions that follow have not taken intoaccount the asymmetry seen in some of the facialstructures, as this will be treated in detail in alater section. In general, the descriptions of thenasal passages and diverticula begin with the deepstructures and proceed to the superficial ones, whilethe muscular descriptions follow the opposite order.

DELPHINIDAE

DELPHININAE

Tursiops

MATERIALS.—The specimens of Tursiops trunca-tus consisted of the heads of two adult females anda 53.5 cm male fetus. One adult head and that ofthe fetus were dissected, while the other adult headwas frozen and sectioned coronally at 2 cm intervals.

NASAL PASSAGE AND DIVERTICULA.—The centralstructure in the facial region of odontocetes is thenasal passage. As in all mammals, the nasal passageis a paired structure within the confines of theskull. As the paired passages exit from the skull,they are separated for a short distance by a cartila-ginous nasal septum. Beyond this septum, they fuseinto a single passage and proceed dorsally throughthe soft tissue. The nasal passages and diverticulaare lined throughout with a thin, darkly pigmented,squamous epithelium.

Within the mass of soft tissue on the dorsalsurface of the skull, the nasal passages send off aseries of paired diverticula. In T. truncatus, as inmost small odontocetes, there are four pairs of

these situated in the soft tissues surrounding thenasal passage. These diverticula are distensible tovarying degrees, but are not generally moveablewithin the surrounding tissues.

Immediately dorsal to their exit from the skull,while they are still separated by the septum, thenasal passages send two diverticula, the premaxil-lary sacs (Murie, 1870), anteriorly along the dorsalsurface of the rostrum (Figures 2, 4). The ventralsurface of these diverticula lies directly upon theperiosteum of the premaxillae, while the dorsalsurface is in contact with the nasal plug muscle.These are the largest of the pairs of diverticula inT. truncatus.

The lateral margins of the nasal passages, as theyexit from the skull, are bounded (and slightlyoccluded) by the diagonal membranes (Lawrenceand Schevill, 1956) (Figure 3). These membranesrun at an angle from the anterolateral wall of thenasal passage, just internal to its exit from theskull, posterodorsally to attach to the posterior endof the nasal septum. They are thin membranes,consisting only of the reflected nasal epitheliumwith a slight amount of connective tissue and some-times a few muscle fibers. In T. truncatus, as inmost 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 adja-cent to the external bony nares in Tursiops truncatus.(bnp=bony nasal passage, dm=diagonal membrane, ps=pre-maxillary sac.)

FIGURE 4.—Diagramatic views of the nasal diverticula of Tursiops truncatus: a, oblique view ofthe 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.)


just external to the diagonal membranes, lies a pairof small chambers, the inferior vestibules (Gallar-do, 1913) (Figures 2, 4). These extend dorsally andposteriorly toward the vertex of the skull. A smallmuscle (which will be discussed later) lies beneaththe posterior wall of these chambers. The anteriorwall is formed by the blowhole ligament, whichruns from the anterior tip of the vertex antero-laterally to the lateral edge of the premaxilla.Dorsally the inferior vestibule opens into the naso-frontal sac, laterally into the accessory sac (de-scribed later). Schenkkan (1973) mentioned a"small ventral extension" near the entrance of thenasofrontal sacs to the nasal passage (inferior vesti-bule) in Tursiops. I did not find this in my limitedmaterial, and am unable to interpret its significance.

The nasal plugs (Lawrence and Schevill, 1956)are two fleshy bodies which protrude posteriorlyfrom the anterior wall of the 'nasal passage, justdorsal to the premaxillary sacs (Figures 2, 4). Theyare oval ventrally, where they fit into the bonynares. Their free margins are produced into lips,which fit into the paired inferior vestibules (Fig-ure 2). The body of the nasal plugs consists of thenasal plug muscle (Lawrence and Schevill, 1956),which lies in a dense connective tissue matrix. Thismuscle originates from the premaxilla anterior tothe premaxillary sac. Dorsally it grades into the fatof the melon. In T. truncatus, as in most of theother delphinids examined, the fat of the melonextends only onto the right nasal plug, as notedby Norris (1969) in Delphinus.

Opening laterally from the inferior vestibule isthe accessory sac (Schenkkan, 1971 = connectingsac of Lawrence and Scheville, 1956). This diver-ticulum extends laterally for a short distance, thenturns anteriorly around the attachment of the blow-hole ligament to the premaxilla (Figure 4). It issmaller than the other diverticula, 1 cm or less indiameter and 1 to 2 cm long. It ends blindly in theposterolateral tissues of the nasal plug muscle. Aswith the other diverticula, the accessory sacs arepaired, the right being the larger. The mouth ofthis diverticulum appears to be occluded by a lat-eral extension of the lip of the nasal plug whenthe nasal plug is in place over the bony nares.Schenkkan (1971) pointed out that this diverticu-lum doesn't connect anything, and applied theterm "accessory sac," as the term "connecting sac"was misleading. The structure termed "connecting

sac" by Evans and Prescott (1962), which connectsthe nasofrontal sac with the nasal passage, is prob-ably the inferior vestibule.

The nasofrontal sac (Murie, 1870 = tubular sacof Lawrence and Schevill, 1956) lies in the tissuessurrounding the nasal passage, dorsal to the nasalplugs (Figures 2, 4). It is convenient to speak of ananterior and a posterior part of the nasofrontal sac,with respect to the nasal passage. The posteriorpart ends as a blind sac medially, just posterior tothe nasal septum. It extends, laterally, around theedge of the nasal passage, where it becomes con-tinuous with the anterior part. The blind terminiof both parts abut against the corresponding ter-minus of the contralateral sac. The collapsed diam-eter of this sac is about 1 cm, the length of theright sac about 10 cm, the left about 7 cm. Thereflection of the sac around the lateral edge of thenasal passage is referred to as the angle of the naso-frontal sac. In T. truncatus the angle is slightlylobulated, particularly on the right side (Gruhl,1911). The nasofrontal sac in T. truncatus is darklypigmented throughout its length. The posteriorpart of the nasofrontal sac opens ventrally, bymeans of a transverse slit, into the inferior vestibule.

The blowhole ligament (Lawrence and Schevill,1956) is a strong connective tissue band, runninglaterally from the anterior tip of the vertex to thelateral edge of the premaxilla, just anterior to theaccessory sac. It lies anterior and ventral to thenasofrontal sac, crossing anterodorsal to the com-munication of the latter with the inferior vestibule(Figure 4). It is widest medially, where it forms asubstrate for the attachment of some of the muscu-lature associated with the nasofrontal sacs. Later-ally it becomes narrower and thicker. It sometimesgives off a branch which passes posteriorly, dorsalto the mouth of the accessory sac, and attaches tothe premaxilla just posterior to the accessory sac.Purves and Pilleri (1973), in their description ofPlatanista, found the homoloque of the blowholeligament to be cartilaginous, and considered itequivalent to the crus lateralis of the lower nasalcartilages of terrestrial mammals.

Immediately anterior to the midportion of theblowhole ligament is an elliptical body (Figures10, 16), which seems to be composed of yellowishadipose tissue in a fine connective tissue matrix.This body lies between the blowhole ligament andthe posterior wall of the nasal passage, and pro-

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duces the faint ridge of the posterior fold (descrip-tion follows).

The central portion of the nasal passage, dorsalto the nasal plugs, has generally been referred toin the literature as the spiracular cavity (Figures2, 4). It is into this cavity that the inferior vestibuleopens ventrally and the vestibular sacs (descriptionfollows) open dorsally. In morbid material of del-phinids, this cavity appears as a transverse slitextending from the nasal plugs upward to theblowhole. It has been generally ignored as ananatomical entity in this group, but is importantfrom a comparative standpoint, as it becomeshighly modified in some other odontocetes.

Dorsal to the nasal plugs, the spiracular cavityopens into a pair of lateral diverticula, the vestibu-lar sacs (Lawrence and Schevill, 1956) (Figures 2,4, 6). These are wide flat diverticula, extending lat-erally from the nasal passage in a horizontal plane.They are about 6 cm wide and 4 cm long. In themorbid state the walls of these diverticula are wrin-kled, indicating a certain amount of distensibility.In T. truncatus, as in a few other species, there isan indication of a small anterior lobe on the leftvestibular sac (Figure 24). This may be variableand possibly accounts for the reverse asymmetrynoted by Schenkkan (1973) in one of his specimens.

On the anterior wall of the spiracular cavity, justventral to the vestibular sacs, is a small recess. Thisextends horizontally across the wall of the spiracu-lar cavity and forms a lip (the anterior fold ofLawrence and Schevill, 1956) between it and thevestibular sac (Figure 2). The posterior wall of thespiracular cavity is produced into a slight ridge atthis point (the posterior fold of Lawrence andSchevill, 1956), which fits against the recess in theanterior wall, and is overlain by the anterior foldwhen the nasal passage is closed.

The nasal passage opens onto the surface of thehead through the blowhole. The blowhole iscrescentic, with the concavity facing anteriorly.Seen in cross section, the anterior lip of the blow-hole is convex, fitting into a concavity in the poste-rior wall just ventral to the posterior lip. Theanterior lip of the blowhole is relatively soft andmobile, while the posterior lip is more rigid.

MUSCULATURE.—The musculature associated withthe nasal passage is extremely complex and, untilthe work of Lawrence and Schevill (1956), had notreceived detailed anatomical coverage. Huber

(1934) stated that this muscular complex representsan elaboration of the primitive m. maxillonasola-bialis of mammals. Lawrence and Schevill (1956)recognized six layers within this complex. I havemodified their plan slightly, as I was not able toseparate the muscles consistently according to theirdefinitions (particularly across the wide range ofmorphologic types with which I was dealing). Ihave, however, used their terminology with somemodifications where necessary.

The most superficial of the muscles associatedwith the nasal passage is the pars posteroexternus(pe). This muscle originates along the posteriorhalf of the supraorbital process, the temporal crest,and a variable portion of the nuchal crest (Figure5). It runs medially, posterior to the nasal passage,to insert upon the vertex and into the contralateralmuscle. As is the case with all of the nasal muscles,pe grades into the adjacent musculature. Antero-laterally it is gradational with the pars interme-dius; posteriorly it is gradational with the parsanteroexternus. I have found that I could makeconsistent separations at its insertion, as its fibershave a much more medial orientation that those ofthe underlying muscle. This differs from the defini-tion of Lawrence and Schevill (1956:119) in thatit includes none of the musculature which is indirect contact with the vestibular sac.

The pars intermedius (i) consists of deep fibersfrom the same muscle mass as pe, which divergefrom pe in an anterior direction (Figure 5). Itoriginates deep to pe, along the posterior half ofthe supraorbital process, and inserts into the massof heavy connective tissue dorsal to the nasal plugs.This follows the definition of Lawrence and Sche-vill (1956:121).

The pars anteroexternus (ae) is a much largermuscle than either pe or i (Figure 6). It originatesfrom the anterior end of the supraorbital processto the temporal and nuchal crests and the adjacentbony surface (usually frontal, but occasionallyincluding the maxilla). Posteromedially it occupiesthe fossa between the vertex and the nuchal crest.The anteriormost fibers insert across the midlineinto the contralateral muscle. Posteriorly the fiberscome to insert first upon the anterior wall of thenasal passage, then the lateral edge, and finally theposterior wall and the dorsal edge of the blowholeligament (Figure 6). The vestibular sac is con-tained within this muscle, which is loosely attached

10 SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

to it both dorsally and ventrally. Thus ae presentsa series of fibers converging upon the nasal pass-age. Lawrence and Schevill (1956:122) defined aeas only the anterior portion of the muscle describedabove. Since I could find no consistent separationinto an anterior and a posterior portion, and, asthe modified definition seems to result in a func-tional entity, I have redefined this muscle.

Ae is most easily defined in dissection at its pos-terior insertion, where its anteriorly directed fiberspresent a marked contrast to the underlying fibersof the pars posterointernus. Although the direc-tions of these two sets of fibers are quite different,they are thoroughly intermeshed, forming an apo-neurosis just dorsal to the nasofrontal sacs. Ae canbe separated from the pars posterointernus at itsinsertion, but merges with it along its origin. Ante-riorly ae becomes continuous with the underlyingfibers of the pars anterointernus at both origin andinsertion, and also with the posterior fibers of therostral muscle.

The pars posterointernus (pi) lies just deep toae, taking its origin from the frontal (and/or max-illa) at the level of the eye (middle of the supra-orbital process) (Figure 7). Its origin extendsposteriorly, then medially into the fossa betweenthe nuchal crest and the vertex. It inserts via aflat tendon, which runs in an arc posterior to thenasal passage, into the contralateral muscle and theaponeurosis formed with the fibers of insertion ofae. Lawrence and Schevill's definition of pi (1956:123) includes only the posterior portion of what Ihave called ae. I cannot find a muscle or portionof a muscle in their description corresponding towhat I have defined as pi. Accordingly, I wastempted to substitute a new name to avoid con-fusion, but felt that this would require a completesubstitution for their names, which form a topo-graphic system. I have found this system to beparticularly useful, and so have retained it, com-pletely redefining pi.

Pi is easily separated at its insertion from therest of the muscles, although at its origin it isindistinguishable from both the overlying (ae) andunderlying (ai) muscles.

The deepest and largest of the muscles associatedwith the nasal passages is the pars anterointernus(ai). This muscle takes its origin from a broad areaof the ascending process of the maxilla, betweenthe origins of ae and pi and the lateral border of

the premaxilla (Figure 8). It is indistinguishableanteriorly from the medial rostral muscle. In orderto separate these two, I have arbitrarily drawn aline from the anterior end of the supraorbital crestmedially to the premaxilla, and have called every-thing posterior to this line pars anterointernus.The insertion of this muscle is into the connectivetissue mass anterior to the nasal passage, andthrough it to the contralateral muscle. This muscleis fanshaped, the posterior fibers running anteriorlyacross the midline, the lateral fibers passingdirectly medially and the anterior fibers runningposteriorly. A few of the deep anterior fibers of ai,instead of inserting across the midline anterior tothe nasal passage, cross the fibers of insertion ofthe posterior portion of the muscle and attach tothe lateral edge of the nasal passage. This defini-tion represents a fusion of the pars anterointernusand the pars profundus of Lawrence and Schevill(1956:123-126).

The rostral musculature consists of an elongateblock lying along either side of the rostrum (Figures8, 9). In transverse section this is seen to consist offibers radiating from a central area of origin alongthe maxilla into the tissue of the lip, dermis, andmelon. This block of muscle can be divided intotwo portions, with slightly differing fiber orienta-tion. These are a lateral portion, primarily asso-ciated with the lip and the connective tissue adja-cent to the melon, and a medial portion, whichinserts into the melon (Figure 9). The separationbetween these two portions is seen in transversesection as a diffuse zone of connective tissue. If thisseparation is followed posteriorly, it becomes appar-ent that the lateral portion is continuous with thesuperficial musculature of the nasal passage (pe, i,ae and pi), while the medial portion is continuouswith the deep musculature (ai). This separationbecomes quite striking at the level of the antorbitalnotch, where there is frequently a strong ridgeproduced on the maxilla along the line of separa-tion of the two parts.

The separation of the rostral muscle into lateraland medial parts, continuous with different por-tions of the nasal musculature, raises the questionof the homologies of these muscle blocks. Huber(1934) considered the posterior musculature to behomologous with the parts nasalis of the m. maxil-lonasolabialis, while the rostral musculature wasconsidered to be homologous with the pars labialis

NUMBER 207 11

of that muscle. The continuity of the rostral mus-culature with the posterior musculature suggeststhat if a division is to be made, it is between medialand lateral elements, not anterior and posterior.

While this is a question best approached throughdevelopmental studies, it seems useful to tentativelydesignate the lateral rostral musculature and itsassociated nasal musculature (pe, i, ae and pi) as

ae

FIGURE 5.—Oblique view of the superficial nasal musculature of Tursiops truncatus. (ae = parsanteroexternus, 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 deeperlevel than Figure 5. Pars posteroexternus, pars intermedius, and part of pars anteroexternusremoved to expose the vestibular sacs. (ae = pars anteroexternus, rm = rostral muscle, vs = vestibu-lar sac.)


derivatives of the pars labialis and the medialrostral musculature and ai as derivatives of thepars nasalis of the m. maxillonasolabialis.

These descriptions are complicated and confus-ing, and a genreal summary may be useful at thispoint. The most superficial muscle, pe, runs from a

ns

ai

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

dmmim

ns

rm

FIGURE 8.—Oblique view of the deep nasal musculature of Tursiops truncalus. Pars postero-internus completely removed. (ai = pars anterointernus, dmm = diagonal membrane muscle,im = intrinsic muscle, ns = nasofrontal sac, rm = rostral muscle.)

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lateral origin to a medial insertion, posterior tothe nasal passage. Ae lies immediately under peand consists of fibers converging upon the nasalpassage from the margins of the facial region. Be-tween these two muscles, and continuous at itsorigin with both of them is i. This muscle differsfrom ae and pe in having a more anterior inser-tion, and thus a different fiber direction. Pi is con-tinuous at its origin with ae, but differs in havingan 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 andai are continuous anteriorly with each other andwith the rostral musculature. Posteriorly ae and aiare separated by pi.

Associated with the vertex and the nasofrontal

sacs are a series of small muscles whose relation-ships are difficult to demonstrate. The muscle fibersare extremely fine and permeated with an equallyfine connective tissue matrix which grades into theconnective tissue of the adjacent structures. Law-rence and Schevill (1956) refer to this group ofmuscles as the intrinsic musculature (of the naso-frontal sac). They separate it into a major portionlying posterior and lateral to the nasofrontal sacs,and a minor portion lying anterior. I have foundthe two to be continuous, and refer to the portionsdescribed by them merely as the intrinsic muscle(of the nasofrontal sac) (Figure 8).

In T. truncatus this muscle originates from theanterodorsal surface of the vertex and the medialend of the nasofrontal sac. It passes laterally, alongthe anterior, ventral, and posterior aspects of the

FIGURE 9.—Cross sections of the rostral structures of Tursiops truncatus (adult female): a, 10cm posterior to the tip of the rostrum; b, 14 cm posterior to the tip of the rostrum; c, 18 cmposterior 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 mus-cle, rm-l=lateral portion of the rostral muscle, rm-m = medial portion of the rostral muscle.)


nasofrontal sacs, occasionally completely encom-passing the sac. Throughout its length, its connec-tive tissue matrix is closely associated with that ofthe adjacent structures, particularly the nasofrontalsac and blowhole ligament. It passes on either sideof the communication of the nasofrontal sac withthe inferior vestibule, then turns anteriorly, enter-ing the dorsolateral surface of the nasal plug massand merging with the nasal plug muscle.

Posterior and ventral to the intrinsic muscle liesanother small muscle of similar composition. Dueto the complexity of this region, this muscle hasescaped the attention of earlier workers. It origi-nates from the anterolateral surface of the vertex,lateral and deep to the intrinsic muscle. It thenpasses anteriorly, ventral to the intrinsic muscleand nasofrontal sac, to insert along the attachedmargin of the diagonal membrane. Very rarely itsends a few fibers into the free portion of the mem-brane. Due to the connective tissue in'which thesemuscles are imbedded, it is difficult to ascertainthe exact relationship of this muscle to the intrinsicmuscle. In some specimens it appears to be sharplydelimited from the intrinsic muscle, while in othersit seems to be continuous with it. I have designatedthis the diagonal membrane muscle, in referenceto its insertion.

MELON.—A frequent problem in the literaturedealing with the odontocete nose is the distinctionbetween melon, adipose cushion, spermaceti organ,and case. At one time or another, all of thesenames have been applied to the adipose connectivetissue structure anterior to the nasal passage indelphinids.

"Melon" is a term apparently originating in thewhaling industry, referring to the similarity of thismass of tissue, when it is removed from the headof the animal, to a section of melon (particularlyin Globicephala, where it resembles a section ofripe muskmelon).

"Adipose cushion" is a term coined by Howell(1930), who evidently did not care for the collo-quial nature of "melon." He described this struc-ture in some detail and specifically indicated thathe was referring to the smaller odontocetes.

The term "case" is another which has originatedin the whaling industry, where it was used in refer-ence to the oil-filled cavity in the head of the spermwhale.

Pouchet and Beauregard (1885) apparently orig-

inated the term "spermaceti organ" in reference tothe structure more colloquially known as the case.

Howell (1930) discussed the possible homologyof the adipose cushion (melon) and the spermacetiorgan (case), and decided that they were probablyunrelated. Raven and Gregory (1933), however,were of the opinion that they were homologous,and applied the term "spermaceti organ" to thestructure seen anterior to the nasal passages inMonodon. This structure, however, appears to beno different from the adipose cushion (melon) ofdelphinids. Schenkkan and Purves (1973) examinedthe anatomy of the nasal complex in physeteridsand concluded that the spermaceti organ in Physe-ter and Kogia was unrelated to the melon ofdelphinids.

Despite the rather colloquial flavor of the term"melon," it has been frequently and consistentlyused in the literature, and I have elected to retainit as applied to delphinids. This is specificallyequivalent to the term "adipose cushion" of Howell(1930). I have not used Howell's term because ofits functional implications. The functions of thisstructure are still not well enough understood thatwe can afford to hamper our reasoning with termsimplying a specific function.

The term "spermaceti organ" should be restrictedto a distinct fatty body, separated from the otherfacial structures by a connective tissue wall, as seenin Physeter. The free usage of these terms in thepast few years has led to considerable confusionas to which animals have a spermaceti organ andwhich do not.

The melon lies approximately in the center ofthe soft tissue mass of the face (Figures 2, 9). Lat-erally it grades into the rostral muscle and ventrallyinto the nasal plug muscle. In some dissections, asharp distinction can be seen between the dorsalsurface of the melon and the adjacent connectivetissue of the dermis. This distinction seems to bemainly on the basis of orientation and distributionof blood vessels, the melon being less vascular thanthe dermis. This is sometimes accentuated uponexposure of a section to the air, the melon and thedermis apparently oxidizing differently. This differ-entiation continues anteriorly, separating the der-mis from the melon. Posteriorly the melon gradesinto the nasal plug mass, penetrating into the tissueof the right nasal plug.

Litchfield et al. (1973) have demonstrated topo-

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graphic variation in the lipid content of the melon,while Norris and Harvey (1974) have shown asimilar variation in acoustic properties of themelon.

VASCULATURE.—The vascular supply of the facialregion in T. triincatus (as in the other delphinids)is derived from blanches of the internal maxillaryartery emerging from the infraorbital foramina.Branches from the posterior infraorbital foraminaramify between the layers of the nasal musculatureand supply most of the region posterior to theantorbital notch. A bundle of parallel vessels arisesfrom one of the anterior infraorbital foramina, justmedial to the antorbital notch, and courses ante-riorly on the surface of the maxilla. At intervalsthese vessels turn dorsally to supply the rostralstructures. The facial artery is small and appearsto supply only the area around the angle of themouth and, to a lesser extent, the tissue of theupper lips. There is a prominent vascular systemin the superficial fascia over the nasal musculature,which appears to be largely venous. It communi-cates posteriorly with occipital vessels and laterallywith temporal vessels.

None of the facial elements are heavily vascu-larized, the most prominent vasculature being thatof the posterior superficial fascia mentioned above.The melon is markedly avascular, the large vesselsseen in its periphery being destined for the skin.

INNERVATION.—The sensory innervation of thefacial structures is derived from infraorbitalbranches of the maxillary division of the trigemi-nal nerve. These emerge onto the surface of theface through the various infraorbital foramina. Pos-teriorly, large branches of these nerves pass to thenonmuscular structures associated with the nasalpassage, particularly the nasal plugs and the deepstructures around the vertex. The diverticula donot appear to be heavily innervated, nor does themelon (contra Huber, 1934). Khomenko (1970)reported encapsulated nerve endings in the wallsof the diverticula, but did not state that they wereparticularly abundant. The skin is known to beheavily innervated (Palmer and Weddell, 1964),but the patterns of this innervation could not bedetermined grossly. Presumably the cutaneousinnervation is also derived from the infraorbitalbranches of the trigeminal nerve, although occipitalnerves were seen to extend into the facial area ina fetal T. truncatu.s. There are extensive anasta-

moses between elements of the facial and trigeminalnerves, particularly between the layers of the nasalmusculature near their origins.

So far as is known, all of the motor innervationof the nasal muscles is provided by the facial nerve.This nerve passes anteriorly, beneath the orbit, toemerge onto the face through the antorbital notch.The facial nerve is heavily invested with connectivetissue throughout its length and is easily mistakenfor a tendinous structure. As it passes through theantorbital notch it branches extensively in thedense connective tissue filling the notch. Beyondthis point it has a diffuse distribution throughoutthe layers of the facial muscles.

GLANDULAR STRUCTURES.—Glandular tissue hasrecently been discovered in the area of the inferiorvestibule in T. triincatus (Maderson, 1968; Evansand Maderson, 1973). These are small exocrineglands, opening via minute crescentic pores. I over-looked these in my dissections, and it is possiblethat their distribution throughout the delphinidsis more extensive than is now known.

The following descriptions of delphinid generaare based upon comparison with T. truncatus, and,in general, only the differences observed are treatedin any detail. The genera are treated in an appoxi-mate taxonomic order, with those most similar toTursiops being described first.

Stenella

MATERIALS.—Forty-four individuals of Stenellaattenuata and S. longirostris were dissected, rangingin size from neonates to large adults. Two adultmales of S. coernleoalba and one adult male of S.plagiodon were also dissected.

The species of Stenella examined show very littledifferentiation from the condition seen in Tursiopstruncatus, and constitute a relatively homogenousgroup in their facial anatomy.

NASAL PASSAGES AND DIVERTICULA.—The premax-illary sac in Stenella was quite uniform in thespecies examined, and was similar to that of T.truncatus (Figure 24). The only difference notedwas a slight increase in the asymmetry of thisstructure in S. cocruleoalba.

The nasal plugs showed little variation in Ste-nella, the right plug always being the larger andhaving a proportionately larger lateral lip. As with

16SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY

a

FIGURE 10.—Dorsal views of dissections of the nasal musculature of Stenella plagiodon (in eachview 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 postero-externus, pi = pars posterointernus, rm = rostral muscle, vs = vestibular sac.)

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a number of characters, this asymmetry was slightlygreater in S. coendeoalba.

An accessory sac was present in all of the Stenellaexamined. This sac was quite small, on the orderof 5 mm or less in length in all but S. coendeoalba,where it was slightly more than 1 cm long. A poste-rior branch of the blowhole ligament, passing overthe mouth of the accessory sac, was seen in someindividuals of all of the Stenella species. It wasonly seen on the left side.

The nasofrontal sac showed some variation inthe Stenella species. The posterior portions abutagainst one another at the midline, as in T. trun-catus. The anterior portions also meet in the mid-line and actually overlapped by about 1.5 cm inthe only specimen of 5. plagiodon examined. Inthis instance the right sac lay dorsal to the left.The pigmentation pattern of these sacs is highlyvariable, and was not seen to fit any particularscheme. The posterior portions are nearly alwaysdarkly pigmented, but were light colored in somespecimens of S. attenuata and 5. longirostris. Theanterior portions are more variable. A commonsituation was that in which the entire left anteriorportion was dark, while the medial portion of theright was unpigmented. In addition to being longer,the right anterior portion was slightly wider thanthe left, more so in S. coendeoalba.

The vestibular sacs are of moderate size in Ste-nella, the left being somewhat larger than the rightin S. attenuata and S. longirostris. The left sac wasalso situated more anteriorly than the right inthese two species. This was not the case in S. coeru-leoalba and S. plagiodon, where the sacs wereroughly equal and both lay slightly more anteriorto the nasal passage. The anterior fold of the rightvestibular sac was consistently larger than the leftin S. attenuata and S. longirostris, the right usuallybeing 1.0 to 1.5 cm wide, while the left was 0.2 cmor 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 ante-rior fold was extremely large, 2.0 cm wide, whilethe left was on the order of 0.2 cm.

MUSCULATURE.—Outside of minor individualvariation in the extent of origin of layers of theposterior musculature, and in the relative size ofsome of these layers, there were no observabledifferences 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 toconsiderable variation in Stenella. It is generallylarger on the right side, although the reverse wastrue in one S. attenuata. As it passes ventral to theblowhole ligament, a few fibers may attach to theligament. There is considerable variation in theextent to which this muscle enters the diagonalmembrane. As in T. truncatus, it usually does not.However, in one specimen of S. attenuata the mus-cle on the left side extended to the free edge of themembrane, while that on the right did not enterthe membrane at all. In another specimen of S.attenuata a few of the lateral fibers of both musclesentered the free portion of the membrane. Thismuscle was extremely large in S. coeruleoalba, butdid not enter the free portion of the membrane.

OTHER STRUCTURES.—The anterior rostral struc-tures, both the muculature and the melon, showedno noticeable variation throughout the Stenellaspecies, nor any appreciable differences from thecondition seen in T. truncatus.

Delphinus

NASAL PASSAGES AND DIVERTICULA.—The arrange-ment of the nasal apparatus in Delphinus delphisis very similar to that of Tursiops and Stenella, asshown by Gruhl (1911), Lawrence and Schevill(1956), and Schenkkan (1973). Gruhl's work isparticularly useful, as he illustrated the diverticulain a number of individuals, including a fetus.

The vestibular sac is very similar to that ofTursiops and Stenella, particularly in the presenceof a small anterior lobe on the left side.

The nasofrontal sac is virtually indistinguishablefrom that of Stenella, and does not have the lobu-lations seen on the angle of the right sac in T.truncatus. Gruhl's illustration of the nasofrontalsac of a 53.8 cm fetus is of interest, in that it showsa marked asymmetry in the degree of developmentof the right and left sacs, the right sac developingits anterior portion more rapidly than the left. Theaccessory sac is similar to that of T. truncatus, andis slightly larger than that of all of the Stenellaspecies, except S. coeruleoalba.

MUSCULATURE.—The musculature appears to beno different from that of Tursiops.


OTHER STRUCTURES.—The melon and the rostral

structures are similar to those of Tursiops.

Lagenorhynchus

MATERIALS.—One juvenile Lagenorhynchus albi-rostris and a juvenile L. acutus were dissected.

NASAL PASSAGES AND DIVERTICULA.—The premax-illary sacs of L. albirostris differ from those of Tur-siops and Stenella in having a lateral diverticulumon the right side (lateral premaxillary sac). Thisdiverticulum opens along the middle two-thirds ofthe 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 poste-rior margin of its orifice (Figure 14). This structurewas either very small or lacking on the left. Noth-ing similar to this diverticulum has been seen inany of the other dissections, except that of a juve-nile Lagenodelphis hosei. Schenkkan (1973) did notmention this diverticulum, though he dissectednine specimens of this species. Its presence in thesingle specimen which I examined might be con-sidered anomolous, were it not also seen in a juve-nile Lagenodelphis hosei. There was but a traceof it, however, in an adult female Lagenodelphishosei, raising the possibility that it may be a juve-nile character which is lost with age. This diver-ticulum was absent in the single L. acutus specimenwhich I dissected, and is not mentioned in Schenk-kan's account of this species. It also seems to belacking in L. obliquidens and L. obscurus (Schenk-kan, 1973).

The nasofrontal sacs in L. albirostris are extremelydifferent from most of the other delphinids. In thespecimen examined, these were injected withsilastic rubber, so some idea of their distended sizewas gained. The posterior portion of the nasofron-tal 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 ofthe sacs, and the sacs do not overlap one another.In this specimen the anterior portion of the leftnasofrontal sac lay on the lateral surface of thenasal plug mass, while that of the right extendedonto the anterior surface, crossing the midline. Theright sac appeared to be about twice the size of theleft, although neither was expanded to its maxi-mum extent. The distension of the sacs was limitedmore by the adjacent tissues than by the dimen-

sions of the sac itself. Murie (1871) apparentlyoverlooked the nasofrontal sacs in his descriptionof L. albirostris. Schenkkan (1973) found the samecondition in the L. albirostris which he dissected.Hypertophy of the nasofrontal sacs is* apparentlylimited 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 ofTursiops.

The accessory sacs in the specimen of L. albiros-tris which I dissected were relatively large, par-ticularly the right sac, which measured 3 cm longby 1 cm wide. Schenkkan (1973) also noted thatthese diverticula were large in this species, anddescribed a caudal portion extending posterior totheir communication with the inferior vestibule.He noted a similar caudal extension on the rightaccessory sac in L. acutus, though I did not findthis in the single specimen which I dissected. Theaccessory sacs in L. obliquidens and L. obscurus areessentially similar to those of Tursiops (Schenkkan,1973).

The vestibular sacs of L. albirostris presented nopronounced differences from those of Tursiops. Theanterior folds were large on both sides, that on theright being about 1.5 cm wide, the left 1.0 cm. Thefolds usually seen in the walls of the vestibular sacwere 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 sacsin L. albirostris were thickened, which probablycorrelates with my observations on folding. Schenk-kan (1973) described extensive tabulation in thelateral edge of the vestibular sacs in L. acutus, andI found a similar condition in the specimen whichI dissected. He also noted that their placement wasmore caudal to the blowhole, which agrees withmy dissection. Schenkkan's (1973) specimen of L.obliquidens was damaged, but did not appear topresent any major differences from Tursiops.Schenkkan (1973) noted a reverse asymmetry in thevestibular sacs of L. obscurus, the left being largerthan the right, though apparently to no greatextent, as it is not apparent in his illustration ofthis species. Gallardo's (1913) comments are toobrief 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 themidline, with only a few fibers attaching to thevertex. There was no discernible i on either side.The tendons of insertion of ae and pi formed moreof an aponeurosis than in T. truncatus, and weremore intimately attached to the connective tissueabove the posterior end of the nasal septum. Thenasal musculature in L. acutus presented nodiscernible differences from that of Tursiops.

The intrinsic muscles, the muscle of the diagonalmembrane, and the membrane itself in both speciesexamined presented no differences from those ofT. truncatus. Nor did the nasal plugs show anyunusual features.

OTHER STRUCTURES.—The structures of the rost-rum showed a few differences from those of T.truncatus. The distinction between the medial andlateral rostral muscles was greater in L. albirostris.There was an area of extremely dense connectivetissue in the dermis just anterior to the blowhole.The connective tissue in this area is ordinarilyslightly denser than in the rest of the dermis, butnot as strikingly so as in this specimen.

Lagenodelphis

MATERIAL.—A juvenile male and an adult femaleof Lagenodelphis hosei were dissected.

NASAL PASSAGES AND DIVERTICULA.—The premax-illary sac possessed a small diverticulum on theright side (lateral premaxillary sac) similar to thatseen in Lagenorhynchus albirostris (Figure 13).This was more pronounced in the juvenile male,hence may be related either to age, sex, or individ-ual variation. Otherwise the premaxillary sacs weresimilar to those of Tursiops truncatus.

The accessory sac was very small on the left,appearing as a slight indentation in the lateral wallof the inferior vestibule. That on the right wasquite large, extending 1 cm anterior to the blow-hole ligament.

The nasofrontal sacs were similar to those ofT. truncatus. While the right sac was larger thanthe left, neither showed any sign of the expansionseen in Lagenorhynchus albirostris. The two sacswere darkly pigmented throughout, met anteriorto the nasal passage in the juvenile, and overlappedanteriorly by about 1 cm in the adult. The angleof 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. trun-catus, ending very close to the lateral edge of thenasal passage. The portion of the sacs posterior tothe nasal passage was larger than the portion ante-rior. The anterior fold was quite large on the right,comparable to the condition seen in Lagenorhyn-chus albirostris and Stenella coeruleoalba.

None of the deep structures associated with thenasal passage (intrinsic muscles, diagonal mem-brane and muscle, blowhole ligament, and nasalplugs) were noticeably different from those of T.truncatus.

MUSCULATURE.—The nasal musculature of L.hosei showed no outstanding differences from thatof T. truncatus. Pe was well developed and insertedacross the midline between the vertex and the nasalpassage. Its origin extended further posteromediallythan in T. truncatus, making it a little more diffi-cult to separate from ae. There appeared to be nodifferentiation of a pars intermedius. The super-ficial fibers of ae had a more anterior orientationthan in T. truncatus, but this became more medialin the deeper layers. The posterior insertion of aewas less well differentiated than in T. truncatus.

OTHER STRUCTURES.—The only noticeable differ-ence from T. truncatus in the rostral structureswas a sharper differentiation of the rostral muscu-lature into medial and lateral portions. The melonshowed no unusual features.

Grampus

MATERIALS.—One adult male of Grampus griseuswas dissected.

NASAL PASSAGE AND DIVERTICULA.—The right pre-maxillary sac is disproportionately larger than theleft in G. griseus (Figure 25). This increase hastaken place in the posterolateral portion of the sac,where the additional space is occupied by an un-usually large lateral lip of the nasal plug. Thelateral lip on the right side is about 2 cm wide,while that of the left side is only 0.5 cm. There areno lateral diverticula from the premaxillary sac,and, aside from the lateral lip, the nasal plugs wereas in Tursiops truncatus.

The accessory sac was somewhat larger than thatof T. truncatus, the right one being 2.0 cm long,the left 1.5 cm long. None of the previous workers


ae

FIGURE 11.—Grampus griseus (dissection of the nasal muscu-lature, dorsal views): a, superficial muscles removed to levelof vestibular sacs; b, ae removed; c, pi removed. (ae = parsantcroexternus, ai = pars anterointernus, ns = nasofrontal sac,pi = pars posterointernus, sc = spiracular cavity, v = vertex,vs = vestibular sac.)

(Murie, 1870; Bouvier, 1889; Danois, 1911) mentiona structure which could be interpreted as this sac.

The nasofrontal sacs present some striking differ-ences from those of T. truncatus (Figures 11, 25).The posterior portions of the sacs are similar tothose of T. truncatus, but the anterior portion ofthe right sac is considerably larger, though notnearly so much as that of Lagenorhynchns albiros-tris. The greatest difference is seen on the left side,where the anterior portion was lacking, the poste-rior portion ending about 1 cm lateral to the edgeof the nasal passage. Murie (1870) described essen-tially the same situation in the specimen of G.griseus examined by him. His illustration of thediverticula, however, appears to be slightly in error,and gives the impression that the anterior portionof the right nasofrontal sac opens into the inferiorvestibule independent of the posterior portion.This gave rise to Bouvier's (1889) mention of a"sac facial impair," which added to the confusionsurrounding the nasal diverticula.

The vestibular sac of G. griseus was unusual inthat the left was larger than the right by about10%, and extended farther laterally (Figure 25).Both vestibular sacs lay more posterior to the nasalpassage than in T. truncatus. The anterior foldswere not particularly unusual, that of the right sidebeing about 0.8 cm wide, while that of the left wasbarely discernible.

MUSCULATURE.—The intrinsic musculature of thenasofrontal sac was slightly larger than in T. trun-catus, and its gradation into the lateral portion ofthe nasal plug muscle was more clearly seen. Alongits posteromedial origin some of its fibers interdigi-tated with fibers of the diagonal membrane muscle.Otherwise the two were quite distinct. The diag-onal membranes were of approximately equal size,and neither muscle reached the free edge of themembrane. Murie (1870) seems to have been theonly author to notice the difference between theintrinsic muscle and the muscle of the diagonalmembrane. The muscle labeled " 1 " in his figure 1appears to represent the latter muscle, although hedid not discern its insertion into the diagonalmembrane.

The pars posteroexternus of G. griseus differsmarkedly from that of T. truncatus (Figure 11).It originates from the posterior fourth of the supra-orbital process, runs posteromedially along thetemporal crest, and inserts upon the lateral portion

NUMBER 207 21

of the nuchal crest. This muscle was about twiceas large on the left as it was on the right. The fibersof pe were heavily invested with fat and connectivetissue, giving an appearance unlike the rest of theposterior nasal musculature. On its deep surfaceit was gradational with ae. A small superficial slipof muscle on the anterior surface of ae may haverepresented a poorly differentiated i. Pi was unusualin that there was a deep posterior portion whichoriginated from the lateral surface of the vertex,medial and deep to the posterior origin of ai. Nor-mally pi originates entirely posterior and superficialto ai.

The rostral muscles were considerably differentfrom those of T. truncatus. They were larger thanin that species, particularly the medial portion(Figure 12). The differentiation between the lateraland medial portions was sharper in G. griseus thanin T. truncatus. This differentiation is associatedwith a strong crest along the lateral edge of themaxilla, which marked the separation of the twomuscle bodies.

OTHER STRUCTURES.—The melon of G. griseus ismuch larger than that of most delphinids (Figures12, 25). This is particularly true in the postero-lateral portions, producing a slightly bilobate,bulbous forehead. The expansion of the foreheadis largely due to an increase in the size of themelon, with little corresponding increase in theheavy dermal connective tissue external to it. Theresult is a very soft mass of tissue, in marked con-trast to the other bulbous-headed genera which Ihave examined.

Aside from some of the points mentioned above,this description agrees with that of Murie (1870).Bouvier (1889) merely compiled data from earlierliterature. The description of a 125 cm fetal G.griseus by Danois (1911 is confused with regardto the nasal diverticula. He illustrated whatappears to be the posterior portions of both naso-frontal sacs, and shows nothing which could be ananterior portion. This might be due to the stageof development of the specimen, although it wasrelatively large. It will be recalled that the anteriorportion of the right nasofrontal sac was well devel-oped in a 53.8 cm fetus of Delphinus delphisdescribed by Gruhl (1911).

There is some confusion introduced into the lit-erature 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 therostral structures, superficial dissection of the nasal muscu-latue, oblique view; b, parasagittal section of the rostralstructures, same view as above, 5 cm lateral to above sec-tion; c, transverse section of rostral structures at level ofantorbital notch. (ae = pars anteroexternus, dct = dermal con-nective tissue, i = pars intermedius, m = melon, pe = pars pos-tcroexternus, r = rostrum, rm = rostral muscle, rm-l=lateralportion of rostral muscle, rm-m = medial portion of rostralmuscle; heavy lines indicate principal orientation of connec-tive tissue fibers in the melon.)

22

sacs. From this they could be interpreted as beingthe accessory sacs. Murie also mentioned that thenasofrontal sac opened into the maxillary sac,which would further support this conclusion. How-ever, in his description of L. albirostris (1871), the"maxillary sac" is clearly equivalent to the vestibu-lar sac. Danois (1911) follows Murie in his illustra-tion ("inspire de Murie") and shows the "sacsmaxillaires" as lying deep to the nasofrontal sacs.I am of the opinion that the maxillary sacs areequivalent to the vestibular sacs in both Murie'sand Danois' accounts, and that both were in erroras to their position. This seems more likely thanthat both of them had missed the large vestibularsacs and were describing the accessory sacs instead.Further confusion arose as a result of Danois' label-ing the spiracular cavity (bony nasal passages) ofMurie as spiracular sacs, and describing them asthough they were diverticula. It is clear that muchof this derives from Danois' misunderstanding ofMurie's illustration.


ORCININAE

Orcinus

MATERIALS.—One large adult male and an adultfemale of Orcinus orca were dissected.

NASAL PASSAGE AND DIVERTICULA.—The premax-illary sacs of O. orca show no unusual features, and,if anything, are relatively small. The diagonal mem-brane of the right is slightly larger than that onthe left.

The accessory sacs are small, relative to the sizeof the animal. The right sac was about 3 cm long,the left about half that size.

The anterior portion of the right nasofrontal sacwas 2-3 times the diameter of the left. The poste-rior portions of the nasofrontal sacs were notnotably larger in diameter than the left anteriorportion and were considerably smaller than theright. Schenkkan (1973) stated that the posteriorportions were larger in diameter than the anterior

FICURE 13.—Orcinus orca: a, nasal musculature, dorsal view of the superficial dissection; b, nasalmusculature, dorsal view of dissection to level of vestibular sac. Dorsal wall of vestibular sacremoved, (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 termina-tions did not reach the mesial axis of the head,whereas they met anteriorly in both of my speci-mens. Gruhl (1911) noted that the anterior por-tions of the nasofrontal sacs developed later thanthe posterior in a series of Delphinns delphis whichhe examined. Thus the differences between myresults and those of Schenkkan may merely reflectage differences.

The vestibular sacs lay considerably posterior tothe nasal passage, quite different from their situa-tion in Tursiops and Stenella. Schenkkan (1973)stated that they lay lateral to the blowhole,although his illustration shows them lying poste-rior, similar to the situation in my dissections.They were subequal in size, the left being slightlylarger. There was a small anterior fold on the leftand a very large one (2 cm deep) on the right.

MUSCULATURE.—The nasal musculature of O. orcaexhibited a few peculiarities. The pars posteroex-ternus was well defined, inserting across the mid-line 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 struc-tures. (bv = blood vessel, dct = dermal connective tissue, m =melon, npm^nasal plug muscle, r = rostrum.)

fibers of ae arising posterior to the blowhole andinserting anterior to it. This is in marked contrastto the rest of the delphinids. The posteromedialfibers of ae inserted into the heavy posterior wallof the nasal passage, instead of into the blowholeligament. However, as they were heavily inter-twined with the posteromedial fibers of pi whichdid insert upon the blowhole ligament, the func-tional insertion was unchanged.

The anterior portion of the intrinsic muscula-ture ran diagonally across the dorsal surface of thenasofrontal sac, but assumed a more parallel course,grading into the rest of the muscle on the ventralsurface. The diagonal membrane muscle was con-tinuous posteriorly with the intrinsic muscle. Inthe large male the diagonal membrane muscle didnot enter the free portion of the membrane, butdid in the female.

The nasal musculature of Orcinus is generallysimilar to that of Tursiops, and shows no particu-lar resemblance to Phocoena, as implied by Schenk-kan (1973).

OTHER STRUCTURES.—The rostral structures in O.orca were relatively small (Figure 14). The medialand lateral rostral muscles were well differentiated,the latter entering the lips more than in otherdelphinids. The melon was small and poorly differ-entiated. Its entry into the nasal plugs was stronglyasymmetrical, showing a clear fatty area on theright side.

Pseudorca

MATERIALS.—An adult male and an adult femaleof Pseudorca crassidens were dissected.

NASAL PASSAGES AND DIVERTICULA.—Pseudorcacrassidens is similar to Tursiops truncatus in theanatomy of the facial structures. The premaxillarysacs and nasal plugs present no unusual features,nor do the nasofrontal sacs (Figures 25). The rightaccessory sac is about 2 cm long, the left is muchsmaller. A small posterior branch of the blowholeligament was seen on the right side. The vestibularsacs lie mostly posterior to the nasal passage, andare relatively small.

MUSCULATURE.—The pars posteroexternus of thenasal musculature was poorly differentiated. Therewas, however, a large pars intermedius. The rest ofthe musculature was similar to that of T. truncatus.

The rostral muscles are relatively small, the lat-


eral rostral muscle entering into the lips more thanin most delphinids.

OTHER STRUCTURES.—The melon is surprisinglysmall, the bulk of the facial mass being made up ofcoarse dermal connective tissue in a fatty matrix.There is a well-defined connection between themelon and the right nasal plug.

A moderate degree of sexual dimorphism wasobserved in the shape and size of the forehead inPseudorca (Figure 15). In the male the fatty con-nective tissue anterior to the melon extended far-ther anteriorly than in the female. No differencecould be seen in the melon, which is not well-defined in this species. A similar situation is seen

a

FIGURE 15.—Pseudorca crassidens, lateral views of the exter-nal appearance of the heads, showing the degree of sexualdimorphism in external head shape: a, female; b, male.

in the illustrations of a saggital section of the fore-head tissues of a male Pseudorca presented byRichard (1936, pi. VI: fig. 10). A comparable situa-tion exists in Globicephala, where the fatty con-nective tissue of the forehead is more extensive inthe adult males than in the females.

Globicephala

MATERIALS.—A large adult male and a neonateof Globicephala melaena were dissected.

NASAL PASSAGES AND DIVERTICULA.—The premax-illary sacs and nasal plugs of G. melaena are similarto those of Tursiops tnincatus, as is the diagonalmembrane.

The accessory sac on the right side is extremelylarge, 4 cm long and 2 cm wide (Figures 16, 24),while that of the left side is about 1 cm long by1 cm wide.

The angle of the right nasofrontal sac in G.melaena is extremely unusual (Figure 16). Thereis a large lateral sacculation, which, when opened,contains a series of trabeculea. These trabeculaeare formed by invaginations of the lateral wall ofthis diverticulum containing slips of the intrinsicmusculature. This may allow the intrinsic muscu-lature to compress this sacculation without affect-ing the rest of the diverticulum. The anteriorportion of the right nasofrontal sac is slightlyexpanded, and is unpigmented in its medial half.The anterior portions of the two sacs abut againstone another. The posterior portion of the left naso-frontal sac has an elongate posterior sacculationalong its posterodorsal surface. Internally this sac-culation is separated from the rest of the sac by afold of epithelium.

The vestibular sacs are roughly equal in size.They extend a short distance anterior to the nasalpassage, where they slope into the anterior lip ofthe blowhole. Their greatest extent is posterolateralto the nasal passage. The anterior folds are welldeveloped on both sides, the cleft beneath thembeing about 1 cm deep. The anterior fold over-hangs the slit of the nasal passage by 1.8 cm on theleft and 1.5 cm on the right. Stenella plagiodonwas the only other delphinid in which the leftanterior fold was larger than the right.

MUSCULATURE.—The general impression obtainedfrom a dorsal view of the nasal musculature ofG. melaena is that it has been anteroposteriorly

NUMBER 207 25

compressed (Figure 17). There is a well-developedpe, which originates from the posterior third of thesupraorbital process and inserts across the midlinewithout attaching to the vertex. The pars inter-medius is larger than in T. trurcatus and the otherdelphinids, apparently having incorporated moreof the underlying fibers of ae into itself. Both peand i are heavily invested with fat and connectivetissue. Ai and pi are closely related posteromedially,where they both originate in the fossa lateral to

the vertex. The deep posteromedial fibers of aegrade into pi with no perceptible break. Therewere several well-differentiated muscle fasciculi inthis zone of intergradation, giving the appearanceof a series of separate muscles interposed betweenthe fibers of ae and pi (Figure 17). The tendon ofinsertion of pi is attached to the connective tissueabove the posterior end of the nasal septum.

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

ans

ans

FIGURE 16.—Globicephala melaena, nasal diverticula: a, dorsal view of nasofrontal sacs andassociated structures; b, dorsal view of the angle of the right nasofrontal sac, medial portion ofthe dorsal wall of the sac reflected to show the internal trabeculae; c, dorsal view of theposterior portion of the left nasofrontal sac, dorsal wall removed to show the internal parti-tioning of this portion of the sac; d, posterodorsal view of the right nasofrontal sac and asso-ciated diverticula. (ans = angle of nasofrontal sac, as = accessory sac, bhl = blowhole ligament,dmm = diagonal membrane muscle, fb = yellow fat body, im = intrinsic muscle of nasofrontalsac, iv = inferior vestibule, us = nasofrontal sac, sc = spiracular cavity, v = vertex.)


membrane. The intrinsic musculature of the naso-frontal sacs is also well developed but, aside fromentering the trabeculae of the angle of the rightsac, offers nothing apart from the usual delphinidcondition.

The rostral muscles in G. melaena are sharplydifferentiated into lateral and medial portions.They are not unusually large, particularly in rela-tion to the size of the melon, and are not as largerelative to the size of the rostrum as in Grampus.

OTHER STRUCTURES.—The melon in G. melaenais larger than that of any other delphinid exam-ined. It extends dorsally to a level above the vertex,and anteriorly about three quarters of the lengthof the rostrum (Figures 18, 24). External to themelon is a layer of fatty tissue containing numerouslarge connective tissue bundles, similar to the con-dition seen in Pseudorca crassidens. Some of theseappear to be derived from the rostral muscle, othersfrom the dermis. There is an area of extremelydense connective tissue in the dermis just anteriorto the blowhole, as noticed in Lagenorhynchusalbirostris.

The melon does not pervade the nasal plugmuscle 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 asymmet-rical invasion of the melon usually seen on theright side. Cephalorhynchus is the only otherdelphinid in which this is known to be the case.

As is generally known, there is sexual dimor-phism in the shape of the head in Globicephala(Figure 19), with the mass of forehead tissue inadult males being larger and projecting fartheranterodorsally than in females. As I was only ableto examine an adult male, I was unable to deter-mine whether or not this was reflected in theinternal structure of this area. I would expect that,as was the case in Pseudorca, this dimorphism islimited to an expansion of the fatty connectivetissue of the dermis and does not involve the melon.So far as I have been able to determine, Pseudorcaand Globicephala are the only delphinids showingsexual dimorphism in the facial region.

STENINAE

Steno

MATERIALS.—A young male Steno bredanensiswas dissected. Additional information on this spe-cies is available from Purves (1967).

scP'

FIGURE 17.—Globicephala melaena, dissections of nasal musculature: «, superficial musculature,oblique postcrodorsal view; b, deep dissection, fasciculi of pi on its posteromedial surfacedorsal view. (ae = pars anteroexternus, fb = fat body, i = p a r s intermedius, pe = pars postero-externus, pi = pars posterointernus, sc = spiracular cavity, v = vertex.)

NUMBER 207 27

a

NASAL PASSAGE AND DIVERTICULA.—There was asmall sacculation on the anterior end of the rightpremaxillary sac in the specimen when I dissected,but none on the left. This was not mentioned inPurves' (1967) account, and I suspect that it was adevelopmental anomoly. Otherwise the premaxil-lary sacs present no unusual features.

The accessory sacs were similar to those of mostof the other delphinids, the right being about 2.4cm long by 1 cm wide, while the left was onlyabout half that size. In both the text and his

a

m

FIGURE 18.—Globicephala melaena, sections of rostral struc-tures: a, oblique view of transverse section 20 cm posteriorto 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 mus-cle, rm = rostral muscle).

FIGURE 19.—Globicephala melaena, lateral views of the ex-ternal appearance of the heads, showing the degree of sexualdimorphism in external head shape: a, female; b, male.


figures, Purves (1967) indicated that the accessorysacs formed a communication between the pre-maxillary and nasofrontal sacs. There has beenconsistent confusion in the literature over the rela-tionship of these diverticula, and this mistakeapparently derives from a misunderstanding of thedescriptions of Lawrence and Schevill (1956).

The nasofrontal sacs are similar to those ofTursiops, although the angles of both sacs weremore lobulated in Steno, reminiscent of the condi-tion seen in Globicephala melaena, though notnearly as well developed as in that species. Thelobulations of the nasofrontal sac were slightlytrabeculate when opened, and a few muscle fiberswere seen in the larger trabeculae.

The vestibular sacs were subequal, the rightbeing slightly larger than the left, and were some-what smaller than in most delphinids. There wereno indications of anterior lobes on either of thevestibular sacs.

MUSCULATURE.—The nasal musculature of S.bredanensis is quite similar to that of Tursiops,with only a few minor differences seen in the singlespecimen examined. Pe was very thin and difficultto define, and there was no trace of i. Both ofthese, however, are variable in other delphinids.The rest of the nasal musculature presented nodifferences from the condition seen in Tursiops.Purves (1967) illustrated the nasal musculature,but did not describe it in any detail. However, hisillustrations are in agreement with my dissections.

OTHER STRUCTURES.—The melon was similar indevelopment to that of Tursiops, and, as in mostof the delphinids, entered asymmterically into theright nasal plug. Purves (1967) described an intrin-sic muscle of the premaxillary sac, which I wasunable to separate from the nasal plug muscle.The diagonal membrane was similar to that ofother delphinids, with a moderately developeddiagonal membrane muscle which did not appearto enter the free portion of the membrane. Thedeep structures associated with the blowhole liga-ment were similar to those of Tursiops.

Sotalia

Schenkkan (1972, figs. 1, 2) illustrated the nasaldiverticula in Sotalia guianensis, and later (Schenk-kan, 1973) gave a brief decription of the facialanatomy of this species. The following discussion

is based primarily upon his illustrations in theearlier paper.

NASAL PASSAGE AND DIVERTICULA.TIIC degree ofasymmetry seen in the premaxillary sacs as shownin Schenkkan's (1972) figure is comparable to thatof Grampus, and is greater than that seen in otherdelphinids. The accessory sacs are moderatelydeveloped and situated similar to those of otherdelphinids, as are the nasofrontal sacs. The vestibu-lar sacs, as shown in the earlier paper, are remark-ably large, particularly the right sac, which appearsto be between two and three times as large as theleft. However, in a later paper (Schenkkan, 1973)they are shown as much smaller and nearlysymmetrical.

Schenkkan's (1972, fig. 2) mesial view of the nasaldiverticula of the right side shows a peculiarity notseen in any other odontocete. This illustrationclearly shows a passage originating from the pos-terolateral edge of the premaxillary sac, just an-terior to the accessory sac, and running dorsally toconnect with the medial side of the vestibular sac.Unfortunately the text of this paper contains noreference to the nasal diverticula of this species, noinformation on this structure is given in the label-ing of the figure, and the brief description in hislater paper (Schenkkan, 1973) contains no informa-tion on this structure, so one is at a loss to inter-pret its significance.

MUSCULATURE.—Schenkkan's (1973) comment thatthe nasal musculature in Sotalia guianensis "wascomparable with the situation found in Delphinusdelphis" does not provide a basis for comparison,but gives no reason to believe that it is any differ-ent from the situation seen in Steno.

OTHER STRUCTURES.—No data are available forother features of the facial anatomy of Sotalia.

CEPHALORHYNCHINAE

Cephalorhynchus

MATERIALS.—A young male (110 cm) Cephalo-rhynchus hectori was dissected. Schenkkan (1973)described a dissection of another male (118 cm) ofthe same species.

NASAL PASSAGE AND DIVERTICULA.—The premax-illary sacs were relatively short as compared toTursiops. The dorsomedial wall of the left pre-maxillary sac was produced into a saccular fold,

NUMBER 207 29

which may have been an individual abnormality,as Schenkkan (1973) noted nothing unusual in thisarea on his specimen.

The diagonal membranes were small and aboutthe same size on both sides. The accessory sacs, asnoted by Schenkkan (1973), were relatively large,with the right sac approximately twice the size ofthe left (2.6 cm long as opposed to 1.4 cm on theleft). There was a small posterior branch of theblowhole ligament passing dorsal to the accessorysacs on both sides.

The anterior portions of the nasofrontal sacswere well developed and were unique among del-phinids in that the left sac was much larger thanthe right. Approximately half of the anterior por-tion of the left nasofrontal sac extended across themidline, where it was partly overlain by the right.In their relaxed condition in this frozen specimen,the left sac appeared to occupy about twice thearea of the right. The angles of both sacs werefaintly sacculated, reminiscent of the situationseen in many other delphinids and found in Globi-cephala melaena to an extreme degree. Schenkkan(1973) also noted the reverse asymmetry of theanterior portions of the nasofrontal sacs.

The vestibular sacs were superficially symmetri-cal and not unusual in size. They lay posterior tothe blowhole, similar to the condition seen inOrcinus. There walls were heavily wrinkled, indi-cating considerable distensibility, as in other del-phinids. There was a pronounced anterior lobeof the vestibular sac on the left and a somewhatsmaller one on the right. The left anterior lobeentered the main portion of the vestibular sacsthrough a slit just dorsal to the anterior fold,while the right appeared to be an extension of theanterior fold itself. A small, shallow fold justdorsal to the right anterior fold may be the actualhomologue of the left anterior lobe of the vestibu-lar sac. Schenkkan (1973) did not note these lobesof the vestibular sacs in his specimen. A similar,though much less pronounced, situation was seenin Tursiops and some of the Stenella, where therewas a slight development of an anterior lobe onthe left.

MUSCULATURE.—In general the musculature wassimilar to that of other delphinids. There was awell-developed pe, but no indication of i on eitherside. The portion of ae overlying the vestibularsacs was thinner than in Tursiops or Stenella, but

was otherwise similar. The intrinsic musculatureof the nasofrontal sacs gave more appearance ofbeing continuous with the nasal plug muscle thanit did in Tursiops or Stenella.

The diagonal membrane muscle was difficult todefine, but appeared to enter the membrane to aslight extent. The lateral and medial rostral mus-cles differed in fiber orientation more than inTursiops or Stenella.

OTHER STRUCTURES.—The melon was of moderatesize, and was unusual in not extending into theright nasal plug as in most delphinids. The nasalplugs were remarkably asymmetrical, the laterallip 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) con-sisting of a tough, unstructurated gelatinous sub-stance" between the medial terminations of thecaudal portions of the nasofrontal sacs. I found notrace of such a structure and suppose that this wasan individual abnormality, possibly a parasiticcyst, such as the cestode cysts sometimes encount-ered in small odontocetes.

LISSODELPHINAE

Lissodelphis

Schenkkan (1973) provided a description of thefacial anatomy of Lissodelphis borealis, upon whichthe following discussion is based.

NASAL PASSAGE AND DIVERTICULA.—The premax-illary sacs were relatively small, but presented nonotable peculiarities. The accessory sacs were welldeveloped and the right sac had a posteriorlydirected extension. The nasofrontal sacs were illus-trated as being substantially larger than in Tur-siops, and the angles of the nasofrontal sacs weresacculated, though it is not clear to what extent.The vestibular sacs appear to be relatively largerthan in any of the other delphinids, and are sit-uated posterior to the blowhole. Schenkkan's (1974)observation that the nasal passages were displacedcaudally as a result of extensive development ofthe melon is difficult to visualize, and is not sup-ported by his illustrations.

MUSCULATURE.—Schenkkan (1973) commentedthat "Due to the caudad displacement of the nasalpassage, the direction of all muscle fibers was


nearly vertical and separation into various layerswas therefore fairly difficult." If this is in fact thecase, it seems very different from the otherdelphinids.

OTHER STRUCTURES.—Schenkkan (1973) statedthat the melon was relatively large in L. borealis,though this is difficult to imagine when consideringthe external shape of the head.

PHOCOENIDAE

Phocoena, Phocoenoides, Neophocaena

The members of the family Phocoenidae presenta number of consistent differences from the Del-phinidae, and appear to constitute a very distinctgroup on the basis of facial anatomy. The nasalapparatus of Phocoena phocoena has been describedmore 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 inNeophocaena, and Ridgway (1966) described thevestibular sacs in Phocoenoides dalli. Yet it stillremains to be described in detail as a functionalsystem. I do not intend to do so at this point, butrather to present a brief description for compari-son with the delphinid nasal system. This is basedupon the extensive literature listed above and uponmy own limited dissections of Phocoena andPhocoenoides.

MATERIALS.—One adult of Phocoena phocoenaand one of Phocoenoides dalli were dissected.

NASAL PASSAGE AND DIVERTICULA.—The premax-illary sac is relatively small in the phocoenids, asindicated both by my dissections and the literatureaccounts. The prenasal area of the skull differsmarkedly from that of the delphinids, in the pres-ence of a strong premaxillary emminence, uponwhich the premaxillary sac lies.

Schenkkan (1971) found that the accessory sacwas small or lacking in the specimens of Phocoenaphocoena which he examined. This sac had notbeen reported in the earlier literature, and I wasable to find only a very small one on the right sidein Phocoenoides dalli.

The deep portions of the phocoenid nasal appa-ratus are more complicated than those of thedelphinids, and warrant much more study.

The nasofrontal sacs are large in the phocoenids

(Gruhl, 1911; Gallardo, 1913; Howell, 1927; Schenk-kan, 1973) and are situated as in the delphinids. Ifound the anterior portion of the nasofrontal sacin Phocoenoides dalli to be lined with a thick,nonpigmented, trabeculate epithelium. This had aglandular appearance, but has not been examinedhistologically. The illustrations of Gruhl (1911)and Moris (1969) suggest that this condition is alsopresent in Phocoena phocoena.

The posterior portion of the deep nasal appara-tus is complicated by a diverticulum which arisesfrom the inferior vestibule and passes dorsally,posterior to the nasofrontal sac. This is the "hinterehohle" of Gruhl (1911), the "sac nasal posterieur"of Moris (1969), and the "hinter unter hohle" ofvon Baer (1826). Schenkkan (1973) refers to thisdiverticulum as part of the nasofrontal sac, butdoes not describe it in detail.

The most striking feature of the phocoenid nasalapparatus is the large vestibular sac, which hasbeen thoroughly described in the literature citedabove. This diverticulum is on the order of twicethe size of those seen in the delphinids. The ven-tral wall is thrown into a series of folds, 0.5 to 1.0cm wide, aligned perpendicular to the long axis ofthe body. The walls of these folds are composedof a thick layer of connective tissue, fixing them inplace and precluding distension of the ventral wall.The middle fold of this series is the deepest, clearlydividing the ventral wall into two halves. Thisfold also appears to form the principal communi-cation with the nasal passage. The vestibular sacis completely enclosed by an intrinsic muscle, andis free to move within the layers of the pars antero-externus. This situation appears to be common toall three of the phocoenid genera, and is notaproached by any other cetacean.

MUSCULATURE.—The nasal musculature of pho-coenids is somewhat different from that ofdelphinids when examined in detail, yet is stillarranged according to the same general plan. Thepars posteroexternus appeared to be absent in mydissections. Gruhl's (1911) account of this muscu-lature indicated a similar condition in Phocoenaphocoena. The pars anteroexternus is arranged inessentially the same manner as in the delphinids.Within this layer, however, a very distinct differ-ence is seen in the structure of the vestibular sac,as described above. The fibers of the musculatureof the vestibular sac are oriented perpendicular to

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those of ae. The muscle of the vestibular sac isattached to the maxilla anteriorly, above the sur-face of the vestibular sac, becoming tendinous onthe ventromedial portion of the sac. I have beenunable to confirm this in Gruhl's (1911) account,but the illustrations of Gallardo (1913) suggestthat this holds for Phocoena dioptrica. Howell'saccount of Neophocaena (1927) indicates a similarcondition in that genus.

Beneath the level of the vestibular sac, the mus-cular arrangement is similar to the delphinids. Thegeneral impression, however, is that the deepermuscles are relatively smaller in the phocoenids.Unfortunately, I was unable to determine thearrangement of the deep musculature around thevertex (intrinsic muscle, diagonal membrane mus-cle) in my dissections, and there is no informationavailable from the literature.

MONODONTIDAE

Monodon

Huber (1934) described the facial structures ina large fetal narwhal (Monodon monoceros) insufficient detail to allow comparison with thedelphinids.

NASAL PASSAGE AND DIVERTICULA.—It is in thenasal passage itself (rather, the spiracular cavity)that Monodon appears to be most specialized.Instead of the slitlike passageway seen in delphi-nids and phocoenids, Monodon has a large, spheri-cal cavity. The blowhole opens directly into thiscavity on its dorsal surface, and the nasal plugsopen from its ventral surface.

Unfortunately, Huber's description was pub-lished posthumously, and Howell, who edited it,expressed some doubt as to the exact relationshipof the apertures of the diverticula to the spiracularcavity. It appears that the vestibular sac ("lateralsac") opens laterally from this cavity. Huber's fig-ures indicate a complicated nasofrontal sac, open-ing both into the inferior vestibule and into thespiracular cavity dorsal to the nasal plugs. He alsoindicates that the anterior portion of the naso-frontal sac opens into the spiracular cavity, justventral to the opening of the vestibular sac. Schenk-kan (1973) found similarities between Huber'sdescriptions of Monodon and his own dissectionsof Phocoena. The degree of complexity of the

nasofrontal sac is similar, but more definite com-parisons require clarification of some of theuncertainties in Huber's description. There is noindication of an accessory sac.

Scoresby (1823), in his brief description of thenasal passages of the narwhal, illustrated thevestibular sacs, but did not menton any otherdiverticula.

MUSCULATURE.—Huber (1934) concluded, basedupon a comparison with Tursiops, that the nasalmusculature of Monodon was derived from thesame general plan as that of the delphinids, butdiffered in detail. The differences appear to belargely due to the extreme modification of thestructures with which the musculature is associated.Although Huber did not attempt to define sepa-rate layers of the nasal musculature, examinationof his illustrations suggest that the same layers asin Tursiops can probably be recognized.

The most superficial of these layers of muscula-ture appears to correspond to the pars postero-externus, but has its origin much more postero-medially than in the delphinids. The configurationof the remaining nasal musculature is more similarto that of the delphinids, at least in terms of originand general area of insertion. None of Huber'sillustrations show the details of insertion of pi orai, both of which must differ from the delphinidcondition as a result of the modifications in thespiracular cavity of Monodon.

Huber's (1934) illustrations give the impressionthat the nasal plug muscle ("retractor muscle") iscontinuous with musculature originating from themaxilla to the spiracular cavity (at?). The nasalplugs seem to have a lateral lip, as in delphinids.

OTHER STRUCTURES.—Due to the expansion of thespiracular cavity and the unusual condition of thenasal plug muscle, the relationship of the melonto the nasal plugs must be very different from whatis seen in the delphinids. The melon, as indicatedby the illustration of Raven and Gregory (1933),is quite large. All told, Monodon is a very unusualanimal, and certainly warrants detailed investiga-tion.

Delphinapterus

The nasal apparatus of Delphinapterus leucaswas briefly described by Watson and Young (1879).Their specimen, unfortunately, was in an advanced


state of decomposition, and the description sufferedaccordingly. A more detailed description has beengiven by Kleinenberg, et al. (1969) in their mono-graph on this species.

NASAL PASSAGE AND DIVERTICULA.—Watson andYoung (1879) were only able to find one pair ofnasal diverticula, the premaxillary sacs, which wererelatively small. They were familiar with the workof Murie (1870, 1871, 1873) and appear to havespent some time trying to locate all of the delphiniddiverticula. The illustration given of the spiracularcavity gives the impression that it is large, as inMonodon, but no mention of this was made in thetext. The muscles were unsuitable for dissection.One interesting finding was the presence of nu-merous openings in the walls of the spiracularcavity, which they took to be glandular orifices.Unfortunately, the condition of their specimenrenders this suspect.

Kleinenberg, et al. (1969) described the systemof nasal diverticula in D. leucas in more detail.The vestibular sacs, premaxillary sacs, and naso-frontal sacs are similar to those of delphinids. Inaddition to these, there is a posterior extension ofthe inferior vestibule, along the posterodorsalaspect of the nasofrontal sacs, reminiscent of thecondition seen in Phocoena. These diverticulawere termed the accessory cavities of the nasofrontalsacs by Kleinenberg, et al. (1969). No accessory sacsproper were found. In most respects, their descrip-tion indicates a greater similarity to the delphinidcondition than is seen in Monodon. In their figure51, however, which illustrates the possible actionof the diverticula during ventilation, they show alarge spiracular cavity immediately dorsal to thenasal plugs. This would correspond to the expan-sion of the spiracular cavity described in Monodon.The other figures of Kleinenberg, et al. do not,however, support this idea. No mention is made ofany glandular structures similar to those describedby Watson and Young (1870), nor are the diver-ticula described as being asymmetrical.

MUSCULATURE.—No data is available on the mus-culature of D. leucas.

OTHER STRUCTURES.—The melon in D. leucas

appears to be quite large, judging from the exter-nal appearance of the head, but no descriptions ofits structure are available.

PLATANISTIDAE

Platanista

The anatomy of the nasal complex in this inter-esting cetacean was briefly described by Anderson(1878), and has been more recently covered indetail by Purves and Pilleri (1973). The blowholeof Platanista is unusual in being a longitudinal slitinstead of the transverse crescent seen in the del-phinids. The mechanics of such a structure arevery different from those of the delphinid nose, andthe anatomy differs accordingly. There are novestibular sacs, a condition otherwise seen only inHyperoodon (Schenkkan, 1973; Purves and Pilleri,1973) (excluding the Physeteridae in which struc-tural homologies are unclear). The "maxillary"sacs described by Anderson (1878) are not homolo-gous to the maxillary sacs ( = vestibular sacs) ofMurie (1870), but to one of the deeper diverticula.The nasofrontal sacs in Platanista are grossly sim-ilar in form to those of delphinids, but differmarkedly in that the distal portion (comparableto the anterior portion of delphinids) extends dor-sally rather than anteriorly. Purves and Piller(1973) described an additional diverticulum orig-inating from the area of the inferior vestibule(which appears to be reduced in Platanista) andlying posterodorsal to the nasofrontal sacs. Theytreated it as a branch of the nasofrontal sac anddid not assign it a separate name. Although therelationship is far from clear, this condition seemscomparable to that seen in Phocoena, where therealso was a diverticulum lying posterodorsal to thenasofrontal sacs. The accessory sacs are absent andthe premaxillary sacs are relatively small.

The most striking features of the facial region inPlatanista are the extensive maxillary crests. Purvesand Pilleri (1973) described these in detail anddemonstrated that they contain an extensive systemof air cavities derived from the pterygoid air sinussystem. In this respect Platanista is remarkablydifferent from any other cetacean.

The nasal musculature is quite different fromthat of the delphinids, as necessitated by theextreme modification of the other facial structures,making comparison with that group difficult andbeyond the scope of this paper.

Purves and Pilleri (1973) described the topo-graphic homologue of the melon as a dense mass

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of fibrous tissue. This seems quite different fromthe condition seen in other odontocetes. However,they ascribe a similar condition to Inia and Ponto-poria, both of which I have examined and foundto have considerable fatty differentiation in thisarea. I suspect the differences are partly due totheir using formalin fixed material, in which theconnective tissue becomes more conspicuous, partlyto actual difference in relative amount of fat andconnective tissue, and partly to semantic differencesin usage of descriptive terms.

The nasal plugs lack a lateral lip, as seems to bethe general situation in the platanistids. An itemof some interest is Anderson's (1878) mention of aglandular recess around the ventral portion of thenasofrontal sac. I have seen such a structure inInia, which may well be homologous to the glandu-lar structures described by Evans and Maderson(1973) in Tursiops.

Lipotes

The anatomy of the nasal region in the Chineseriver dolphin, Lipotes velixifer, has been verybriefly commented upon by Hinton and Pycraft(1922) and Hinton (1936). The blowhole is peculiarin being a longitudinal rectangular opening. In thelateral margins of the blowhole are two small bones,one on either side. Various slips of musculature areattached to these, and Hinton and Pycraft (1922)felt that the bones were instrumental in effectingblowhole closure. Hinton (1936) mentions thatthey also occur in Pontoporia, the La Plata riverdolphin, though Schenkkan (1972) does not men-tion them in his description of this species, and Idid not find them in the fetus which I dissected.Hinton and Pycraft (1922) described two pairs ofsuperficial diverticula, an anterior one dorsal tothe bones, and a posterior one ventral to them.The posterior one is of considerable extent on theright side, covering the whole of the "dilatornaris," while that of the left side is concealedbeneath the small bone. Both of these diverticulaare at the level of the vestibular sac, and one ofthem (probably the posterior) is homologous to it.Hinton (1936) said that the same configuration ofdiverticula was found in Pontoporia, but that thedegree of asymmetry was less. None of the otherfacial structures were described in the above works.

Pontoporia

Burmeister (1867) briefly described parts of thenasal system in Pontoporia blainvillei, while morerecently, Schenkkan (1972) described the nasalcomplex in some detail. The discussion of thisspecies is primarily based on the latter work. Inaddition, I have made a preliminary dissection ofa near-term fetus of this species, confirming muchof Schenkkan's description.

As opposed to the two preceding genera, theblowhole is a crescentic slit, as in delphinids. Thedeeper nasal diverticula in this species, as appar-ently in all of the platanistids, are relatively small.The premaxillary sacs are comparable to those ofdelphinids, differing primarily in size, while theaccessory sacs are absent. A small caudal portionof the nasofrontal sac is present, but the anteriorportion is missing. The vestibular sacs, in strikingcontrast to the other diverticula, are extremelylarge and complex, covering much of the dorsaland lateral surface of the facial region. As in mostof the delphinids, the right vestibular sac was largerthan the left, though to a much greater degree.

The nasal musculature appears to be more com-parable to delphinids than that of Platanista, butdetailed comparisons remain to be made. Themelon is moderately developed and situated similarto that of delphinids. Schenkkan (1973) indicatedthat the nasal plugs were relatively simple, withoutlateral lips.

Inia

I have made some preliminary dissections of thefacial region of Inia geoffrensis, which are of usein comparing it to the other river dolphins. Theblowhole is of the type normally seen in delphinids,crescentic with the concavity facing anteriorly.There were no bony elements in the margins ofthe blowhole, nor did I find two pairs of superficialdiverticula. The vestibular sac is extremely large,much more so on the right, and covers the wholeof the posterolateral portion of the nasal muscula-ture. The nasofrontal sacs are moderately devel-oped and, as in Platanista, are associated with aglandular structure, the exact nature of which hasyet to be determined. The anterior portions of thenasofrontal sacs are lacking, the posterior portionextending to a point just lateral to the nasal pass-


age. The accessory sacs are well developed, andsituated as in delphinids. I have not attempted towork out the pattern of the musculature in Inia,which appears to be very different from that of thedelphinids. The melon is well developed, thoughit appears to contain a greater amount of connec-tive tissue than any of the delphinids examined.

Summary of Descriptive Anatomy

NASAL PASSAGE AND DIVERTICULA

DELPHINIDAE.—This is the most variable portionof the delphinid nasal complex. Of the delphinines,the group comprised of the genera Tursiops, Sten-ella, and Delphinus appears to represent the mostgeneralized condition and the included forms showfew differences among themselves.

Lagenorhynchus albirostris differs from this groupof genera in the extreme expansion of the naso-frontal sacs and the development of a lateral diver-ticulum from the right premaxillary sacs. Lageno-delphis is similar to Lagenorhynchus albirostris inhaving a lateral diverticulum from the premaxil-lary sac, but does not show any expansion of thenasofrontal sacs.

Grampus is also distinctive in the morphologyof its nasofrontal sacs. The anterior portion isabsent on the left side and is greatly enlarged onthe right.

Of the orcinines, only Globicephala shows anynotable modifications of the diverticula. Again, itis the nasofrontal sac which is specialized, havingan unusual trabeculate sacculation on the angle ofthe right sac.

The Steninae and the Lissodelphinae show nooutstanding modifications of the nasal diverticula,while the only member of the Cephalorhynchinaeexamined, Cephalorhynchus hectori, shows a strik-ing enlargement of the anterior portions of thenasofrontal sacs, and is further unusual in that theleft sac is larger than the right.

The vestibular, accessory, and premaxillary sacsare relatively conservative in the delphinids, thenasofrontal sac being the most variable portion ofthe system.

OTHER FAMILIES.—The nasal diverticula are ex-tremely variable in the other odontocete families.The vestibular sacs in the phocoenids have rigid,

heavily folded ventral walls. In some of the plata-nistids these sacs are extremely large, covering mostof the posterior facial region. They appear to berelatively small in the monodontids.

The nasofrontal sacs of the phocoenids are morecomplicated than those of the delphinids, and pos-sess a trabeculate anterior portion. The posteriorportion is also more complicated, with an addi-tional diverticulum arising from the inferior vesti-bule and lying posterior to the nasofrontal sac. Inthe monodontids, the nasofrontal sacs are rela-tively complex, and are in some ways reminiscentof those of the phocoenids. These diverticula arerelatively small in the platanistids, most of whomappear to lack an anterior portion. They are some-what more complicated in Platanista, which has adiverticulum lying posterodorsal to the nasofrontalsacs, somewhat similar to the condition seen inphocoenids.

MUSCULATURE

DELPHINIDAE.—Within the delphinids the nasalmusculature is relatively conservative. Pe and i arethe most variable elements, the former being par-ticularly so in the Orcininae. The deeper portionsof the musculature are more constant.

OTHER FAMILIES.—Outside of the Delphinidae,this portion of the anatomy shows considerablevariation. The phocoenids are probably closest tothe delphinid pattern, differing mainly in thearrangement of the superficial portions of the mus-culature. The reverse seems to be true in Monodon,where the deep musculature is most divergent fromthe delphinid pattern. None of the other odonto-cetes have been examined in sufficient detail todraw comparisons.

MELON

DELPHINIDAE.—In most of the delphinines, themelon is relatively small. In Grampus, however, itbecomes quite large, but without the proliferationof dermal connective tissue seen in some otherdelphinids.

In the orcinines this structure is more variable.In Orcinus and Pseudorca it is relatively small. Inthe latter, however, the dermal connective tissue

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superficial to the melon has become thick, giving abulbous appearance to the forehead, particularlyin the male. In Globicephala both the melon andthe connective tissue have hypertrophied, again,more so in the male than in the female. Thebulbous-headed genera Grampus, Pseudorca, andGlobicephala are compared in more detail in alater section.

OTHER FAMILIES.—In the phocoenids the melonis relatively small, with the possible exception ofNeophocaena, which has a bulbous forehead. Inthe monodontids the melon is relatively large,apparently without a thickening of the dermal

connective tissue. The melon in the platanistids isrelatively small.

OTHER STRUCTURES

The rest of the nasal complex shows little varia-tion in the delphinidae. The platanistids stand outas an unusual group in many ways, one of themore important of which may be the lack of lat-eral lips on the nasal plugs in this group. Glandu-lar structures are apparently present in all of thefamilies, but are not well enough known to permitgeneral comparisons.

FUNCTION OF THE FACIAL COMPLEX

Introduction

The facial complex is potentially involved in avariety of functions. This complex has differentiatedaround the external nasal passages, and most ofits possible functions involve movement of air inthese passages. The functions can be broken downinto two general categories, those associated withrespiration and those associated with sound pro-duction. Respiratory functions are of undoubtedimportance, but do not account for the degree ofmorphologic specialization seen in this area, sug-gesting that sound production may be of consider-able importance in this region. In this contextsound production is meant to include not only thegeneration of acoustic energy, but also modificationof that energy, such as modulation, reflection, andrefraction.

In this chapter the possible roles of the facialstructures in respiration are considered first. Thefacial structures are discussed in the same order asin the descriptive section, and the possible func-tion of each element is considered separately. Fol-lowing this, the questions of sound production areconsidered in detail, with a review of the literaturepertinent to this problem. In the next section ofthis chapter, the functional significance of cranialasymmetry is gone into in a similar manner. Fi-nally, a summary section is given, presenting themost likely of the functions in which this region isinvolved.

Respiratory Considerations

One of the general functions proposed for theelaborate nasal apparatus of odontocetes has beenthe exclusion of water. While this is of undoubtedimportance to a diving animal, I believe that ithas been overemphasized with respect to odonto-cetes. It has been commonly thought that thedeeper an animal dives, the greater will be thetendency for water to enter the nares or for air tobe lost. This would only be the case if a pressuredifferential existed at the point of closure of thenasal system. In general, it can be assumed thatthe air within the respiratory system of a divinganimal will be compressed by collapse of the lungs,thus equalizing the internal and external pressuresupon the system. A problem exists only if the airavailable in the collapsible portions of the respira-tory system is not sufficient to raise the pressurewithin the noncollapsible portions of the system toa level equal to that of the external pressure. Ithas been suggested that this is compensated for incetaceans by expansion of vascular tissues into therigid air spaces (e.g., the middle ear), thus reducingtheir volume and equalizing the pressure. In anyevent, this is only a problem in structures deep tothe fleshy nasal passages, as this sort of pressuredifferential would tend to force the nasal plugsmore firmly into the bony nares, effectively tight-ening the seal. Pinnipeds, with relatively simplenasal passages, have been reported to dive to depths

SMITHSONIAN CONTR1BU I IONS TO ZOOLOGY

of 600 meters (Kooyman and Anderson, 1969), sub-stantiating the idea that deep-diving does notdemand an extremely specialized nasal apparatus.

A different sort of question involving the entryof water into the nasal passages has also beenraised. This is the possibility of water entering thepassages during breathing. Cuvier (1797) thoughtthat the diverticula in the delphinid nose served astraps to prevent inspiration of water. Lawrenceand Schevill (1956) noted that water frequentlyentered the vestibular sac if the animal started tosubmerge with the blowhole partially open. Thisappeared to present no problems to the animal, andthe water was expelled in the next breathing cycle.They also noted that one of their experimentalsubjects experienced no difficulty if the blowholewas manually forced open underwater. Conse-quently they suggested that the vestibular sacsfunction as a water trap. This would, however, beeffective only if the nasal plugs were seated andwater penetrated no farther than the spiracularcavity. If, however, the vestibular sacs were absent,water would merely be forced out by closure of thenasal passage. Thus, although the vestibular sacswill hold water, this ability seems to be merely aconsequence of their presence and does not provideany particular advantage to the animal.

Lawrence and Schevill (1956) were of the opin-ion that there is no mechanism for removing wateronce it got into the deeper portion of the respira-tory system. The normal respiratory cycle of theseanimals, however, is sufficiently rapid that everyexpiration is essentially a cough, and should besufficient to clear small amounts of water from thepassages. Tomilin (1967) described a series ofexperiments in which water was introduced intothe respiratory passages of dolphins, sometimes inconsiderable quantity. This seemed to present noproblem to the animals and was expelled in subse-quent expirations.

Schenkkan (1973) suggested that the vestibularsacs were filled with air from the nasofrontal sacsimmediately before surfacing to breathe, and thatthis provides a "pneumatic cushion beneath thesuperficial fascia of the vestibular sections of them. maxillonasalis, facilitating the rapid openingof the blowhole. . . ." It is not clear how this wouldfacilitate opening of the blowhole, nor is it evidentthat it actually occurs. Blockage of the entrance ofwater to the nasal passage by the initial outflow

of air from the vestibular sacs, as suggested bySchenkkan (1973), would seem to be of negligibleimportance when compared to the outflow ofrespiratory air from the lungs. Water may, in fact,enter the vestibular sacs, but it is difficult to seehow the "small particles enclosed in the epitheliallining of the vestibular sacs in some species" relatesto this question. Much of Schenkkan's material wasderived from stranded animals, as was mine, inwhich it is not uncommon to find sand and detritusas far back in the respiratory tract as the terminalbronchioles, either washed in post mortem, or, inthe more extreme cases, inspired when the animalswere thrashing about in the surf.

The observation that "in general a living dolphinseems to be unable to open its blowhole unless thevestibular sacs have been previously expanded" isapparently based upon a misunderstanding of theobservation by Anderson (in Purves, 1967) on adead Phocoena. Schenkkan (1973) interpreted thestatement to mean that "when the air was expressedfrom the (vestibular) sacs of a specimen, it died ina motionless condition as the head and indeed theentire animal sank beneath the surface." The state-ment in Purves (1967) is as follows: "Recently deadanimals have been observed to sink below the sur-face when the vestibular sacs have been punctured."This observation does relate to Purves' (1967) dis-cussion of the vestibular sac as a buoyancy regula-tor, but not to Schekkan's (1973) speculations.

Thus, the complexity of the odontocete nosecannot be accounted for by the obvious demandsof an aquatic existence. Movement of air duringsound production, however, may require particu-larly tight closure of the nasal passages. It may alsobe advantageous to be able to control the passagesat different level, isolating some of the diverticula.The layered structure of the nasal musculaturesupports such an idea.

Nasal Passage and Diverticula

A great variety of suggestions have arisen for thefunctioning of the nasal diverticula. It was firstsuggested (Ray, 1671) that they were part of theolfactory system, later (Sibson, 1848) that they werefilled with air to maintain the head of the animalnear the surface while it was sleeping. The olfac-tory hypothesis has long been abandoned in viewof the lack of olfactory innervation in these ani-

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mals. The idea of buoyancy regulation by thediverticula appears in a number of later papers(e.g., Purves, 1967), but has not been demonstratedexperimentally.

Norris (1964) suggested that the vestibular sacsserve as reflective elements, directing sound emittedfrom the region of the external bony nares ante-riorly. If these sacs are air-filled during vocalization,then they would certainly be effective reflectors ofsound energy. Their situation with respect to thesurrounding muscles allows them to expand pri-marily in a horizontal plane, increasing their reflec-tive surface. As these sacs are capable of distension,the area of reflective surface could be modified, thusaltering the shape of the emitted sound field. Thevariation in morphology of these diverticula sug-gests that there may be considerable variation inthe shape of the sound field between differentspecies.

The anterior folds, as pointed out by Lawrenceand Schevill (1956), provide a tight closure of thenasal passage at the level of the vestibular sacs.

Lawrence and Schevill (1956) proposed that thenasofrontal sacs formed a pneumatic seal aroundthe nasal passage. This certainly appears to be themechanism functioning to produce closure of thenasal passage in a dead animal when air is intro-duced into the nasal system through the larynx,not action of the lateral lips of the nasal plugs asstated by Schenkkan (1973). While this is a pos-sible function for the nasofrontal sacs, it is alsopossible to achieve the same end with the two largemuscle masses, pi and ai, which encircle the pass-age at this level. In Grampus the anterior portionof the left nasofrontal sac is absent, precludingpneumatic closure of that side. In Lagenorhynchusthe nasofrontal sacs have been greatly enlarged,beyond what would seem to be useful for pneu-matic closure. These modifications suggest a role inaddition to or other than closure of the nasalpassage.

At the moment, however, it is difficult to assigna primary function to these sacs. Certainly anycavities connected with the nasal passage can serveas reservoirs for recycling of air during phonation.If they contain air, they are going to be effectivereflectors of sound. The large nasofrontal sacs ofsome species suggest that one of these functionsmight 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 theposterolateral edge of the premaxillary sacs into thenasofrontal sacs. But as Schenkkan (1971) haspointed out, the accessory sacs are blind diverticula,unsuited for the conduction of air between othercavities. He also noted that they are extremelyvariable and suggested an inverse relationshipbetween their size and that of the posterior portionof the nasofrontal sacs. As with any of the diver-ticula, air storage and sound reflection are likelypossibilities. Air can pass into them without passingthrough many other structures, arguing for theirusefulness as reservoirs in laryngeal sound produc-tion. The intrinsic musculature surrounding themwould be able to return the air to the respiratorypassages without involving manipulations of therest of the nasal complex. Their small size, ofcourse, is a point against their being effective inthis role.

Of all of the diverticula, the premaxillary sacsare probably the best situated for storage andrecycling of air for sound production (particularlyfor laryngeal sound production). They are largerthan the other diverticula, and open directly intothe bony nasal passage. Fibers of ai which run fromthe maxilla over the nasal plug mass could easilyprovide the compression necessary to recycle airback into the nasal passage. At the same time thiswould firmly seat the nasal plugs posteriorly andblock the escape of air into the dorsal parts of thenasal tract. Purves (1967) is a strong proponent ofthis view and thinks that the premaxillary sacs arethe primary reservoirs of air during phonation.They are also effectively situated to contribute toreflection of sound anteriorly.

Musculature

The pars posteroexternus (pe) of the nasal mus-culature, as defined in this paper, appears to be acompressor of the underlying structures (Figure20). This is certainly the case where its insertionis upon the vertex, and thus fixed with respect toits origin. Compression would limit vertical expan-sion of the vestibular sacs, and in so doing wouldserve to increase lateral expansion. The same func-tion could be performed by the pars anteroexter-nus, but since it also has a large insertion upon


the nasal passage, its contraction might produceother, possibly undesirable, effects.

The pars intermedius (i) has no immediatelyobvious function. Lying as it does, it could producecompression as well as posterior displacement ofthe structures deep to it. These functions couldalso be performed by the pars anteroexternus (ae)(Figure 20). The functional differentiation betweeni and ae will have to await experimental evidence.

The most posterior of the superficial fibers of thepars anteroexternus (ae), which insert upon theposterior wall of the blowhole, act to draw theposterior lip backward, facilitating opening of theblowhole aperture. The superficial fibers originat-ing just anterior to this, however, run from anorigin posterior to the nasal passage to an insertionanterior to it. These perform the antagonistic func-tion of drawing the anterior lip posteriorly, thusacting to close the blowhole aperture. As theanterior lip is more mobile than the posterior,simultaneous contraction of all the superficial fibersof ae would probably result in maintaining blow-hole closure, drawing the aperture slightly poste-riorly and compressing the underlying structures.The fibers of ae which lie adjacent to the vestibularsacs are loosely attached to them and could pos-

FICIRF. 20.—Diagramatic view of the actions of the layers ofthe nasal musculature. (ae = pars anteroexternus; ae-a = parsanteroexternus, anterior fibers; ae-p = pars anteroexternus,posterior fibers; ai = pars anterointernus; i = pars interme-dius; npm = nasal plug muscle; pe = pars posteroexternus;pi = pars posterinternus).

sibly serve to draw the sacs {posteriorly. The greaterpart of ae passes beneath the vestibular sacs, whereits fibers converge radially upon the walls of thenasal passage. At this level ae is a strong dilator ofthe nasal passage.

The pars posterointernus (pi), inserting via atendinous sling around the posterior wall of thenasal passage, draws the posterior wall anteroven-trally, opposing the action of the posterior fibersof ae (Figure 20). Pi is certainly one of the mainagents of passage closure at this level. In drawingthe posterior wall ventrally it also serves to bringthe blowhole ligament to bear upon the lip of thenasal plug, facilitating closure of the bony nasalaperture.

The pars anterointernus (ai) is the largest andthe most powerful of the nasal muscles. Its princi-pal function is closure of the nasal passages, bothby drawing the anterior wall posteriorly and bycompressing the nasal plug mass, forcing the plugsback over the bony nares (Figure 20). The anteriorportions of ai, which insert upon the nasal passagecould, however, be functional in dilation of thepassage. As suggested by Purves (1967), ai couldalso compress the premaxillary sac and recycle airfrom that sac to other parts of the system. In addi-tion, Purves suggested that ai compresses the acces-sory sac, a function which may be better performedby parts of the intrinsic musculature.

Purves (1967) contended that the separate layersof nasal musculature (ae, pi, etc.) could not oper-ate independently, owing to the disposition of thenerves and blood vessels among them. His observa-tions were based on studies of specimens in whichthe vasculature had been injected with latex orpolyester resin. He found that the innervation andvasculature "which supply the major groups ofmuscles spring each from a separate main trunkand pass from layer to layer within the group,branching only within the 'layer' of the muscle."He concluded that shearing stresses produced byindependent action on the muscle layers couldcause ruptures of the vessels. I found the samedistribution of vessels and nerves in my dissections,and did not consider it remarkable, as it is thenormal pattern for innervation and vascularizationof skeletal musculature. One has only to examinean injected preparation of the human forearm,where the same pattern can be seen in the muscu-lature controlling the fingers, to realize that this

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arrangement can permit considerable independenceof muscle action.

It is difficult to assign a discrete function to theintrinsic musculature of the nasofrontal sac. Itsdisposition along the posterior portion of this diver-ticulum, around the communication of the naso-frontal sac with the inferior vestibule, and aroundthe accessory sac puts it in a position to produce avariety of actions upon these structures. It probablyprovides partial isolation of these diverticula, allow-ing independent emptying and filling of theircavities. It can also provide constriction of thesediverticula, altering their shape and capacity.Purves (1967) suggested that it draws the naso-frontal sacs laterally, assisting in pneumatic closureof the nasal passage. I do not see how this wouldwork and think that it must be a minor functionat best.

As pointed out by Lawrence and Schevill (1956),the nasal plug muscle withdraws the nasal plugsfrom the bony nares. This muscle may also beinvolved in complex movements of the nasal plugsduring phonation.

The rostral musculature is difficult to interpretfunctionally. Lawrence and Schevill's (1956) con-tention that it serves to "keep the melon undertension and makes a strong connection between itand the rostrum" is difficult to accept. This couldlie performed equally well by the connective tissueof the rostrum.

The melon is known to have considerable mo-bility in the beluga (Delphinapterus leucas). Thishas not been demonstrated in any other odonto-cetes, and the relationship of the beluga to thedelphinids is not well understood. It is possible,nevertheless, that the rostral musculature may pro-duce slight changes in the shape of the melon indelphinids.

There is a possibility that the rostral muscula-ture may play a role in sound projection. Recentwork by Norris and Harvey (1974) has demon-strated gradients in sound velocity in the melon,which they feel may be of importance in shapingthe sound field. The rostral musculature, lyingimmediately adjacent to the melon, may beinvolved in this system, and may be capable ofaltering its effect upon the sound field throughchanges in its acoustic properties upon contraction.

The lateral portion of the rostral musculature ispartly 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 inanimals such as Globicephala and Grampus andthe relatively large mass of muscle inserting intothe connective tissue of the lips in these forms, acertain amount of mobility may be present andmay be important in feeding. It is interesting tonote that a greater portion of the rostral muscula-ture was concerned with the lips in Orcinus andPseudorca than in other delphinids. This may bepart of their specialization for feeding on largeprey.

At least one of the functions of the nasal plugs,that of closing the nasal passage at the level of thebony nares, seems relatively clear. These plugs fittightly over the surface of the premaxillae, sealingthe nasal passage at that point. It is possible, assuggested by Lawrence and Schevill (1956), thatair could be forced arovind the plugs from below.This would involve unseating the plugs at somepoint determined by the pattern of compression ofthe muscles dorsal to the plugs, and could allowair to flow into either the premaxillary sacs or theinferior vestibule. From the inferior vestibule airwould be free to enter both the accessory and naso-frontal sacs.

Evans (1973) provided a new suggestion on therole of the nasal plugs in sound production.According to his theory, movement of the plugsagainst the margin of the bony nares would set uprelaxation oscillations, "much the same mechanismthat causes chalk to screech when pushed across ablackboard." This hypothesis was later amplified(Evans and Maderson, 1973), taking more anatom-ical details into consideration.

The lips of the nasal plugs have been implicatedin sound production, a function which will bediscussed in detail later in this paper. They alsoappear to provide a more effective seal over thebony nares by projecting posteriorly beneath theblowhole ligament.

The function of the diagonal membrane is prob-ably more complex than has been suggested.Lawrence and Schevill (1956) thought that it facil-itated closure of the nasal passage by the nasalplugs. Norris (1969) suggested that it may formpart of an air metering system for sound produc-tion. It is also possible that these membranes maybe directly involved in sound production. Now thatit is known that they are under muscular control,


it seems likely that they play a more active rolethan was previously thought.

The blowhole ligament and the fat body asso-ciated with it maintain stability in the complexarea around the inferior vestibule. The blowholeligament prevents the mouths of the accessory andnasofrontal sacs from collapsing, and provides asurface against which the nasal plugs fit in closingthe nasal passage. The fat body maintains the shapeof the posterior fold.

Melon

The melon has constituted one of the most enig-matic portions of the nasal complex. One sugges-tion as to its function was that of Howell (1930),who thought it might be a buffer to reduce theeffect of water pressure on the skull. While therole of water pressure in influencing the shape ofthe cetacean head has been exaggerated, the ideaof the melon as a buffer is fairly plausible. It issuitably constructed for such a purpose, having asoft, almost fluid core contained within a toughsheath of dermal connective tissue. It seems likelythat in some of the bulbous-headed delphinids(particularly Globicephala) the melon actuallyserves this purpose. It seems less likely, however,that this is of primary importance in other, lessspecialized delphinids.

Huber (1934) was of the opinion that the melonserves as a special sensory organ to detect changesin pressure "when the animal accelerates, when itdives to greater depths, or approaches unyieldingobjects. . . ." This seems to have been based on itspresumed rich innervation. I attempted to followthis innervation, and believe that most of it runsto the area around the nasal passages and to theskin. The skin is known to be highly innervated(Palmer and Wenddell, 1964) and could betteraccomplish some of the functions suggested byHuber. The detection of changes in hydrostaticpressure requires a different sort of mechanism.Since animal tissues are relatively incompressible,this function is likely to be performed by sensorsin air-containing structures which are subject tocompression with changes in depth.

Another group of suggestions has been that themelon served as a reservoir for dissolved gases.Howell (1930) suggested that the melon and otherfatty structures might absorb carbon dioxide, but

felt that this was more possible than probable.Kooyman and Andersen (1969) suggested that fattystructures in diving mammals might serve as nitro-gen buffers during serial deep dives. The lack ofvascularity in the melon makes it unlikely that itis involved in any sort of gas exchange.

Raven and Gregory (1933) thought that thelesser density of the melon served to buoy up theanterior end of the animal, making breathingeasier. This has been recently revived by Clarke(1970), with respect to the extreme situation seenin the sperm whale. In the case of the spermwhale, as in the bulbous-headed delphinids, theamount of energy required to push this structurethrough the water is likely to more than make upfor the small advantage conferred in raising thehead to the surface. It must also be borne in mindthat, while a slightly positive buoyancy may be ofsome advantage in rising to the surface to breathe,it is of a corresponding disadvantage in diving.Clarke (1970) has hypothesized that the spermacetiorgan in Physeter is cooled by drawing water intothe nasal passage, thus altering the density of thismass when the animal is ready to dive. Lawrenceand Schevill (1956), however, note that cetaceansseem to be able to rapidly alter their buoyancy,probably through altering lung displacement.Ridgway (1971) further discussed Clarke's hypothe-sis from a physiological standpoint and concludedthat it was unlikely.

Raven (1942) thought that the melon served asa cushion upon which the nasal musculature actedto compress the nasal plugs against the bony nares.While this may occur in the most posterior por-tions of the melon, the greater portion of it liesanterior to the insertion of this musculature.

Recently, with the increased knowledge of echo-location in delphinids, the melon has been exam-ined with respect to possible acoustic roles. Theshape and position of the melon led to the sug-gestion (Lilly, 1961) that it is an acoustic lens, atheory which has received considerable acceptance.The principal objections to this theory have beenthat the melon is not shaped like a lens and thatthere was no evidence that its acoustic propertiesdiffer sufficiently from those of the surroundingtissues to make it effective as an acoustic refractor.

Kleinenberg et al. (1969) subscribed to the ideaof the melon as an acoustic lens, although with nonew evidence along this line. They also suggested

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that the melon may be able to focus sufficient acous-tic power to enable prey to be stunned at a "con-siderable distance." It seems highly unlikely thatthe animals would be capable of generating enoughpower to do this without disrupting their owntissues.

Norris (1968) has suggested that the melonserves as an acoustic waveguide, offering a path ofminimum resistance through the forehead tissues.This, of course, can be countered by the suggestionthat there would be even less acoustic resistance ifthere were no tissue there at all. However, assum-ing that the elevated vertex and the posterior nasalapparatus are important to the animal, removingthe tissue of the melon would result in a concaveforehead, producing more drag than a convex fore-head as the animal moves through the water. Theconclusion from this line of reasoning is that themelon is merely filler to produce a particular exter-nal form. While this may have been important inthe early evolution of the melon, it is probablethat other functions are presently more important.

The work of Bullock et al. (1968), in whichareas of sensitivity to sound were mapped on thehead of a live animal, suggested that the melonmight be involved in acoustic reception. Theyfound two general areas of sensitivity: a ventralone over the posterior end of the lower jaw and adorsal one anterolateral to the blowhole. Norris(1968) suggested that an acoustic waveguide mayextend from the dorsal area through the antorbitalnotch to the lower jaw and thence to the ear. Theantorbital notch is occupied by dense connectivetissue through which the facial nerve runs andseems unlikely as a route for sound conduction.Experimental work by Norris and Harvey (1974)did not demonstrate acoustic transmission in thisarea. The alternative is conduction through thebones of the skull, which is contrary to the presenttheories of cetacean hearing. However, of these twoalternatives, I would tend to support the lattertheory, rather than the idea of an antorbital wave-guide. More work needs to be done to demonstratethe paths of sound reception, and to clarify thepossible role of bone conduction in hearing.

Ackman et al. (1971) noted that the lipids ofthe melon and mandibular fat bodies (which aresuspected of playing a role in sound transmission)were similar and that they differed from the lipidcontent of the blubber. They speculated that these

differences may reflect differing physical propertiesadvantageous for high frequency sound transmission.

Recent experiments by Norris and Harvey (1974),utilizing tissues from freshly dead specimens, havedemonstrated a gradient in sound velocity in themelon tissues. They found that the center of themelon possessed relatively slow transmission veloci-ties, while peripheral areas were somewhat faster(ca. 10%). These differences may be due to varia-tions in lipid composition or lipid content, asdescribed by Litchfield et al. (1973). Unfortunately,it is not possible to make a precise comparisonbetween Norris' sound velocity data and Litch-field's lipid data, as the exact correspondencebetween the sites measured cannot be determined.This would be of great interest, as the greatestvelocity difference (in Norris' section C, about30%) does not appear to correspond to any of thelipid differences described by Litchfield, nor to anyanatomical differences known to me.

Unfortunately, no data is available on the invivo acoustic properties of any of the tissues of thefacial complex. Until this is available, the acousticfunctioning of the structures will remain unclear.

Glandular Structures

Glandular structures have been described in thenasal passages of Delphinapterus leucas (Watsonand Young, 1879), Platanista gangetica Anderson(1878), and Tursiops truncatus (Maderson, 1968).I have found tissue which appeared to be glandularin Phocoenoides dalli and Inia geoffrensis. Theobservation of Watson and Young (1879) may bein error, as their specimen was in an advanced stateof decomposition. Such structures were not men-tioned by Kleinenberg et al. (1969) in their exten-sive monograph on D. leucas.

Glandular tissue in /. geoffrensis and P. gangeticawas located around the nasofrontal and accessorysacs and the inferior vestibule. I could not discernany ducts or openings into the nasal passage, leav-ing the functional relationships of the glandsunclear.

In P. dalli the anatomical situation is muchdifferent. Here the anterior portion of the naso-frontal sac itself is modified into what appears tobe a glandular structure.

Glandular tissues have recently been discoveredin the area of the inferior vestibule in T. truncatus


(Maderson, 1968; Evans and Maderson, 1973). Theyare described as compound acinar, exocrine glands,opening onto the surface via small crescentic pores.The secretion of these glands is not mucinous andis suggested to contain a lipid, possibly for lubrica-tion of adjacent structures.

Functional Basis of Sound Production

REVIEW

Odontocetes have long been known to producesounds and there is a relatively voluminous litera-ture dealing with this subject. With the discoveryof echolocation in odontocetes, there has been atremendous increase of activity relative to cetaceansound production. In the last ten years, by far thebulk of the literature dealing with odontocetes hasbeen concerned with acoustic problems. Unfortu-nately the problems are complex and much remainsto be resolved.

The mechanism of sound production in Cetaceais poorly understood and the literature pertainingto it is full of confusion, errors, and misunder-standing. Norris (1969) lists the following as beingthe only definitely known sources of sound produc-tion in odontocetes: the lips of the blowhole (ex-ternal), movements of the jaws, and slaps of thebody, flippers, or flukes against the water. Noneof these mechanisms accounts for the variety ofcomplex sounds which these animals have beenobserved to produce.

In the following pages I will review first thenature of the sounds and the sound field, then thetheories of the site and mechanism of sound pro-duction. Following this, I will consider these prob-lems in the light of the present study.

The nature of the sounds themselves has receivedthe greatest attention, as this has been the mostaccessible part of the problem. Norris (1969) andEvans (1973) have provided summaries of thedescriptive information on odontocete sounds. Un-fortunately the state of our knowledge is not suchthat detailed comparisons of delphinid sounds canbe made. An extremely wide variety of equipmenthas been used to record these sounds, limiting thefrequencies which could be analyzed in many cases.The relatively recent discovery that the sound fieldis highly structured (Evans and Prescott, 1962;

Norris and Evans, 1967; Schevill and Watkins,1966; Evans, 1973) has made it imperative that theorientation of the animal with respect to the receiv-ing apparatus be precisely known. This has seldombeen the case. Norris (1969) presented evidencethat there may be considerable individual variationin echolocation, further complicating the situation.Caldwell et al. (1965) have demonstrated individ-ual variation in the low frequency components ofdelphinid vocalizations. Thus it is impossible atpresent to make any correlations between anatom-ical differences and differences in sound production.

Odontocetes are known to produce sounds fromwithin the audible range of humans to over 250kHz (Norris and Evans, 1967). Within this fre-quency range there is a variety of sound types. Twogeneral types of sounds are important for consid-eration of sound production mechanisms: (1)whistles or squeals, which are within the audiblerange of man and which seem to be primarilycommunication signals; and (2) clicks, which arebroad-band pulsed sounds extending well abovethe audible range. The latter are usually consid-ered to be primarily important for echolocation.

As noted above, the sound field produced bydelphinids has been shown to be highly directional.The shape of this field has been described for afew animals and had been shown to vary with thefrequency of the emitted sound. Most measure-ments of this field have been made in the horizon-tal plane and indicate an asymmetry in the shapeof the field. In general, the greatest amount ofenergy is radiated directly anterior to the animal,with the field strength dropping laterally and pos-teriorly. This is particularly true of the higherfrequencies. Norris and Evans (1967) presenteddata based upon work with live animals (Steno).Their data indicate that the sound intensity 20degrees to the left of the midline is 1-2 db greaterthan that 20 degrees to the right of the midline(frequency unspecified). Evans et al. (1964) obtainedessentially the same results with an artificial soundsource implanted "in the area of the nasal sacs" inan infant Stenella microps ( = S. longirostris) ca-daver. Their tests ranged from 20 to 60 kHz andindicated that the asymmetry increased with anincrease in frequency. The sound field observed bythese workers was less directional than that meas-ured by Norris and Evans (1967) with live Steno.

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Evans et al. (1964) also measured the sound fieldin the vertical plane (under the same conditions)and found slightly more energy dorsally in the lowrange, changing to ventrally at 60 kHz. Evans(1973) presented further data based upon workwith a live Tursiops truncatus. He noted a doublepulse waveform with maximum energy at 30 kHzand a striking right-left asymmetry in relativestrength of the two pulses. Measurements of theshape of the sound field indicated a rapid loss ofenergy below the horizontal plane of the animal.These measurements were apparently based on the30 kHz pulses, although the frequency or band-width of the measurements is not given.

Evans et al. (1964) conducted tests on dry skullsof Tursiops and found that for the lower portionof the range (20-40 kHz) more energy was radiatedlaterally than anteriorly. At 60 kHz, however, thischanged and the anterior portion of the sound fieldwas about 10 db above the lateral portion. Theirdata also indicated that for the skull alone, theasymmetry becomes less at higher frequencies.

Evans and Prescott (1962) produced sounds byforcing air through the upper respiratory system(including larynx) of a severed head of Stenellagrafjmani (= S. attenuata), as well as by forcing airthrough the excised larynx alone. They stated thatthe 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 onthe right side in both the horizontal and verticalplanes. They also found a substantial ventral ele-ment to the sound field.

The statement that there is no significant ventralportion of the emitted sound field (i.e., that soundis emitted "above the level of the mouth") hasappeared in the literature as an argument againstthe larynx as a sound source (Norris, 1968). Thisis based upon the findings of Norris et al. (1961),who stated that when their experimental animalpresented the ventral surface of the head to thehydrophone, "the volume decreased markedly." Nofrequency specific measurements were made andthe type of sound (whistle or click) was not speci-fied. The text implies that this concerned theaudible sound range only. Since the data of Evanset al. (1964) indicate that the strength of the ven-tral portion of the sound field increases with fre-

quency, the implications of Norris et al. (1964)may not hold for the higher frequencies of theecholocation sounds.

At this point I would like to review the argu-ments concerning the site of sound generation inodontocetes. These are concerned with two areas,the larynx (which is somewhat removed from thearea of my work) and the upper portion of thenasal passage.

At the moment there is no direct evidence relat-ing to the mechanism of sound production, andrelatively little indirect evidence.

The diverticula of the nasal passage have fre-quently been implicated in sound production (Lillyand Miller, 1961; Lilly, 1961, 1962; Evans andPrescott, 1962; Norris, 1964, 1968; Norris andEvans, 1967), a possibility originally suggested byLawrence and Schevill (1956). Lilly and Miller(1961) speculated that the cavities of the nasal tractare "shock excited." I have trouble following theirarguments, but it seems that shock excitation is bymeans of sound (specifically, clicks) produced else-where. This is in accordance with the view ex-pressed by Lilly (1961) that the clicks were producedby the larynx. He does, however, state that thenasal plugs and sacs are used to produce sound, butdoes not produce any evidence for this statement.Lilly's other work (1962) merely contains a refer-ence to his book (1961). Thus, the work of Lilly,which is frequently cited as supportive of nasal sac

xsound production, contains no evidence and, infact, expresses the view that the larynx is the sourceof the "echolocation clicks."

In their work on severed heads of Stenella graff-mani (= S. attenuata), Evans and Prescott (1962)noted that production of "echolocation clicks"ceased if the nasal diverticula were deflated bydepressing the anterior surface of the head (overthe melon). This could be interpreted as evidencethat the nasal sacs were involved in sound produc-tion (as the authors suggested). It is also possiblethat such manipulation more firmly seats the nasalplugs, slowing the flow of air through the entiresystem.

Another line of evidence which has been broughtforward as implicating the nasal diverticula is thatthe sound field is stronger on the dorsal surface ofthe animal. As noted earlier, the evidence for thisis scanty and indicates that this is true principallyfor low frequencies. Even if this were demonstrably


the case, it does not preclude laryngeal soundproduction.

One of the underlying problems of this questionconcerns the anatomy of the nasal diverticula.Lawrence and Schevill (1956:114) described theaccessory sac (connecting sac) in such a way thatit is possible to get the impression that it has twoopenings, one into the nasal passage and one intothe nasofrontal sac. This is further implied by thename ("connecting sac") which they used for thisdiverticulum. Their illustrations, however, do notshow this to be the case. I think that this hasresulted in a number of people believing that theaccessory sac forms an alternate pathway for air toreach the nasofrontal sac. This view is implicit inseveral papers of Norris (1964, 1969) and is ex-plicit in van Heel's (1970) illustration of the nasalpassages. Norris (1964) postulated that air is forcedfrom the vestibular sacs into the nasofrontal sacs,passing around the lateral lips of the nasal plugsand producing clicks. According to him the airpasses from the nasofrontal sacs through the acces-sory sacs to the nasal passage below the level of thenasal plugs. The plugs remain seated throughoutthis procedure. When the supply of air in thevestibular sacs is depleted the nasal plugs withdrawfrom the nares and air is passed to the vestibularsacs, allowing a new cycle to start. Neither Schenk-kan (1971) nor I have found any anatomical basisfor the idea of a continuous passage for air pastthe lateral lips of the nasal plug.

The lateral lips of the nasal plugs rest withinthe common orifice of the accessory and nasofrontalsacs (the inferior vestibule), but both of these sacs(as described by von Baer, 1826; Gruhl, 1911; andLawrence and Schevill, 1956) are in fact blind.This limits the amount of air which can be passedthrough this system without pausing for recycling.

Kleinenberg et al. (1969) discussed the role ofthe nasal diverticula in sound production, basingtheir observations on the beluga. According tothem, the sound source could be located by ear inthe upper part of the nasal passages of belugasexamined on land. Tampering with the nasalapparatus by hand affected sound production.These observations, of course, dealt with sound inthe human audible range, apparently of the whistletype. They suggested that sound is produced bythe movement of air between the diverticula (withthe nasal plugs seated). This general idea has

appeared in the work of many people, usually,however, involving recycling of the air between theupper and lower respiratory passages. The explana-tion of Kleinenberg et al. (1969) involves only thesupracranial portion of the respiratory system. Thedetails concerning the operation of this mechanismwere not discussed.

Purves (1967) discussed sound production incetaceans at great length and concluded that thelarynx is capable of producing the sounds used forecholocation by odontocetes. His initial argumentis that of Occam's Razor, whereby the larynxshould be assumed to be used in sound productionunless there is some compelling reason to believeotherwise. He eliminated the lack of "true vocalchords" as an argument against laryngeal soundsource in cetaceans by noting their absence in mostmammals other than man. Mammals generallyemploy modifications of the thyroarytenoid fold,artiodactyls utilizing the aryepiglottic folds (Negus,1949). Purves carried out a series of experimentalinvestigations on the larynx and concluded that itwas capable of producing the sounds recorded fromodontocetes. He also concluded that coupling ofsound to the skull via the palatopharyngeal mus-cles would result in the observed pattern of theemitted sound field. His data do not, however,eliminate the possibility of nonlaryngeal soundproduction, as he did not investigate this aspectof the problem in his experiments.

Evans (1973) argued against Purves' theories oflaryngeal sound production on a variety of points.His observation that a "closed tube" model couldnot produce the observed sounds may be correct,but probably does not apply to the cetacean larynx,which is a complex, flexible structure, nor doesthe argument that the lack of demonstrated differ-ences in the laryngeal anatomy of whistling andnonwhistling species carry much force. The ob-served differences in sound production may belimited by behavior rather than anatomy, and,definitive anatomical studies of the larynx remainto be done.

The hypothesis proposed by Evans (1973), thatsound is produced by movement of the nasal plugsagainst the edge of the bony nares and not throughairflow past apposed surfaces, has several advan-tages. It removes the questions of complex airflowand the problem of sound production at greatdepth, where the air volume is very limited. Al-

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though it is not explicit in his papers (Evans, 1973:Evans and Maderson, 1973), it is presumed thatthis explanation is meant to cover production ofhigh-frequency clicks and not the lower frequencywhistles.

Recently Norris et al. (1971) have presented ananalysis of low frequency "chirp" production basedupon cineradiography of the head of a live Stenellalongirostris. They demonstrated complex move-ments in the nasopharynx and nasal diverticulaconcurrent with production of squeals or chirps,and concluded that the most probable site for pro-duction of these sounds was the left nasal plug.Briefly, the sequence of events described by themconsisted of movement of air (recycling) from thenasal diverticula into the nasopharynx, closure ofthe nasal plugs and posterior nasopharynx, move-ment of air past the nasal plugs into the premaxil-lary sacs, then pulsation of the tissues around theleft nasal plug, with air movement into the spacesabove the plug. The last part of this sequence wascorrelated with production of squeals. This activitywas observed only in the left naris.

One of the critical factors in this experiment wasthe determination that there was no airflow throughthe larynx during sound production. Althoughtheir arguments are convincing, the question maybe raised of the adequacy of the resolution of thecineradiography equipment to demonstrate thisconclusively. If there remains a possibility of airmovement through the larynx, the events observedabove may be correlated with movement of air intoreservoir space rather than sound production per se.As noted by the authors, their evidence relates toproduction of low-frequency squeals and not toclicks.

Schenkkan (1973) raised a series of objections tothe hypothesis of Norris et al. (1971). His state-ment that "no one has disputed that dolphins canproduce sounds with their nasal passages when thehead is above water" is irrelevant, as the authorswere not dealing with the familiar noises producedby trained animals with their blowholes open, butrather with sounds apparently identical to thesqueals produced underwater with the blowholeclosed. The nasal plugs are not essential to pre-clude water from being taken into the internalnares, as stated by Schenkkan (1973), since closurecan be effected both by the blowhole and betweenthe level of the vestibular sacs and the nasal plugs

by tissue elasticity and muscular control. The naso-palatine sphincter is capable of movement antero-dorsally, contra Schenkkan's statement, as can bereadily demonstrated by manual pressure in a freshspecimen. This muscle is very loosely attached tothe periosteum of the nasal passage and movesquite readily over it. Schenkkan's (1973) views con-cerning the loss of any air which passes distal tothe nasal plugs is based upon the assumption thatthe nasal plugs cannot be unseated underwater,which has been partly discussed above. Anatom-ically the plugs appear capable of complex move-ments, and there is no reason to assume that aircannot be moved around them without losing itout the blowhole or allowing water to enter.

Schenkkan (1973) presented a rather elaboratedescription of the functions of the nasal diverticulaand associated structures during phonation. Unfor-tunately he appears to have adopted fairly rigidideas of the possible relative movements of air andof the anatomical structures, without sufficientallowance for the complexity of the system. Hisfunctional observations are further clouded by thederivation of a sequence for the evolution of thecetacean nasal complex based upon an arrange-ment of the highly specialized living forms into asupposedly phylogenetic series.

Schenkkan (1973) argued heavily against manyof the current theories of sound production. Hisobservation that ziphiids produce echolocationclicks but do not possess lateral lips on the nasalplugs is certainly an argument against those struc-tures being used for sound production in thatgroup, and clearly suggests that echolocation clickscan be produced by some other mechanism. It doesnot necessarily apply, however, to the somewhatdistantly related and structurally different del-phinids. Nor would it be necessary, as he postu-lates, for the entire nasal plug mass to vibrate inorder to produce sound in the absence of laterallips. His argument that air expanded in vibratingthe lateral lips of the nasal plug could not berecovered is unlikely and is in contradiction tomost of his earlier statements about airflow, par-ticularly in and out of the nasofrontal sacs. Thefurther argument that clicks would be confined tothe right side and as such could not be producedinto a beamed transmission, since such transmis-sions are only produced through interferencebetween two or more sources, is incorrect. This is


indeed one way to produce a beamed pattern,which can also be produced by reflection, refrac-tion, attenuation, or any combination of these.

Schenkkan's arguments for laryngeal sound pro-duction suffer similar deficiencies. As stated in hispaper, production of relaxation oscillations througha constricted aperture is efficient, but can be appliedequally to all of the suggested sites of sound pro-duction, not just the larynx. His concept of"matched loads" equally fits all other areas of thesystem. The fact that the lips of the nasal plugsare nonmuscular has no bearing on the theoriesinvolving their action in sound production, all ofwhich postulate vibration between apposed sur-faces, not freely in an air cavity as stated by Schenk-kan. His calculations of the potential power outputof this musculature (based upon Gray's (1936)estimate of the power output of dolphin axial mus-culature) suffers from the consideration that thevisceral musculature associated with the larynxprobably differs considerably in physiological char-acteristics from the skeletal muscles used in loco-motion.

In short, Schenkkan's (1973) functional discus-sions of sound production seem to have little actualbearing on the problems involved.

The fact that odontocetes can produce both"whistles and clicks" simultaneously, starting andstopping one without affecting the other, and withno indication of one modulating the other, hasbeen cited as an indication that two separate soundsources were active (Lilly and Miller, 1961). Thisis circumstantial evidence for both the larynx andthe nasal apparatus being active in sound produc-tion. Following the suggestions of Evans (1967)and Schevill (1964), among others, that the larynxis responsible for whistles, this would leave thenasal apparatus responsible for the "echolocationclicks." It is also possible, as suggested by Norriset al. (1971), that the left nasal plug produceswhistles while the rigTit produces clicks.

One thing which must be borne in mind in anydiscussion of sound production is the possible dif-ferences between apparent and actual sources ofsound. Sound may be conducted from its actualsource to another point at which it becomes appar-ent to the observer. The evidence to date suggeststhat sound radiates from a point external to theskull, but deep within the facial complex. Thisdoes not, however, preclude a laryngeal sound

source, as sound could easily be conducted fromthe larynx to the external bony nares.

ANATOMICAL CONSIDERATIONS

Purves (1967) discussed the nature of the soundsproduced by odontocetes and concluded that theywere of the relaxation oscillation type, producedby the approximation of the walls of some portionof the nasal passage, forming an aperture throughwhich air is forced. This mode of sound productionhas also been variously referred to as "raspberry"or "Bronx cheer" sound production. If this is thecase, only those portions of the nasal apparatuswhich can be approximated to form suitable aper-tures are likely to be involved in sound production.

Unfortunately, there are a great many structuresof this description within the nasal passages anddiverticula. Thus, while it is not possible to con-clusively delimit the site of sound production onan anatomical basis, it may be possible to decidewhich structures are most likely to be involved andwhich are least likely. In production of sounds ofthis sort, it would seem that relatively small aper-tures would be advantageous, as they would permithigher velocities of airflow with the restrictedamount of air available. For the same reason,structures which can be tightly appressed are moresuitable than those which can only be looselyapproximated. It is also advantageous to have alarge reserve volume on either side of the site ofsound production to minimize the necessity forrecycling the air.

The juncture of the spiracular cavity with thevestibular sacs, while under considerable muscularcontrol, is quite wide and thus probably notinvolved in sound production. The apertures ofboth the nasofrontal and accessory sacs are heldopen by the blowhole ligament and are thusincapable of sound production by themselves. Thelateral lip of the nasal plug, however, may beinserted into the apertures of these diverticula toform an appropriate mechanism for sound produc-tion. This is the prevalent theory at the presenttime. The principal objection to this theory is thatin most species the volume of the nasofrontal andaccessory sacs is quite small. There is not, as wassometimes supposed, a connection between thedistal portion of the nasofrontal sacs and the restof the nasal passage via the accessory sac. This

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limited volume would impose serious limitationson the duration of individual cycles of phonation.

The nasal plugs are capable of being apposed toa great variety of surrounding surfaces to createapertures, some of which are suitable for soundproduction. These include the bony aperture ofthe nasal passages, the posterior wall of the spiracu-lar cavity, and the diagonal membrane. If air ispassing from the bony nasal passages into the distalportion of the nasal system, the nasal plugs mustbe partly unseated. Depending upon the move-ments of the nasal plugs, air could escape upwardvia several routes. It could pass anteriorly into thepremaxillary sacs, but the surface between thenasal plugs and the anterior edge of the bony naresdoes not seem particularly suitable for sound pro-duction. Air could also pass between the nasal plugand the diagonal membrane, entering anteriorlywhere the membrane slopes ventrally into the bonynasal passage. It could then pass posterolaterallyinto the inferior vestibule, and from there into theaccessory and nasofrontal sacs. If the nasal plugswere not closely appressed to the posterior wall ofthe nasal passage, air could then pass dorsally intothe vestibular sacs. Along this route are severalstructures which seem capable of sound production.The most likely of these are the diagonal mem-brane, where it lies against the nasal plug, and thelateral lip of the nasal plug, where it is in contactventrally with the wall of the inferior vestibule.Either of these sites would probably allow passageof air into the spiracular cavity and vestibular sacs.

The above ideas have presumed movement ofair from the bony nasal passage into the supra-cranial portion of the nasal system. There is alsothe possibility of involvement within the supra-cranial system between the diverticula or move-ment from the supracranial system ventrally intothe bony nares.

If the vestibular sacs are involved in the move-ment of air during sound production, it is mostlikely that they serve as reservoirs to receive air,rather than as sources of air. This is due to thearrangement of the anterior fold, which wouldprobably not allow passage of air toward the deeperstructures without the spiracular cavity beingopened fairly widely.

The premaxillary sacs are better suited to serveas sources for air during phonation. With the nasalplugs seated, air could pass from the premaxillary

sacs posterolaterally, ventral to the lateral lips.The insertion of ai is suitably placed to compressthe premaxillary sacs, providing the pressure neces-sary for high air velocity.

An interesting possibility is the movement of airfrom the premaxillary sacs into the bony nasalpassage past the apposed surfaces of the nasal plugand diagonal membrane. This seems like an admir-able site for sound production, except that airmovement in this direction would probably inter-fere with production of sound by the larynx. Itmight, however, be possible for air to flow betweenthe nasal plug and the posterior wall of the nasalpassage. The arrangement of musculature withinthe nasal plug is reminiscent of the intrinsic muscu-lature of the tongue, suggesting that it might becapable of complex movements.

A principal consideration in the functioning ofthe nasal structures is the levels at which thevarious portions of the system can be isolated. Thevestibular sacs can certainly be isolated from struc-tures ventral to them through the combined actionsof the anterior folds and the nasal musculature.The interaction of the deeper structures is morecomplex. As noted earlier, the apertures of theaccessory and nasofrontal sacs are held open bythe blowhole ligament, and it is only throughmovements of the lateral lip of the nasal plug thatthese diverticula might be closed. The nasal plugswould also be the critical factor in isolation of thepremaxillary sacs. In view of their possible plas-ticity, it is possible that they may be able to isolatemany of the deeper structures, allowing compli-cated airflow in this area.

As noted above, the nasal plugs are capable ofbeing apposed to a variety of structures, and areprobably capable of complex muscular activity.This agrees well with Evans' (1973) theory ofsound production by movements of the nasal plugsindependent of any airflow. As he noted (Evansand Maderson, 1973), the premaxillary sacs mayfunction as clefts allowing free anteroposteriormovement of the nasal plugs for this type of soundproduction.

In summary, it appears that the structures mostlikely to be involved in sound production are thosein the vicinity of the nasal plugs. The discoveryof musculature associated with the diagonal mem-brane renders it more likely than previously supposed that it is involved in sound production. All


of the available evidence, particularly that of theasymmetry (to be discussed later), implicates thenasal plugs in sound production.

Functional Aspects of Cranial Asymmetry

REVIEW

One of the striking peculiarities of the delphinidskull is the asymmetry of the facial elements. Theentire area of the external nares is shifted slightlyto the left. This primarily involves the elementsbordering the nares, the premaxillae and the nasals.The frontals and the maxillae are distorted to alesser degree. This sinistral displacement is mostpronounced along the median sutures between thepremaxillae, nasals, and the posterior portion ofthe frontals. The lateral sutures, between the pre-maxillae and maxillae, and the maxillae and front-als are much less affected (Figure t). The rostrumis usually free from this distortion. Correlated withthe displacement of the bones bordering the naresis an enlargement of the right-hand elements. Thisis most pronounced in the premaxillae, where theascending process of the right premaxilla is some-times half again as wide as that of the left. Onlythe facial elements are involved in this asymmetry.The internal nares and nasal passages are sym-metrical.

All living odontocetes show this cranial asym-metry to one degree or another. It seems to be leastin some of the river dolphins and is greatest in thesperm whale (Ness, 1967). Mysticetes, however, arecompletely unaffected by this phenomenon.

The question of the origin and functional sig-nificance of this asymmetry has been treated exten-sively in the earlier literature, which is reviewedin the following pages.

Pouchet (1886) ascribed the cranial asymmetryin odontocetes to a process which he termed "pleu-ronectism," derived from a comparison with theflatfish, Pleuronectes. This term was applied tosymmetry modifications resulting from swimmingon one side. Pouchet pointed out the advantages ofthe dorsal situation of the blowhole, arriving at theconclusion that the blowhole will tend to seek thedorsal surface. Thus, if the animal preferentiallyswims on one side, the blowhole will migrate tothe other side. He presented very little evidence forthe relevance of this theory to odontocetes, merely

citing the old tale of handedness in the spermwhale (see Scammon, 1874). He did note thatmysticetes swim on their sides as well, and attrib-uted the asymmetrical pigmentation of Balaenop-tera physalus to pleuronectism. He did not, how-ever, explain why this had no effect on theblowholes of mysticetes.

Weber (1886) briefly mentioned the cranialasymmetry of odontocetes and considered it incomparison with asymmetric variation seen inpinniped crania without arriving at any conclusions.

Beddard (1900) discussed the phenomenon ofasymmetry in odontocete crania. He correlated itwith the presence of a specialized nasal apparatus,but was unable to proceed further.

Abel (1902a, 1902b) provided one of the moreextensive overlooks of the question of odontocetecranial asymmetry. Noting the fundamental differ-ences between mysticetes and odontocetes in thenarial region, Abel correlated cranial asymmetryin the latter with posterodorsal displacement ofthe nares. He ascribed the immediate cause of theasymmetry to the development of the nasal andinterparietal bones during ontogeny, but was un-able to arrive at any functional or phyletic con-clusions. He did state that the asymmetric pigmen-tation of the finwhale was not related to the cranialasymmetry of the odontocetes, thus implicitly con-tradicting Pouchet's (1886) theory of pleuronec-tism. He also felt that Kiikenthal's (1893) ideasabout the relationship of the flukes to cranialasymmetry were incorrect.

Lahille (1908) examined a skull of Balaenopteraacutorostrata in which there was a slight asymmetryof the nasal bones. He correlated this with lack ofa hypoglossal canal on one side, which he feltmight have produced a physiologic asymmetry, andsuggested that cranial asymmetry in cetaceans ingeneral might be connected with similar asymme-tries in soft structures. The lack of a hypoglossalcanal on one side (the hypoglossal nerve thenexiting through the posterior lacerate foramen) isrelatively common and not connected with anyother manifestations of asymmetry. The cranialasymmetry of odontocetes is certainly correlatedwith soft part asymmetries, but not as far removedas the ventral surface of the head.

Kiikenthal (1908) was of the opinion that Ceta-cea progressed through the water with a spiralmotion of the flukes. This was based partly on the

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observations of earlier writers (Beddard, 1900) ofanimals at sea, where the motion of the flukesseemed more complex than a simple up and downstroke. It was also based on Kiikenthal's own obser-vations on fetal material (1893), where the flukesare folded in a spiral fashion. Kukenthal felt thatthis mode of locomotion produced a torque, bend-ing the head to the left, and that the cranial asym-metry was produced by the difference in waterpressure on the two sides of the head as the animalswam.

The principal defect in Kiikesthal's theory is thatthe evidence applies equally to mysticetes, in whichthere is no cranial asymmetry. Slijper (1936) sug-gested that the folding of the flukes in the fetusmay play a role in the uterus. The question ofmovements of the flukes in locomotion is very com-plex. However, there is no sound evidence for anyasymmetry in their movements (Parry, 1949).

Lillie (1910) noticed that the larynx in twospecimens of Physeter examined at a whaling sta-tion was situated on the left side of the pharynx.He concluded that this had developed to facilitatepassage of food through the gullet and that it hasresulted in asymmetric development of the nares(the idea being implicit that differential use ofthe nares in respiration resulted in the asymmetry).One would expect on the basis of his hypothesisthat the left naris would be the larger of the two.This, however, is the opposite of what actuallyoccurs. Lillie noted that Pouchet and Beauregard(1892) found the larynx to be situated on the rightin Physeter. I would suspect that the larynx ismobile, and that the position in which it liesdepends upon postmortem manipulation of thecarcass. Purves (1967:299) commented further onthis:

To complete the general description of the nasopharynx,it must be stated, that, as with the larynx, this part of therespiratory tract is perfectly bilaterally symmetrical and inmarked contrast with the upper narial region, which in theodontocete is noted for its asymmetry. Even in the spermwhale Physeter catodon, in which one of the upper nares isfrom five to seven times greater in diameter than the other,there is not the least trace of asymmetry in the posteriornarial region.

I would agree with this. However, on page 259 ofthe same paper Purves stated:

In most odontocetes the left bony narial aperture is largerthan the right and the naris follows a more vertical course.

The epiglottic spout is bent slightly to the left (markedly soin the Ziphiidae and Physeterida) and when the larynx ispushed upward into the nasopharynx the glottis movestowards the left posterior naris.

It is difficult to decide what Purves had in mind.The narial passages of the odontocetes which Ihave examined were symmetrical, except for thearea immediately adjacent to their exit from theskull. As for Physeter, the narial asymmetry is con-siderable and apparently extends well down thebony nasal passage. Hosakawa (1950) noted thatone of the intrinsic laryngeal muscles was asym-metrical in Physeter, as was the relationship of theesophagus to the larynx. He did not, however,mention that the larynx itself was asymmetrical.

Houssay (1912) agreed with Kiikenthal's corre-lation of cranial and caudal asymmetry, but thoughtthat the cause and effect were somewhat different.According to his theory, the early cetacea wereunstable, tending to capsize. This resulted in thecranial asymmetry. Subsequently the caudal asym-metry developed to correct for the instabilityproblem.

Steinmann (1912) followed the theory of Kiiken-thal (1908), but went beyond it in attempting toexplain the origin of the asymmetry in the flukes.According to this theory, cetaceans are descendedfrom ichthyosaurs and the horizontal flukes of theformer are derived from the vertical tail of thelatter. He noted that the vertebral column ofichthyosaurs extended only into the lower lobe ofthe tail, which is larger than the upper lobe. Asthe tail rotated to assume a horizontal position, thevertebral column regressed, but the former lowerlobe remained larger and the flukes retained anontogenetic vestige of this rotation in the form ofthe spiral folding observed by Kiikenthal.

Howell (1925) discussed cranial asymmetry onlyin noncetaceans and concluded that, when devel-oped to an appreciable extent, it was due to diseaseor injury.

Howell (1930) reviewed a few of the earlytheories on cranial asymmetry and dismissed themas unconvincing. He stated that he and Ernst Huberhad suspected the nasal musculature, but uponexamining it found it to be symmetrical, and wasunable to shed further light on the question.

Richard (1930) described an asymmetrical bend-ing of the hemal arches in several specimens ofthe sperm whale. From this he concluded that


unequal forces were being applied by the caudalmusculature originating from them, and that thesewere producing the asymmetry of the skull. Heapplied this theory to cetaceans in general, andsuggested that cranial asymmetry was not producedin the mysticetes because the elastic jaw joints andthe large mass of the tongue acted as cushionsto absorb the forces applied by the tail. Slijper(1936), however, stated that he could not find theconsistent caudal asymmetry upon which Richardbased his theory.

Slijper (1936), in his monograph on cetaceananatomy, gave considerable attention to the ques-tion of cranial asymmetry. Building upon thewealth of theories advanced by earlier workers(largely Abel, 1902b; Houssay, 1912; and Pouchet,1886), Slijper arrived at a phyletic and functionalinterpretation of odontocete cranial asymmetry.He accepted Pouchet's (1886) pleuronectism theoryas the immediate cause of the cranial asymmetry,and looked for the cause of the swimming insta-bility postulated by that author. Slijper's extensiveexamination of the relationships of the viscera(which are normally asymmetrically disposed invertebrates) resulted in the observation that theCetacea were uncommonly symmetrical in this area.He countered this observation by supposing that,in the transition from terrestrial forms, there musthave been an ancestral form which had the viscera(mainly the lungs) asymmetrically arranged, andthat the cranial asymmetry became fixed duringthat stage of phylogenetic development. Subse-quently Slijper (1958) discovered that the apparentorgan symmetry documented earlier (Slijper, 1936)was in error, and that the viscera of cetaceans areas asymmetrically disposed as those of terrestrialmammals.

Sleptsov (1939) investigated the state of cranialasymmetry in fetal specimens of Delphinus, Del-phinaptents, and Phocoena with regard to Kiiken-thal's (1908) theory. Sleptsov found asymmetry tobe present at an early stage and strongly criticizedKukenthal's ideas. He also measured a series offlukes and found no consistent asymmetry. Sleptsovsuggested that the cranial asymmetry resulted frommore rapid ontogenetic reduction of the olfactorynerve on the left. He also suggested that the asym-metry is useful in breathing without, however,providing any basis for this.

Purves (1967) presented the most recent discus-

sion of the problem of cranial asymmetry in odon-tocetes. He considered asymmetry of the narialdiverticula to be related to hydrostatic problems.This was based on the argument that lateral dis-placement of the blowhole is advantageous duringventilation, to reduce the amount of expired airand water vapor taken in on inspiration. It isdifficult to imagine that the observed displacementof the blowhole laterally (on the order of 1 to 2cm in a large Tursiops) has an appreciable effecton the pattern of flow of air and water vapor dur-ing expiration. At any rate, one might expect thepattern of flow in expiration and inspiration to besimilar (i.e., if expired air is expelled laterally,then inspired air should be drawn from that direc-tion as well).

Displacement of the blowhole, along with theassociated diverticula would, according to Purves(1967), result in a shift in the center of buoyancyof the head, tending to return the blowhole to amiddorsal position. In order to counteract this, thediverticula have become larger on the right. Thisdisparity of size in the diverticula is true for thedeeper diverticula, but not for the vestibular sac,to which Purves assigns a particular hydrostaticimportance. The vestibular sac is slightly larger onthe right in some animals, equal in others, andlarger on the left in some. In some genera, such asStenella, this sac is consistently larger on the leftthan on the right.

Purves (1967) further argued that paired nasalpassages of equal size are less efficient (in terms ofairflow) than if one is increased in size and theother correspondingly decreased. His argument interms of surface/volume ratio is quite plausible.However, it also follows that efficiency would beeven more drastically improved if both nasal pas-sages were increased in size, and thus is not anargument in favor of asymmetry, but of increaseddiameter alone. It would seem that if the factorscontrolling the diameter of the nasal passages wouldallow an increase in the size of one, then theymight also allow an increase in the other. Thesame net increase in efficiency gained by increasingthe size of one passage, while decreasing the sizeof the other, could be gained by a relatively smallincrease in the size of both passages. The abovearguments aside, it does not appear that the bonynasal passages, in delphinids at least, differ indiameter at any point other than their immediate

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exit from the skull. As for the fleshy portion of thepassages, the right is much larger than the left,contra Purves' arguments.

To summarize the discussion thus far, the earlytheories attempting to explain the functional basisof the cranial asymmetry fall largely into two cate-gories: (1) those based upon the assumption ofasymmetrical locomotory forces (Kiikenthal, 1908;Steinmann, 1912; Richard, 1930; Borri, 1931) pro-duced by a screwlike movement of the flukes; and(2) those based upon a buoyancy-related instabilityor some unspecified lopsidedness (Pouchet, 1886;Houssay, 1912; Slijper, 1936). Slijper (1936, 1961)presented anatomical and observational data suffi-cient to indicate that the first group of theories hasno basis in fact and concluded that the folding ofthe flukes observed in fetal material could be relatedto problems of gestation and birth. He also con-cluded that the axial musculature showed noasymmetrical development and that there was noobservational basis for asymmetrical movements inswimming. In addition, it is obvious that thosetheories apply equally well to the mysticetes. Rich-ard (1930) had countered this argument by suggest-ing asymmetrical forces were absorbed by the elasticjoints and tongue of mysticetes. But, according tothis reasoning, Physeter, with its enormous mass ofconnective tissue and fat on its head, should be theleast affected of all whales, whereas it is the mostasymmetrical in its facial anatomy.

The second group of theories can also be criti-cized on the basis that it applies equally well toboth suborders (as well as to other aquatic mam-mals) and, in fact, would apply most strongly toarchaeocetes, which show no signs of cranial asym-metry. In addition, these theories rest upon Pou-chet's (1886) hypothesis that the blowhole will tendto migrate dorsally. Thus, it would be expectedthat the blowhole would be the most asymmetri-cally situated element in the system. While theblowhole is placed slightly laterally, its relationsare not nearly as asymmetrical as those of thedeeper elements.

This brings us to the observation (Howell, 1930;Abel, 1902; Beddard, 1900) that asymmetry of theskull is correlated with the development of a com-plex nasal apparatus. This is based upon the factsthat (1) the blowhole apparatus is more complexin all odontocetes than it is in any mysticete, and(2) that the most complicated nasal complexes,

those of the physeterids, are associated with themost asymmetrical skulls.

Norris (1964) discussed cranial asymmetry as itmight relate to sound production and suggestedthat it might be instrumental in producing theobserved asymmetrical sound fields. He also sug-gested that the sound field asymmetry might bemore complicated than it seems, particularly withrespect to frequency distribution. In a later paper(Norris, 1968), he noticed that the melon enteredonly the right nasal plug in Delphinns, but did notseem to connect this with the rest of the cranialasymmetry.

Wood (1967), in a discussion of the nasal pass-ages of Kogia, made the following observation:"I think this asymmetry in the skull reflects theevolutionary development of sound producingmechanisms and the utilization of one narial pas-sage primarily for sound production, and the otherfor breathing."

This is the conclusion at which I have arrivedthrough examination of the delphinids, and whichI think can be applied to odontocetes in general.

ANATOMICAL CONSIDERATIONS

I have approached the problem of cranial asym-metry by first assuming that it is probably not thebones which are primarily asymmetrical, but thesoft tissues associated with them. This workinghypothesis is based upon the generalization thatbony elements of a complex system are likely tobe more strongly influenced by the soft tissueswhich they support than the other way around(Moss and Salentijn, 1969). Accordingly, I haveattempted to ascertain which soft structures exhib-ited the greatest degree of asymmetry, as an indica-tion of where the primary source of asymmetrymight lie.

This approach was largely confined to specimensof Stenella, which provided the only sample largeenough to take individual variation and dissectingerrors into account. The small amount of datacollected from other genera show the same trendsas the Stenella data. My data on muscle weightsconfirms the observation of Howell (1930) that themusculature is relatively symmetrical (Table 3).While a number of the weights of individual mus-cles were markedly asymmetrical in some of thespecimens, the combined weights of all of the


muscles for the specimens were less so. There isconsiderable variation in the muscle weight ratios,some of which is, no doubt, due to factors of dis-section. These factors are substantially reduced bylumping the weights for all the muscles on eachside of a specimen (total muscle weight ratio). Thisratio shows a consistent asymmetry, on the orderof 5 to 10 percent. If anything, I feel that this isdue to inclusion of more connective tissue in themuscle samples from the right sides. The tendonof insertion of these muscles is larger and, eventhough I attempted to remove it consistently onboth sides, probably accounts for some of the asym-metry. At any rate, this asymmetry is much lessthan that seen in the relative widths of the nasalpassages, which is on the order of 50 percent. Theasymmetry of the deep diverticula, as estimatedvisually, is on this order as well, as is the width ofthe lateral lip of the nasal plug. -The vestibular sacdid not appear to fit into this pattern, so it wasdissected and the epithelium of the sac weighedto obtain relative size. The data of Table 3 indicatethat for the Stenella sample, the vestibular sacsare equal in size, or slightly larger on the left, incontrast to the deeper diverticula, which are largeron the right. As with many other characters, Sten-ella coeruleoalba was an exception, the right ves-tibular sac being 50 percent larger than the left.

Having seen that the primary asymmetry prob-ably lies in the fleshy portion of the nasal complexbetween the levels of the premaxillary and vestibu-lar sacs, we can attempt to interpret it functionally.As discussed earlier in this paper, these structuresare apparently concerned with the production and/or manipulation of sound.

Since the larynx normally occupies an intra-narial position, all of the theories of sound produc-tion necessitate movement of air through thecranial portions of the respiratory tract. Observa-tions on living animals indicate that most soundsare produced without loss of air from the system,the advantages of which are obvious to a divinganimal. This means that air must be stored in thedistal portions of the system and recycled for soundproduction. Since the diverticula are larger on theright, it may be suggested that more air is cycledthrough the right-hand portions of the system. Thisis equally applicable, whether the sound is pro-duced by the larynx, around the nasal plugs, or inboth places. In any case, it suggests that greater

acoustic activity takes place on the right side. Thesame logic applies if the diverticula are consideredas reflective structures.

If the melon functions as an acoustic pathway,then its posterior extension into the right nasalplug supports both the idea of the nasal plug as asound source and the idea of greater acoustic activ-ity on the right side.

As noted above, these arguments work equallywell for laryngeal or nasal sound production. If,however, sound production by the lateral lip of thenasal plug is considered separately, some interestingpossibilities appear. The lip of the nasal plug andthe adjacent structures are larger on the right,which might render them more suitable for soundproduction.

Lawrence and Schevill (1956) presented someinteresting data relevant to the functioning of thelarge nasal plug on the right side. They observedan asymmetry in the opening and closing of theblowhole, with the left side opening earlier thanthe right. Their sequential photographs of blow-hole movements also indicate that the left passageopens wider than the right. In some of their photosit is possible to see straight down into the bonynasal passage on the left side, while the right sideis always slightly occluded by the nasal plugs. Iwould suggest that this is due both to the greatersize of the lips of the nasal plug on the right, andto the invasion of the nasal plug muscle by themelon on that side, rendering it less effective as aretractor of the plugs. It does seem clear that theright nasal passage is less effective than the leftduring ventilation. This implies that the modifica-tions on the right side must be of sufficient func-tional importance to offset the respiratory disad-vantage incurred.

Norris et al. (1971) noted asymmetric activity inthe blowhole during production of squeals inStenella longirostris. In this case, the left side wasactive, while the right side appeared quiet. Theysuggested the possibility that the left side is pri-marily involved in low-frequency sound produc-tion, while the right side may be specialized for theproduction of clicks. However, if movement of airthrough the larynx is involved in low-frequencysound production, as suggested by several workers,it would be reasonable to expect movement of airprimarily through the less specialized left naris, asin respiration.

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Taking all of the preceding arguments intoaccount, I believe that at some point in cetaceanevolution, the nasal plugs, which probably orig-inally developed as valves, became involved insound production. As a result of the mechanism ofsound production it became advantageous to in-crease their size. This, however, had an adverseeffect on ventilation, so that one passage becamespecialized for vocalization, while the other re-mained as a respiratory pathway. Consequently theblowhole was shifted slightly, to lie more directlyover the respiratory side.

A larger nasal plug requires a larger postero-lateral area in the premaxillary sac to accommodateit. As the premaxillary sac is intimately related tothe ascending process of the premaxilla, thisaccounts for that portion of the bony asymmetry.This also explains the shift to the left in the aper-ture of the bony nasal passage. The increase in thesize of the other deep diverticula may be relatedto their function as air reservoirs, reflecting ele-ments, or to direct involvement in sound production.

It must be borne in mind that the acoustic func-tioning of the structures in the odontocete head isstill poorly understood. While I have emphasizedthe possible role of asymmetry in differences insound quantity, it may equally well be involved indifferences in sound quality (e.g., sound of a higherfrequency may be differentially produced on oneside, or the asymmetry may affect generation ofharmonics).

Summary of Facial Complex Function

NASAL DIVERTICULA

The nasal diverticula probably function both asair reservoirs during phonation and as soundreflectors serving to direct the sound field ante-riorly. The exact relationships of these functionsare not known, but it seems likely that the ves-tibular sac serves as both a receptable for air andas one of the principal reflectors. The premaxillarysac may serve as a source of air during phonation.

The nasofrontal sac is more of a problem. Inmost delphinids it appears to be too small to beparticularly important as either a reservoir or areflector. In these animals its primary function maybe that suggested by Lawrence and Schevill (1956),as a partial pneumatic seal of the nasal passage

above the level of the nasal plugs. In Lagenorhyn-chus this diverticulum has been greatly enlargedand may be of considerable importance as both areservoir and a reflector. In Grampus, where theanterior portion of the nasofrontal sac is absenton the left, its effectiveness as a pneumatic seal isimpaired. The enlarged right-hand portion, how-ever, may be more effective as a reservoir orreflector.

The function of the accessory sac is difficult toascertain, as it appears to be inconsequential dueto its small size. If the source of sound is close tothis diverticulum, as is hypothesized, then it maybe important as a reflector of sound which wouldotherwise radiate laterally.

The lateral premaxillary diverticulum of Lage-norhynchus and Lagenodelphis probably servesprincipally to increase the volume of the premaxil-lary sac, substantiating the role of the latter as anair reservoir.

The pronounced directionality observed in thedelphinid sound field necessitates the presence ofan effective focusing mechanism. At the momentit seems likely that this is accomplished at least inpart 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 soundproduction. The more superficial of these muscles(pe, i, ae, and to a certain extent pi) effect closureabove the level of the nasal plug. Pi and at alsoserve to seat the nasal plugs in the orifice of thebony nasal passage. Ae and a small anterior por-tion of at are functional in opening the nasalpassage. This is in marked contrast to the interpre-tation of Schenkkan (1973), that the musculaturefunctions only to open the nasal passages.

The nasal plug muscle serves both to withdrawthe nasal plugs from the aperture of the bony nasalpassage during respiration and possibly to effectcomplex movements of the nasal plugs duringphonation.

The role of the intrinsic musculature is verypoorly understood. It is capable of altering theconfiguration of the posterior portion of the naso-frontal sac, but in which functions this would beimportant is unknown. The diagonal membrane


muscle is possibly active during phonation, servingto change the tension of the diagonal membraneand thus to alter its contact with the nasal plug.

OTHER STRUCTURES

Both the nasal plug and the diagonal membranehave been implicated in sound production. Theyalso serve to close the nasal passage at the lower ofthe bony nares. The blowhole ligament providesstability in the relationships of the deep structures,principally the apertures of the nasofrontal andaccessory sacs. It is also important in providing asurface against which the nasal plug fits to closethe nasal passages.

The melon is probably an acoustic channel, pro-viding a path of minimum resistance for soundpassing in an anterior direction. The rostral mus-culature may be involved in movements of the lipsor may be related in some obscure way to soundtransmission.

Experimental Approaches

As stated earlier in this paper, none of theexperimental data currently available allows corre-lations to be made between structure and function.It is most important to obtain comparative datawhich will allow such parameters as shape of thesound field to be correlated with differences in

anatomy of the facial complex. This will provideinformation of the structures important in shapingthe sound field. It should also be ascertainedwhether the shape of the sound field is capable ofbeing actively altered by the animal. To a lesserextent, comparative data on the frequency rangeof sound production may allow correlations to bemade with anatomical differences.

The nasal complex appears to be suitable forinvestigation by electromyography. Simultaneoussynchronized recording of muscular activity andboth vocalization and respiratory movementswould provide evidence on the function of thevarious components of this complex. These tech-niques could also be useful coupled with cine-radiography, such as used by Norris et al. (1971).

To a lesser extent, the nasal structures may bemodified experimentally in order to see what effectthis would have on sound production. Perhaps themost useful approach here would be to fill thevarious diverticula with some inert substance, suchas silicone rubber, which would alter both theirfunctioning as reservoirs and reflectors. Surgicalalteration of these elements has the drawback ofintroducing the element of trauma and thus ren-dering the conclusions suspect.

In any of these approaches it would be usefulto obtain information from as wide a morphologicrange as possible. Data on the phocoenids wouldbe of particular interest, as their nasal structure isconsiderably different from that of the delphinids.

PHYLETIC RELATIONS OF THE DELPHINIDAE

Relationships within the Delphinidae

The classification of odontocetes used in thispaper is essentially that of Simpson (1945), withthe suprageneric groupings of Fraser and Purves(1960). Peponocephala has been placed in the Del-phininae on the basis of osteological resemblancesof Lagenorhynchus, but its position here is stillsubject to question. Peponocephala electra was for-merly 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 Delphini-dae is generally felt to constitute a coherent assem-blage. The arrangement of Delphinids into sub-familial groups is a fairly recent development.Slijper (1936) made one of the better attempts toestablish groups of genera within the Delphinidae,and recognized that a distinction needed to bemade between the delphinines and the orcinines.Fraser and Purves (1960) provided the most well-founded grouping of delphinid genera, based uponcharacters of the ventral portion of the skull.

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I have found that, in general, the delphinids arefairly conservative in their facial anatomy. Thus, Ihave found no characters which consistently sep-arate the Orcininae and the Delphininae, the onlytwo subfamilies for which I have had extensivematerial. Nor do the subfamilies Steninae andLissodelphinae, for which there is comparativedata, present any major differences from thesedelphinids. The Cephalorhynchinae, as representedby Cephalorhynchus hectori, seem quite distinctfrom the other delphinids in terms of facial mor-phology. In the following discussions involving therelationships of various genera, it must be bornein mind that in some of these all of the specieshave not been examined and the conclusions aretherefore somewhat tentative.

Within the Delphinidae, Tursiops appears to bea conservative, generalized animal, and can berelated with equal facility to all but the most diver-gent species. Within the subfamily Delphininae itis structurally most similar to Stenella and Del-

FIGURE 21.—Phyletic relationships of the delphinid generaexamined in this study, based upon both data from thefacial anatomy and from the literature.

phinus. The relationships of the species in thisgroup of three genera have been examined byFraser and Purves (1960) and Mitchell (1970).They agree that Tursiops is the most generalizedof this series, and Delphinus is the most specialized.The interrelationships of the numerous species ofStenella are uncertain at this time. Mitchell (1970)has suggested that S. attenuata and S. longirostrisare the most generalized of this group, so far asexternal pigmentation is concerned, and that theother species may represent divergent specializa-tions. The data from facial anatomy indicate thatthe Stenella species form a closely related group,with only one of the species examined being un-usual. Stenella coeruleoalba differs from the otherStenella species in a number of features of thenasal diverticula. It thus appears to be theonly member of the Tursiops-Stenella-Delphinusgroup which has diverged on the basis of nasalspecializations.

In addition to the Stenella species group, thereis a large group of species gathered into the genusLagenorhynchus. Of the four species for whichinformation is available, three (L. acutus, L. obli-quidens, and L. obscurus) are essentially similar toTursiops in facial morphology, while the fourth(L. albirostris) differs in development of the nasaldiverticula. A number of authors (True, 1889;Fraser, 1966; Fraser and Purves, 1960; Mitchell,1970) have suggested that L. obscurus is similar inmany ways to Stenella, and it may be the mostgeneralized of the Lagenorhynchus species, whileL. albirostris may be the most specialized.

Lagenodelphis should probably be grouped withthe Lagenorhynchus species, as it shows a resem-blance to L. albirostris in its facial anatomy, anddiffers from the rest of the delphinids in this point.Fraser (1956), in the initial description of Lageno-delphis, suggested not only a relationship toLagenorhynchus, but also to Delphinus andStenella.

Grampus seems to be closely related to Tursiopsin osteological characters, structure of the ptery-goid air sinuses (Fraser and Purves, 1960), and theexistence of possible hybrids (Fraser, 1940). It isquite different from Tursiops in its facial anatomy,and I would be tempted to put it in a subfamilyby itself if not for the data relating it to Tursiops.

There is no anatomical information availablefor Peponocephala, which seems to represent a


development toward a bulbous-headed form fromthe Lagenorhynchus group.

The Orcininae appear to form a natural groupon the basis of development of the pterygoid airsinuses (Fraser and Purves, 1960), but specific rela-tionships within this subfamily are not clear. Fraserand Purves suggested that Pseudorca, Orcinus, andOrcaella formed a "natural sequence of specializa-tion," while Feresa and Globicephala showed cer-tain resemblances to one another and to Orcinus.Mitchell (1970) suggested a slightly differentarrangement, with Feresa and Orcinus forming onegroup, Globicephala, Orcaella, and Pseudorcaforming another. Anatomical data is available onlyfor the three genera which I dissected, Orcinus,Pseudorca, and Globicephala. Orcinus appears tobe a very generalized delphinid, which has attaineda large size and has become specialized for feedingon large prey. The melon is relatively small andstructures posterior to it show no specializations.Pseudorca is similar to Orcinus (and to Tursiops,for that matter), except in the development of alarge, elongate connective tissue mass on the fore-head external to the melon. As described earlier,there is no increase in the size of the melon, and itis thus quite different from both Grampus andGlobicephala. Globicephala has developed a sim-ilar layer of thick dermal connective tissue, buthas greatly enlarged the melon as well. In addition,Globicephala shows some specializations in thenasal diverticula, separating it from the rest of theorcinines.

Information is available for only one species ofthe Cephalorhynchinae, Cephalorhynchus hectori.The anterior portions of the nasofrontal sacs areextremely large, somewhat similar to the conditionseen in the Lagenorhynchus albirostris specimenwhich I dissected. Cephalorhynchus hectori differsmarkedly, however, in that the left nasofrontal sacis by far the larger, whereas the right is larger inall other delphinids for which there is information.Cephalorhynchus hectori was also unusual in thatthe fatty tissue of the melon did not penetrate theright nasal plug as it does in most delphinids.

Cephalorhynchus is clearly different from theother delphinids in a number of other characters,such as details of the skull, postcranial skeleton,and external body form. In some of these it showsresemblances to phocoenids, and may in fact besomewhat convergent upon them.

The Lissodelphinae (consisting only of the twospecies of Lissodelphis) show no particular speciali-zations from the general delphinid facial morphol-ogy and are separated on the basis of their peculiarelongate body form. In general cranial charactersthey are perhaps most similar to Lagenorhynchusand may represent a locomotory specialization froman origin near that genus.

The data available for the Steninae indicate ageneralized facial morphology, essentially similarto that of Tursiops. Dohl et al. (1974) reported aviable hybrid between Tursiops sp. and Stenobredanensis, suggesting a fairly close genetic rela-tionship between these genera.

Relationships to Other Families

In the structure of the face the Phocoenidae areas different from the delphinids as are any of thenonphyseteroid odontocetes. This is manifest in theform of the vestibular sac and the greater compli-cation of structures around the inferior vestibule.

The Monodontidae also represent a divergentgroup, with Monodon appearing to be more spe-cialized facially than Delphinapterus. In somerespects the monodontids resemble the phocoenids,and may actually be more closely related to thatgroup than to the delphinids. The details areunclear, however, and more work is needed toestablish the degree of relationship of these twogenera to one another and to the other delphinoidfamilies.

The data available for the Platanistidae suggestthat this is a very heterogeneous grouping ofgenera. They have been grouped in a variety ofways in different systems of classification, perhapsthe most soundly based being that of Fraser andPurves (1960) in which Inia and Lipotes aregrouped together. There is some indication, how-ever, that Lipotes and Pontoporia are related infacial structure (Hinton, 1936). There seems to begeneral agreement that Platanista is not particu-larly related to the other genera, largely on thebasis of facial characters. The relationship of thePlatanistidae to the Delphinidae is uncertain, butdoes 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

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Relationships of Bulbous-headed Delphinids

GENERAL CONSIDERATIONS

Bulbous-headed species have developed inde-pendently in a number of odontocete groups. Inthese animals some portion of the facial apparatushas become hypertrophied, resulting in a bulbousappearance of the forehead.

In the delphinines, Grampus represents an ex-treme development of this type, while Pepono-cephala shows a slight hypertrophy of this area.Hypertrophy of the facial structures is common inthe orciniines, all members of this subfamily exceptOrcinus showing it to a certain extent. In none ofthe other delphinids, however, is this conditiondeveloped.

Among the nondelphinid odontocetes, severalgroups show hypertrophy of the facial elements.The monodontids are quite bulbous-headed, as aresome of the ziphiids (Hyperoodon and Berardius).Although facial structures in the platanistidsappear to be extremely complicated, none of themhave developed a bulbous forehead. One phocoe-nid, Neophocaena, should probably be included inthe category of bulbous-headed animals. Both ofthe physeterid genera show extreme hypertrophyof this area, but in a manner totally unlike that ofthe other odontocetes.

FIGURE 22.—Phyletic relationships of the suprageneric groupsof odontocetes. (Based upon both data from the facial anat-omy and from the literature.)

another, but appear to be even more different fromthe rest of the odontocetes, and bear no particularrelationship to the delphinids.

The Ziphiidae are another unusual group whoserelationships are not clear. They are commonlygrouped with the Physeteridae, though the evidencefor this relationship is tenuous. The scanty infor-mation on ziphiid facial anatomy (Schenkkan,1973) indicates a morphology more comparable todelphinids than to physeterids, but still quite dif-ferent from either. Relationships within theZiphiidae are equally unclear.

Globicephala

Tursiopsmost othedelphinids

small largeMelon Size

FIGURE 23.—Structural relationship of the bulbous-headeddelphinids, according to which portion of the rostral tissueshas become hypertrophied.


Of the bulbous-headed odontocetes, I haveexamined material of three of the delphinids,Grampus, Globicephala, and Pseudorca.

If the structures of the facial region are exam-ined, two principal elements are seen to be involvedin this hypertrophy: (1) the melon and (2) thedermal connective tissue overlying the melon. Acoordinate system can be devised, as in Figure 23,in which the relative degree of hypertrophy ofthese elements can be presented graphically. Inthis graphic system the bulk of the delphinids, inwhich the facial structures are not hypertrophied,fall near the origins of the axes. Any displacementin a positive direction along these axes representsdevelopment toward bulbous-headedness. It can beseen from this graph that the three animals exam-ined represent the three possible extremes of devel-opment of these characters. Presumably, when theother bulbous-headed odontocetes are examinedthey will occupy intermediate positions in thissystem. Physeterids must be excluded from theseconsiderations, as they do not appear to be com-parable to other odontocetes in these characters.

COMPARISON OF Pseudorca, Globicephala, ANDGrampus

The general shape of the head differs consid-erably among these animals. In Pseudorca (Figure26) the facial mass is enlarged anteriorly, retaininga more or less streamlined configuration. In Globi-cephala (Figures 18, 26) the enlargement takesplace both anteriorly and dorsally, producing anextremely protuberant forehead (hence the com-mon name "pot-head," which is sometimes appliedto this animal). In Grampus (Figures 12, 25),enlargement is mainly in a dorsal direction, result-ing in a high forehead, which slopes steeply downto the tip of the rostrum. In addition, there is amedian sulcus on the anterior portion of the fore-head of Grampus (Figure 12), resulting in a dis-tinctly bilobed external surface.

As is indicated in Figure 23, the relative degreeof hypertrophy of the anterior facial elements dif-fers among these three animals. In Pseudorca onlythe dermal connective tissue is hypertrophied,while in Grampus only the melon is involved. InGlobicephala, which has by far the largest foreheadmass, both of these elements have increased in size.As a result, the consistency of the forehead is dif-

ferent in these animals. In Pseudorca and Globi-cephala, in which the dermal connective tissue isvery thick, the forehead mass is extremely firm andresilient. In Grampus, on the other hand, theforehead is quite soft. In this connection it isinteresting to note that a prominent feature of thebehavior of Globicephala is head-butting (Kritzler,1952; Brown, 1962). This appears to be connectedwith mating behavior. Comparable data are notavailable for Pseudorca and Grampus, but it mightbe expected on the basis of anatomical similaritiesthat Pseudorca would engage in this behavior,while Grampus would not.

The nasal diverticula present some interestingmodifications in these animals. The vestibular sacsare not remarkably different from those of theother delphinids, but lie consistently somewhatmore posterior to the nasal passage. The nasofrontalsacs of Pseudorca are similar to those of Tursiops,while Grampus and Globicephala are markedlydifferent. In Grampus the anterior portion of theright nasofrontal sac is extremely large, while thatof the left is absent. In Globicephala the generalsize and shape are not peculiar, but there is anunusual trabeculate sacculation on the angle of theright sac. None of these modifications of the naso-frontal sac, however, appear to be related to thehypertrophy of the anterior structures. The re-mainder of the diverticula in all three animals arenot notably different from those of Tursiops.

In the musculature, as in the diverticula, Pseu-dorca is similar to Tursiops, while Grampus andGlobicephala present what appear to be indepen-dent specializations. In Grampus, pe is differentfrom the condition seen in Tursiops, while in Glo-bicephala it is pi which has been modified.

The degree of cranial asymmetry does not appearto be related to development of a bulbous forehead.In fact, Globicephala is unusual in being one ofthe two known delphinids in which the melon doesnot invade the right nasal plug.

These three animals clearly represent indepen-dent developments of enlarged facial structuresIn most respects Pseudorca is conservative, whileGrampus and Globicephala represent extreme con-ditions. Very little information is available on thenatural history of these animals, making it difficultto correlate facial hypertrophy with behavior orecology. It is interesting to note that both Globi-

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dc t

a Tursiops

c t

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. Lagenorhynchusalbirostris: 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 = premax-illary sac, vs = vestibular sac).

60SMITHSONIAN 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=lateralpremaxillary sac, m=melon, npm = nasal plug muscle, ns=nasofrontal sac, ps=premaxillarysac, 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=acces-sory sac, dct=dermal connective tissue, lps=lateral premaxiliary sac, m=melon, npm=nasalplug 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 infeeding predominantly on fish. The extreme hyper-trophy of the anterior facial elements may be insome way correlated with a cephalopod diet, or itmay merely be due to coincidence.

ORIGIN OF THE ODONTOCETE NASAL APPARATUS

The nose of most mammals is a relatively com-plex organ, and there is no reason to assume thatthe nose of the terrestrial ancestor of the cetaceanswas any less complex than that of an ordinary dogor cat. It was probably provided with a series of

muscles (of the maxillonasolabialis group) capableof constriction and dilation of its orifice accordingto the ordinary needs of terrestrial animals. Duringthe course of evolution from such a terrestrialancestor to the completely aquatic Cetacea, there


should have been little difficulty in adapting thenose to fit the altered needs of an aquatic existence.Mere exclusion of water from the nasal passagesappears to present very little problem, and has beenaccomplished many times by aquatic and semi-aquatic vertebrates. The skull of the early archaeo-cetes does not indicate any special modifications inthe nasal apparatus.

Elaboration of the soft tissues of the nose incetaceans seems to have occurred after the separa-tion of the lines leading to mysticetes and odonto-cetes. As noted in the introduction, the nose of theformer is relatively simple and presents little inthe way of modification from what was probablythe primordial mammalian plan. Odontocetes, how-ever, have drastically modified the structure of thenose. If such modifications are not necessary toexclude water from the nasal passages, as is evidentfrom their absence in other aquatic mammals, thenthey are connected with some other function ofthe respiratory passages, in this case probablysound production.

The production of sound in mammals normallyinvolves movement of air through the larynx. Ifthis takes place underwater, where the animal can-not replenish its air supply, provisions must bemade to prevent the loss of air through the nostrils.This movement of air results in an increase ofpressure in that portion of the respiratory systemdistal to the larynx, proportional to the ratio of thevolume of air used in phonation to the volume ofthe distal portion of the respiratory system. Thepressure thus produced tends to force air throughthe nostrils, and poses a problem entirely differentfrom that of excluding water from the nasal pas-sages. One approach to this problem is to increasethe capability of the nostrils to retain air underpressure, the other is to increase the volume of thedistal air reservoir (assuming that the means ofsound production has not altered in order toutilize a smaller volume of air in the productionof sound).

Odontocetes appear to have approached thisproblem from both ways. The nasal musculaturehas greatly increased in size, making it possible forthe animal to close the nasal passages effectively,and at several different levels. They have alsodeveloped a series of diverticula, expanding thevolume of the reservoir available for storage of air.The mammalian nose seems to readily develop such

diverticula in response to changing needs of theanimal, as they are seen in a great variety of mod-ern mammals. Anthony (1926) discussed the ques-tion of the homology of the nasal diverticula incetaceans with those of other mammals, and con-cluded that they are most comparable to those ofperissodactyls. Cetacea, however, seem to bear noother particular resemblance to perissodactyls, andthere seems to be no reason to assume that theodontocete nasal diverticula were not developedde novo (particularly in consideration of theirabsence in mysticetes). It is easy to imagine thatany increase in the volume of the distal portion ofthe nasal passage would prove of value to the earlyodontocetes and might lead to the development ofa diverticulum. Norris (1968) has also suggestedthat the diverticula were an early developmentrelated to sound production.

The point might be raised that, since mysticetesare known to utilize underwater sound production,such a system would be advantageous to them, butis seen to be lacking. The difference between thetwo major divisions of living whales, in the struc-ture of the noses and the larynx, suggest thatspecialized underwater phonation was probablydeveloped independently by each. Mysticetes havealways been large animals, and it may well be thatthe initial volume of the nasal passage was suffi-cient for retention of air during vocalization.

Once the nasal diverticula have developed, forwhatever initial reasons, they will become effectivereflectors of sound when filled with air. It seemslikely that this has been utilized to some advantageby the odontocetes, and may now be one of theprincipal functions of these diverticula. This sameline of reasoning is applicable to the possible func-tion of the nasofrontal sac in pneumatic closureof the nasal passage.

The origin of the melon is a more difficult prob-lem. Schenkkan (1972) stated that the melon is a"degenerate, hypertrophied part of the musculusmaxillolabialis." Purves and Pilleri (1973) elab-orated this view somewhat, suggesting that themelon was initially a fibrous structure derived by"hypertrophy of the tendinous origin of the maxil-lolabialis," and that the fatty melon seen in mostodontocetes represents a degeneration of thiscondition.

One of the critical problems in understandingthe origin of the melon is our lack of understand-

NUMBER 207 63

ing of its function. It seems clear that it is struc-turally related to the insertion of the medialportion of the rostral muscle (which is equivalentto part of the m. maxillolabialis as used by theabove authors), but its functional relationship tothis muscle is uncertain. At this point it is notpossible to decide whether the musculature as suchwas once more extensive and the melon developedthrough fibrous or fatty degeneration of the muscle,whether it developed as a fibrous or fatty additionto the muscle, or whether in fact the medial por-tion of the rostral muscle was absent primitivelyand developed along with a fibrous or fatty struc-ture in this area.

The possible relation of cranial asymmetry tosound production raises some interesting evolu-tionary possibilities. If extra-laryngeal sound pro-duction in modern odontocetes is connected withcranial asymmetry, as suggested earlier in thispaper, this gives us a functional character whichcan be traced back into the fossil record. A cursoryexamination of the data available for fossil odonto-cetes indicates that many of the Miocene forms

show cranial asymmetry similar to that of theliving delphinids, and they may therefore havepossessed a similar acoustic system. The nature ofthe fossil material is such, however, that a detailedstudy is necessary to demonstrate the extent of thecranial asymmetry in the early forms.

There is, however, a comparative anatomicalapproach to the question of the origin of the mod-ern odontocete acoustical system. The fact that thecranial asymmetry in all of the odontocetes involvesa displacement of the nares to the left suggeststhat this cranial asymmetry was present in a com-mon ancestor. This raises the possibility that someof the very early odontocetes utilized the nasalapparatus for sound production and had reacheda level of specialization where one passage wasdominant in this role. Whether or not echolocationwas involved is something which we probably cannever determine. It does suggest, however, thatsound production was important and formed oneof the bases for the differentiation of the odonto-cetes from the mysticetes and from the more archaiccetaceans.

Appendix 1

CLASSIFICATION OF THE ODONTOCETES (TOOTHED WHALES)

Order Cetacea Brisson, 1762Suborder Odontoceti Flower, 1867

Superfamily Physeteroidea Gill, 1872Family Physeteridae Gray, 1821

Subfamily Physeterinae Flower, 1867Physeter Linnaenus, 1758 [sperm whale]

Subfamily Kogiinae Gill, 1871Kogia Gray, 1846 [pigmy sperm whales]

Family Ziphiidae Gray, 1865Mesoplodon 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, 1945Family Platanistidae Gray, 1863

Subfamily Platanistinae Flower, 1867Platanista Wagler, 1830 [Susu]

Subfamily Iniinae Flower, 1867Inia D'Orbigny, 1834 [Boutu]Lipotes Miller, 1918 [white flag dolphin]

Subfamily Stenodelphininae Miller, 1923Pontoporia Gray, 1846 [franciscana]

Superfamily Delphinoidea Flower, 1864Family Monodontidae Gray, 1821

Monodon Linnaeus, 1758 [narwhal]Delphinapterus Lacepede, 1804 [beluga]

Family Phocoenidae Bravard, 1885Phocoena Cuvier, 1817 [harbor porpoises]Phocoenoides Andrews, 1911 [Dall's porpoise]Neophocaena Palmer, 1899 [finless porpoise]

Family Delphinidae Gray, 1821Subfamily Delphininae Slijper, 1936

Delphinus Linnaeus, 1758 [common dolphin]Stenella Gray, 1866Grampus Gray, 1828 [Risso's dolphin]Tursiops Gervais, 1855 [bottlenose dolphin]Lagenorhynchus Gray, 1846Lagenodelphis Fraser, 1956 [Fraser's dolphin]Peponocephala Nishiwaki and Norris, 1966 [melon-

headed 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, 1964Steno Gray, 1846 [rough-toothed dolphin]Sotalia Gray, 1866 [tucuxi]

Subfamily Lissodelphinae Fraser and Purves, 1964Lissodelphis Gloger, 1841 [right whale dolphins]

Subfamily Cephalorhynchinae Fraser and Purves, 1964Cephalorhynchus Gray, 1846

64

Appendix 2

TABLES

TABLE 1.—Nomenclature of nasal structures

Presentstudy

Lawrence andSchevill, 1956

von Baer,1826

Murie,1870, 71 , 73

Gruhl, 1911 Anthony, 1926 Huber, 1934 Moris, 1969

vestibularsac

nasofrontalsac

accessorysac

premaxillarysac

Inferiorvestibule

spiracularcavity

pe

1

vestibularsac

tubularsac

connectingsac

premaxillarysar

nasal passage(constriction

sl i t )

pe

1

ae, pi

a i , pr

spritzsacke

hintere oberehflhle; vordereobere hBhle

vordereuntere hBhle

gemeinschSft-liche hBhle

— -

maxillarysac

nasofrontalsac

premaxillarysac

nasal passage

occipito-frontal is

several

?pyranidal1s

depressora l l nasi

spritzsacke

haupthflhle

blind sicke

vorderduntere hUhle

parssuperficial

parsprofunda

diverticulelateral

diverticule

diverticuleanterleur

lateral sac

nasofrontal

premaxillarysac

sac paranasalsuperieur

sac paranasal

sac paranasalmoyen?

sac nasalanterleur

sac paranasalmoyen?

pars nasal is

muscle evental,plan superieur

muscle evental,plan moyen

'Levator labii superioris alaeque nasi, zygoraaticus, levator superiorisproprius.

TABLE 2.—Muscle weight ratios (right/left) for species of Stenella (pe = parsposteroexternus; ae = pars anteroexternus; pi = pars posterointernus; ai = parsanterointernus; vest, sac = vestibular sac; total muse. = total musculature;x = mean)

s.

s.

s.

s.

£•

s.

Species

attenuata

attenuata

lonairostris

longirostris

plagiodon

caeruleoalba

Sex

HnH>tHMMM

FFFFF

M

FFFFFF

M

M

SpecimenNo.

WFP 48WFP 49WFP 51WFP 56WFP 77WFP 81JSL 91JSL 92

X =

WFP 55WFP 66WFP 73WFP 78JSL 96

X =

WFP 47

WFP 54WFP 57WFP 58WFP 74WFP 79WFP 80

X -

EOM 844

EDM 845WFP 50

Pe

0.871.371.171.311.101.180.961.11

1.13

1.371.241.542.091.42

1.53

0.78

0.721.191.441.220.970.99

1.09

-

0.910.86

Ae

_0.920.940.820.860.820.941.07

0.91

1.080.930.850.791.14

0.96

0.94

1.001.081.080.950.910.87

fl.98

0.95

1.011.23

Pi

.0.721.312.341.221.440.821.04

1.27

1.080.921.091.550.71

1.07

1.27

0.701.352.630.661.140.78

1.21

1.55

1.210.64

Ai

.1.241.091.151.011.180.971.08

1.10

1.031.121.031.090.86

1.03

1.08

1.261.100.961.181.221.20

1.15

1.03

0.881.23

Vest.Sac.

1.00.830.860.821.040.940.950.89

0.92

0.850.950.931.021.02

0.95

1.22

0.871.001.111.120.960.93

1.00

1.03

1.471.93

NasalPassage

1.47

1.261.381.681.561.471.50

1.47

1.671.26-

1.37

1.43

-

1.38

1.641.47

1.50

1.28

1.51-

total%iSC.

.32

.07

.05

.083.99.08

).95.08

.08

.07

.09

.04

.071.98

.05

.01

.04

.10

.13

.03

.08

.02

.07

.04

.90

.13


TABLE 3.—Data on specimens examined (measurements in size columnare total lengths; specimen catalog numbers are from collection ofDivision 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 blainvi l lei

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

USNMC a t a l o 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

adul t

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

USiMCatalog Nunber

396024

396018

396025

396172

396019

396033

396022

396169

396020

396017

396023

396031

396170

396026

396030

396036

396021

396035

396174

396168

396032

396173

504089

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