J. small Anim. Pract. (1979) 20,675-679.
The larynx of the Basenji dog R. R. ASHDOWN
AND
TERESA LEA
Department of Anatomy, The Royal Veterinary College, Camden Town, London NWl
ABSTRACT In two aged Basenji bitches, the lateral laryngeal saccules were absent or reduced and the laryngeal recesses (ventricles of Morgagni) were shallow compared with those of other dogs. No other significant differences were discovered. It is not yet established whether or not these anatomical features are directly related to barklessness in these dogs. The terminology used for these anatomical features is discussed. INTRODUCTION Basenjis are hunting dogs native to Central Africa. They were first exhibited at Cruft’s Show in 1895 but present-day stock in Britain is descended from animals imported between 1935and 1962(Tudor-Williams, 1976).In her detailed account of the breed Miss Tudor-Williams says (p. 9) ‘They make all the usual doggy noises . . . but the usual doggy bark is conspicuous by its absence’. She comments that ‘after nearly 40 years among barking dogs the Basenji still does not bark’, and concludes that there may be some structural basis for barklessness. Tembrock (1960a,b) studied vocalization in a wide range of Canidae and found that barking was characteristic and fundamental for the group. Oscillograms show that the typical canine bark is monosyllabic with an upper syllable limit of 1 second. Domesticated dogs tend to bark more than do wild species of the genus Canis, but some breeds bark very little (Tembrock, 1963).An anatomical study of the larynxes of two Basenji bitches has been made in the hope that this may throw some light on the problem of why these dogs do not bark. MATERIALS A N D METHODS The larynxes were removed, post-mortem, from a 14-year old female Basenji, B1 0020-4510/79/1100-0675$02.00
675
0 1979 BSAVA
676
R . R . ASHDOWN AND T . LEA
(Fula of the Congo, born in Africa) and a 12-year old spayed female Basenji, B2 (Fulafab of the Congo; born in Britain). Neither of these dogs had ever been known to bark. Both specimens were fixed by immersion in formal saline before being sectioned mid-sagittally. Similar material was prepared from seven dogs of both sexes (one Great Dane, two Greyhounds, one Wire-haired fox terrier, and three terrier-sized mongrels). The larynxes from the embalmed carcases of twenty dogs of both sexes (seven Greyhounds, two Foxhounds and eleven mongrels of various types) were also sectioned in the mid-sagittal plane. The surface features were studied in all specimens, with especial attention to the vestibular and vocal folds, the laryngeal recess (ventricle) between them and the laryngeal saccule (see Appendix for anatomical terminology). Angles and length ratios for the vocal folds were measured (Schneider, 1962) for both Basenjis and for the four small dogs in the first group of specimens. Detailed dissections of muscles, nerves and ligaments of the left halves of the two Basenji larynxes were made and compared with simultaneous dissections of the organs of the 10-year old Wire-haired fox terrier (WHFT) and two adult Greyhounds. Right and left laryngeal recesses and saccules of these were radiographed after filling with barium sulphate (Micropaque; Damancy). RESULTS Muscles, nerves, ligaments and folds showed no striking differences in the Basenjis. Angles and length ratios of the vocal folds in the Basenjis fell within the ranges of those measured in the other dogs. However, in Basenji B2 the left and right laryngeal recesses were almost completely filled by thick and solid folds of mucosa and were therefore markedly shallow and less extensive than those seen in the other dogs. In Basenji B1 the same was true, but the mucosal folds were not so solid. Also, a careful search failed to reveal any sign of a laryngeal saccule leading from the right recess in B 1, but in the left recess a small orifice was present, 3 mm wide, through which a blunted bristle could be introduced to a depth of 7 mm in the small saccule. In the larynx of B2, on both right and left sides an orifice 3 mm wide opened from the recess into a small laryngeal saccule and admitted the bristle to a depth of 6 mm. In the comparable larynx of the WHFT, the widths of the orifices into the laryngeal saccules were 6 mm and 7 mm on the left and right sides, and the depths of the saccules were 17 mm and 16 mm respectively. Similar values were obtained for the other dogs. In all of the 'normal' dogs, the saccules expanded dorsally to occupy a large space between the vestibular folds and the thyroid cartilages; the blunt end of the bristle was easily palpated in the floor or the lateral wall of the lateral food channel. In the Basenji larynxes, however, this was not so on either side and the radiographs in Fig. 1 clearly indicate the differences. The laryngeal recesses were exceptionally well developed in both specimens from Foxhounds, compared with those from the other large dogs.
L A R Y N X OF THE BASENJI DOG
FIG.1 Radiographs of the left halves of the larynxes of Basenjis B1 (upper), B2 (middle) and a Wire-haired fox terrier (lower). Barium sulphate has been used to distend and fill the lateral laryngeal saccules (arrows) and to outline the laryngeal recesses (arrow heads).
677
678
R . R . ASHDOWN A N D T. LEA
DISCUSSION Miss Tudor-Williams (1976) has drawn attention to an anatomical report on two Basenji larynxes written by Drs Small & St. Clair for Johnson (1971). They found that ‘The ventricle has a position as usual except that it is shallow. This prevents the vocal cord from being free on its lateral side. Apparently this limits the vibrations of the vocal fold’. The present authors’ findings agree with this, and they also found a marked reduction, or absence, of the laryngeal saccule which might similarly reduce the mobility of the vestibular fold. According to Pressman & Kelemen (1955), ‘a point of prime importance in respect of the phonatory efficiency of a given larynx is that the vibratory mechanism . . . has free upper margins capable of unimpeded movement . . . In man, the presence of a deep ventricle permits free unimpeded movements of the vocal cords and a resulting most efficient vocal mechanism’. Berg (1955) has suggested that the size of the human laryngeal ventricle has an effect on amplitude and frequency of sound produced. Tomograms of the larynx revealed variations in the size of the ventricle related to character and volume of the sounds being produced. Miller, Christensen & Evans (1964) suggest that in the dog these air-filled spaces allow freedom of lateral movement for vocal and vestibular folds. The oscillogramspublished by Tembrock (1960a,b) reveal that in barking there is a sudden onset of high intensity sound and it is possible that a reduction in mobility of these folds might affect ability to bark. It should be stressed that Basenjis are not lacking in vocal powers; they seem unable to bark, but can make their own special sound which Miss Tudor-Williams (1976) describes as ‘not unlike a young cockerel’s first attempt at crowing’ (p. 10). Further investigations of Basenji larynxes are needed to establish whether these anatomical features are breed characteristics and whether they cause inability to bark. Some strains of Basenjis (especially Liberian) show at least a tendency to bark (Tudor-Williams, 1976 pp. 82, 87) and the laryngeal anatomy of such dogs would be interesting. Basenji-like dogs have been reported from the Far East (Carpenter, 196243; Borgaonkar et al., 1968) and some, if not all, of these do not bark: it would be interesting to know if these non-barking dogs also show similar features of the larynx. The laryngeal recesses and lateral saccules are variable in man, and these variations may be, in part, related to race (Bartels, 1905).A major investigation of the canine larynx would be needed to evaluate the significanceof the variations that occur in the dog.
ACKNOWLEDGMENTS
We are deeply grateful to the owners who gave us permission to carry out these anatomical investigations. Radiography was by Mr S. W. Barnett.
L A R Y N X OF THE BASENJI DOG
679
REFERENCES BARTELS, P. (1905) fjber die Nebenraume der Kehlkopfhohle. Z. Morph. Anthrop. 8, 1 1. BERG,J. VAN DEN (1955) On the r81e of the laryngeal ventricle in voice production. Foliophoniat. 7 , 57. BORGAONKAR, D.S., ELLIOT,O.S., WONG,M. & SCOTT,J.P. (1968) Chromosome study of four breeds of dogs. J. Hered. 59, 157. CARPENTER, C.A. (1962-63) Basenji-like dogs of Thailand and Borneo. Sarawak Mus. J . 2,266. DORST,J. (1973) Appareil respiratoire. In TraitP de Zoologie (ed. P. Grasse) 16,5484. JOHNSON, F.B. (1971) Basenji-Dog from thepast. LESBRE,F.X. (1892) Notes prises sur le larynx de l’ane compare a celui du cheval. J. MPd. VPt. Zootech. 43,20. MILLER,M.E., CHRISTENSEN, G.C. & EVANS, H.E. (1964) Anatomy of the Dog, p. 726. Philadelphia, Saunders. NOMINA ANATOMICA VETERINARIA (1972) 2nd. edn. World Association of Veterinary Anatomists, Vienna. PRESSMAN, J.J. & KELEMEN, G. (1955) Physiology of the larynx. Physiol. Rev. 35, 506. SCHNEIDER, R. (1962) Vergleichende Untersuchungen am Kehlkopf der Robben (Mammalia, Carnivora, Pinnipedia). Morph. Jb. 103, 177. SCHNEIDER, R. (1964) Der Larynx der Saugetiere. In: Handbuch der Zoologie (eds. J. G. Helmcke, H. van Lengerken, D. Starck and H. Wermuth), 5, 1. TEMBROCK, G. (1960a) Homologie-Forschung an Caniden-Lauten. Zool. Anz. 23, Suppl. 320. TEMBROCK, G. (1960b) Lautforschung an Vulpes und anderen Caniden. Zool. Anz. 24, Suppl. 482. TEMBROCK, G. (1963) Acoustic behaviour of mammals. In Acoustic behaviour of animals (ed. R. G. Busnel), 754. Elsevier, Amsterdam. TUDOR-WILLIAMS, V. (1976) Basenjis. The barkless dogs of Central Africa. David & Charles, Newton Abbott.
APPENDIX Anatomical terminology The Nomina Anatomica Veterinaria (1972) makes no distinction between the recess situated between vocal and vestibular folds (laryngeal recess or sinus; lateral laryngeal ventricle; ventricle of Morgagni) and the extension of this recess which is seen in many mammals including the dog (lateral laryngeal saccule; appendix of the ventricle). It is possible that this terminology is based on the horse, in which the communication between the two is wide and the distinction arbitrary. However, in the donkey the two are clearly separate, communicating by a narrow duct only 5-8 mm in width (Lesbre, 1892). In most dogs, the saccule arises from a clearly defined orifice situated in the cranio-ventral wall of the recess and it extends cranio-dorsally to separate the vestibular fold from the cranial edge of the thyroid cartilage. For mammals in general, it seems that the distinction between recess (i.e. ventricle of Morgagni) and lateral saccule is valid (Schneider, 1964; Dorst, 1973) and it was therefore decided to use these terms, rather than to follow the terminology suggested by the Nomina Anatomicu Veterinaria (1972).
The larynx of the Basenji dog R. R. ASHDOWN
AND
TERESA LEA
Department of Anatomy, The Royal Veterinary College, Camden Town, London NWl
ABSTRACT In two aged Basenji bitches, the lateral laryngeal saccules were absent or reduced and the laryngeal recesses (ventricles of Morgagni) were shallow compared with those of other dogs. No other significant differences were discovered. It is not yet established whether or not these anatomical features are directly related to barklessness in these dogs. The terminology used for these anatomical features is discussed. INTRODUCTION Basenjis are hunting dogs native to Central Africa. They were first exhibited at Cruft’s Show in 1895 but present-day stock in Britain is descended from animals imported between 1935and 1962(Tudor-Williams, 1976).In her detailed account of the breed Miss Tudor-Williams says (p. 9) ‘They make all the usual doggy noises . . . but the usual doggy bark is conspicuous by its absence’. She comments that ‘after nearly 40 years among barking dogs the Basenji still does not bark’, and concludes that there may be some structural basis for barklessness. Tembrock (1960a,b) studied vocalization in a wide range of Canidae and found that barking was characteristic and fundamental for the group. Oscillograms show that the typical canine bark is monosyllabic with an upper syllable limit of 1 second. Domesticated dogs tend to bark more than do wild species of the genus Canis, but some breeds bark very little (Tembrock, 1963).An anatomical study of the larynxes of two Basenji bitches has been made in the hope that this may throw some light on the problem of why these dogs do not bark. MATERIALS A N D METHODS The larynxes were removed, post-mortem, from a 14-year old female Basenji, B1 0020-4510/79/1100-0675$02.00
675
0 1979 BSAVA
676
R . R . ASHDOWN AND T . LEA
(Fula of the Congo, born in Africa) and a 12-year old spayed female Basenji, B2 (Fulafab of the Congo; born in Britain). Neither of these dogs had ever been known to bark. Both specimens were fixed by immersion in formal saline before being sectioned mid-sagittally. Similar material was prepared from seven dogs of both sexes (one Great Dane, two Greyhounds, one Wire-haired fox terrier, and three terrier-sized mongrels). The larynxes from the embalmed carcases of twenty dogs of both sexes (seven Greyhounds, two Foxhounds and eleven mongrels of various types) were also sectioned in the mid-sagittal plane. The surface features were studied in all specimens, with especial attention to the vestibular and vocal folds, the laryngeal recess (ventricle) between them and the laryngeal saccule (see Appendix for anatomical terminology). Angles and length ratios for the vocal folds were measured (Schneider, 1962) for both Basenjis and for the four small dogs in the first group of specimens. Detailed dissections of muscles, nerves and ligaments of the left halves of the two Basenji larynxes were made and compared with simultaneous dissections of the organs of the 10-year old Wire-haired fox terrier (WHFT) and two adult Greyhounds. Right and left laryngeal recesses and saccules of these were radiographed after filling with barium sulphate (Micropaque; Damancy). RESULTS Muscles, nerves, ligaments and folds showed no striking differences in the Basenjis. Angles and length ratios of the vocal folds in the Basenjis fell within the ranges of those measured in the other dogs. However, in Basenji B2 the left and right laryngeal recesses were almost completely filled by thick and solid folds of mucosa and were therefore markedly shallow and less extensive than those seen in the other dogs. In Basenji B1 the same was true, but the mucosal folds were not so solid. Also, a careful search failed to reveal any sign of a laryngeal saccule leading from the right recess in B 1, but in the left recess a small orifice was present, 3 mm wide, through which a blunted bristle could be introduced to a depth of 7 mm in the small saccule. In the larynx of B2, on both right and left sides an orifice 3 mm wide opened from the recess into a small laryngeal saccule and admitted the bristle to a depth of 6 mm. In the comparable larynx of the WHFT, the widths of the orifices into the laryngeal saccules were 6 mm and 7 mm on the left and right sides, and the depths of the saccules were 17 mm and 16 mm respectively. Similar values were obtained for the other dogs. In all of the 'normal' dogs, the saccules expanded dorsally to occupy a large space between the vestibular folds and the thyroid cartilages; the blunt end of the bristle was easily palpated in the floor or the lateral wall of the lateral food channel. In the Basenji larynxes, however, this was not so on either side and the radiographs in Fig. 1 clearly indicate the differences. The laryngeal recesses were exceptionally well developed in both specimens from Foxhounds, compared with those from the other large dogs.
L A R Y N X OF THE BASENJI DOG
FIG.1 Radiographs of the left halves of the larynxes of Basenjis B1 (upper), B2 (middle) and a Wire-haired fox terrier (lower). Barium sulphate has been used to distend and fill the lateral laryngeal saccules (arrows) and to outline the laryngeal recesses (arrow heads).
677
678
R . R . ASHDOWN A N D T. LEA
DISCUSSION Miss Tudor-Williams (1976) has drawn attention to an anatomical report on two Basenji larynxes written by Drs Small & St. Clair for Johnson (1971). They found that ‘The ventricle has a position as usual except that it is shallow. This prevents the vocal cord from being free on its lateral side. Apparently this limits the vibrations of the vocal fold’. The present authors’ findings agree with this, and they also found a marked reduction, or absence, of the laryngeal saccule which might similarly reduce the mobility of the vestibular fold. According to Pressman & Kelemen (1955), ‘a point of prime importance in respect of the phonatory efficiency of a given larynx is that the vibratory mechanism . . . has free upper margins capable of unimpeded movement . . . In man, the presence of a deep ventricle permits free unimpeded movements of the vocal cords and a resulting most efficient vocal mechanism’. Berg (1955) has suggested that the size of the human laryngeal ventricle has an effect on amplitude and frequency of sound produced. Tomograms of the larynx revealed variations in the size of the ventricle related to character and volume of the sounds being produced. Miller, Christensen & Evans (1964) suggest that in the dog these air-filled spaces allow freedom of lateral movement for vocal and vestibular folds. The oscillogramspublished by Tembrock (1960a,b) reveal that in barking there is a sudden onset of high intensity sound and it is possible that a reduction in mobility of these folds might affect ability to bark. It should be stressed that Basenjis are not lacking in vocal powers; they seem unable to bark, but can make their own special sound which Miss Tudor-Williams (1976) describes as ‘not unlike a young cockerel’s first attempt at crowing’ (p. 10). Further investigations of Basenji larynxes are needed to establish whether these anatomical features are breed characteristics and whether they cause inability to bark. Some strains of Basenjis (especially Liberian) show at least a tendency to bark (Tudor-Williams, 1976 pp. 82, 87) and the laryngeal anatomy of such dogs would be interesting. Basenji-like dogs have been reported from the Far East (Carpenter, 196243; Borgaonkar et al., 1968) and some, if not all, of these do not bark: it would be interesting to know if these non-barking dogs also show similar features of the larynx. The laryngeal recesses and lateral saccules are variable in man, and these variations may be, in part, related to race (Bartels, 1905).A major investigation of the canine larynx would be needed to evaluate the significanceof the variations that occur in the dog.
ACKNOWLEDGMENTS
We are deeply grateful to the owners who gave us permission to carry out these anatomical investigations. Radiography was by Mr S. W. Barnett.
L A R Y N X OF THE BASENJI DOG
679
REFERENCES BARTELS, P. (1905) fjber die Nebenraume der Kehlkopfhohle. Z. Morph. Anthrop. 8, 1 1. BERG,J. VAN DEN (1955) On the r81e of the laryngeal ventricle in voice production. Foliophoniat. 7 , 57. BORGAONKAR, D.S., ELLIOT,O.S., WONG,M. & SCOTT,J.P. (1968) Chromosome study of four breeds of dogs. J. Hered. 59, 157. CARPENTER, C.A. (1962-63) Basenji-like dogs of Thailand and Borneo. Sarawak Mus. J . 2,266. DORST,J. (1973) Appareil respiratoire. In TraitP de Zoologie (ed. P. Grasse) 16,5484. JOHNSON, F.B. (1971) Basenji-Dog from thepast. LESBRE,F.X. (1892) Notes prises sur le larynx de l’ane compare a celui du cheval. J. MPd. VPt. Zootech. 43,20. MILLER,M.E., CHRISTENSEN, G.C. & EVANS, H.E. (1964) Anatomy of the Dog, p. 726. Philadelphia, Saunders. NOMINA ANATOMICA VETERINARIA (1972) 2nd. edn. World Association of Veterinary Anatomists, Vienna. PRESSMAN, J.J. & KELEMEN, G. (1955) Physiology of the larynx. Physiol. Rev. 35, 506. SCHNEIDER, R. (1962) Vergleichende Untersuchungen am Kehlkopf der Robben (Mammalia, Carnivora, Pinnipedia). Morph. Jb. 103, 177. SCHNEIDER, R. (1964) Der Larynx der Saugetiere. In: Handbuch der Zoologie (eds. J. G. Helmcke, H. van Lengerken, D. Starck and H. Wermuth), 5, 1. TEMBROCK, G. (1960a) Homologie-Forschung an Caniden-Lauten. Zool. Anz. 23, Suppl. 320. TEMBROCK, G. (1960b) Lautforschung an Vulpes und anderen Caniden. Zool. Anz. 24, Suppl. 482. TEMBROCK, G. (1963) Acoustic behaviour of mammals. In Acoustic behaviour of animals (ed. R. G. Busnel), 754. Elsevier, Amsterdam. TUDOR-WILLIAMS, V. (1976) Basenjis. The barkless dogs of Central Africa. David & Charles, Newton Abbott.
APPENDIX Anatomical terminology The Nomina Anatomica Veterinaria (1972) makes no distinction between the recess situated between vocal and vestibular folds (laryngeal recess or sinus; lateral laryngeal ventricle; ventricle of Morgagni) and the extension of this recess which is seen in many mammals including the dog (lateral laryngeal saccule; appendix of the ventricle). It is possible that this terminology is based on the horse, in which the communication between the two is wide and the distinction arbitrary. However, in the donkey the two are clearly separate, communicating by a narrow duct only 5-8 mm in width (Lesbre, 1892). In most dogs, the saccule arises from a clearly defined orifice situated in the cranio-ventral wall of the recess and it extends cranio-dorsally to separate the vestibular fold from the cranial edge of the thyroid cartilage. For mammals in general, it seems that the distinction between recess (i.e. ventricle of Morgagni) and lateral saccule is valid (Schneider, 1964; Dorst, 1973) and it was therefore decided to use these terms, rather than to follow the terminology suggested by the Nomina Anatomicu Veterinaria (1972).
