S, Afr, J, Zool. 1998,33(1) 23-30

The larynx and trachea of the barking , garrulus maculatus (Reptilia: ) and their relation to vocalization

David R. Rittenhouse, Anthony p, Russell' Vertebrate Morphology Research Group, Department of Biological Sciences, University of Calgary, 2500 University Drive N,W" Calgary, Alberta, Canada T2N 1 N4 Aaron M, Bauer Department of Biology, Villanova University, 800 Lancaster Avenue, VIllanova, Pennsylvania 19085-1699, U.S.A.

Received 13 March 1997; accepted 28 July 1997

Since its discovery by science almost 150 years ago, has been recognized as a highly vocal gekkonid, While this ability has been the SUbject of ecological and ethological investigations, and while its call has been sonographically analysed, the means of sound production has remained uninvestigated. This has been partly due to a lack of context in which to place morphological investigations of the gekkonid vocal appara­ tus, In recent years greater attention has been paid to the functional morphology of this system, and ~s form in Ptenopus can now be evaluated In a comparative light. Herein we document the morphology of the larynx and trachea by way of dissection, histological investigation, computer-assisted three-dimensional reconstruction, and scanning electron microscopy. These investigations reveal a highly unusual structure of the laryngeal skele­ ton: the cricoid cartilage is a flattened plate of cartilage; the trachea is highly folded and inserted deeply into the larynx; the laryngeal constrictor muscle is asymmetrical in males; the vocal cords are horizontally disposed; the laryngeal aditus is also horizontal and is placed much more anteriorly than in any other for which this relationship is known, Ptenopus garrulus macula/us exhibits the most anuran-like vocal apparatus yet discov­ ered in gekkonids.

*To whom correspondence should be addressed

Introduction noise so disagreeable, as to cause the traveller to Most are not considered to possess 'voices', but they change his quarters.' (Smith 1849) and can produce hisses, grunts, growls, gurgles, croaks, squeaks 'Each call consists of a series of clicks uttered in quick

. A ) and roars (Mertens 1946; Bogert 1953; Cott 1961; Bustard succession .... considerable variation in the number 9

0 1967; Blair 1968; Bellairs 1969; Campbell & Evans 1972; of clicks per call and the rate at which the clicks were 0

2 Young 1991), of the family Gek,konidae are notable uttered has been observed.' (Haacke 1969)

d among reptiles in their vocal abilities, in that the sounds they The studies of Haacke (1969, 1974, 1975) have been effective e t in demonstrating that is highly vocal, that these a emit often have tonal or harmonic qualities (Steck 1908; Ptenopus d

( & vocal signals have a social function, and that only the males Bogert 1960; Blair 1968; Werner, Frankenberg Adar 1978; r e Brown 1985; Moore, Russell & Bauer 1991). As such, geckos are involved in this behaviour, often contributing to a chorus h s while standing at the mouths of their burrows, [t ~as been i are often described as the only reptiles with true vocal abili­ l b ties (Haacke 1969), even though the vocalizations of some postulated that the funnel-shaped burrow entrance may act as u an amplifier for the call (Haacke 1969), The characteristics of P lacertid have also been reported to be tonal in quality e (B(jIune, Hutterer & Bings 1985), the call change throughout the calling period (from sunset to h t The gekkonid Ptenopus is endemic to southern darkness and sometimes through the night) and with the y b

Africa and currently comprises three species - Ptenopus changing seasons, with the winter months being periods of d e carpi, p, garrulus and P. kochi. In many respects Ptenopus silence, t n displ~ys primitive characteristics when compared with the Although significant data are now at hand to enable the a r remainder of the Afro-Madagascan gekkonid radiation calls of Ptenopus to be characterized and analysed, little is g

e (Bauer 1990; Kluge & Nussbaum 1995), and certainly lacks known of the mechanism of sound production. Haacke (1969) c n the subdigital adhesive system associated with so many summarized the speculation that had been afforded this prob­ e c i lem up to the time of his studies, He dismissed ideas that the l geckos, With respect to its vocal abilities, however, Ptenopus r shows a highly derived situation (Smith 1849; Falk 1921; sounds were produced by some form of 'tongue clicking' and e d Fitzsimons 1935; Mertens 1946; Loveridge 1947; Brain instead favoured a laryngeal mechanism of sound production, n u He predicted that because Ptenopus is 'so exceptionally 1962; Oiess 1965; Haacke 1968; Patterson 1987; Seufer y vocal' the larynx would be 'well developed' and noted that its a 1991), Since its discovery and description in 1849, it has been w structure had not yet been investigated,

e the subject of interest in this regard, from initial reports of its t

a call volume and persistence (Smith 1849), to studies of the It is now established that gekkonid vocalizations are pro­ G

acoustiQ characteristics of its call (Haacke 1969), as the fol­ duced by the vibrations of elastin-rich vocal cords, housed in t e lowing two quotes vouchsafe: a cartilaginous larynx (Moore, et ai, 1991; Rittenhouse 1995), n i

b 'In the localities in which it occurs, many individuals Although many lacertid taxa have been described as possess­ a

S may be seen peeping from their hiding places, each ing 'membranous folds' or 'vocal cords' (Meckel 1833;

y uttering a sharp sound somewhat like chick, chick; and Henle 1839; Wiedersheim 1876; Steck 1908; Vogel 1976), b

d the number thus occupied is at times so great and the elasticized folds of the laryngeal respiratory mucosa, or true e c u d o r p e R 24 S. AfT. J. Zool. 1998.33(1)

vocal cords, have only been documented in the Gekkonoidea tine scanning electron microscopy (SEM) by isolating the (Paulsen 1967; Niemann 1971; Gans & Maderson 1973). The larynges from their attached segments of tracheae, dividing vocalizations of other reptilian species are produced by for­ the larynges in half longitudinally, and dehydrating each in a cing air past the closely apposed edges of the arytenoid carti­ series of ethanol solutions of increasing concentration, over a lages ofthe glottis, or by inducing vibrations in the soft tissue period of2 h. Each laryngeal specimen was placed in a 50: 50 of the glottal lips (Henle 1839; Wiedersheim 1876; Steck mixture of hexamethyldisilazone (HMOS) and 100% ethanol 1908; Keleman 1963; Paulsen 1967; Gans & Maderson 1973; for 30 min, and then two solutions of 100% HMOS for 30 Vogel 1976; Milton & Jenssen 1979). min each. After drying, the two halves of each larynx were While geckos have long been renowned for their ability to mounted on an SEM stub cleaned with acetone, one half dor­ vocalize (Hasselquist 1757; Smith 1849) and the study of sal surface down and the other dorsal surface up. The stubs their vocal apparatus began long ago (Tiedmann 1818; were then sputter coated, and observations were made on a Meckel 1819), relatively few studies have been published that scanning electron microscope at the University of Lethbridge, document the physical characteristics of different species' Lethbridge, Alberta. calls, the social functions they perform, or the morphological The four remaining laryngeal specimens were decalcified means by which they are produced (see Niemann 1971; Gans in a I: I mixture of2% ascorbic acid and 0.3M NaCI for 24 h, & Maderson 1973; and Moore, et al. 1991 for summaries). Of following the methodology of Dietrich & Fontaine (1975). the approximately I 000 species of geckos, only about 80 Decalcified material was dehydrated and cleared, then have been reported to emit sounds, and of these accounts, embedded in paraffin wax using standard procedures. One fewer than 30 species have had their calls analysed sono­ larynx of each sex was sectioned in the tranverse plane, the graphically (Rittenhouse 1995). Furthermore, until recently other in the frontal plane. Section thickness varied between 8 descriptions of laryngeal morphology were few in number and 10 11m. Sections were mounted in Permount on glass and fragmentary in nature. A survey of the laryngeal mor­ slides and alternate slides were stained with Milligan's tri­ phology of representatives of 15 genera of AtTican and Mada­ chrome, for the differentiation of muscle and collagenous gascan geckos (Rittenhouse 1995) has augmented this data connective tissues, and Verhoeffs stain for elastin fibres base. It is in the context of these findings that we examine the (Humason 1978). structure of the larynx and trachea of Ptenopus garru/us mac­ The best set of transverse sections (female) was chosen to IIlallls and interpret it in the context of the unusual vocal abil­ be the model for a computer-based method of reconstructing ities of this taxon and its congeners. the laryngeal skeleton in three dimensions. With a projection microscope, outline drawings of the sectioned laryngeal carti­ Materials and methods lages were made at regular intervals, digitized with a flatbed . ) scanner, and aligned using NIH Image (Version 1.54) for 9 To determine the relative placement of the larynx in relation 0 Macintosh computers. Once concatenated, physical connec­ 0 to other landmarks the following measurements were taken: 2

tivity between successive outlines was provided by draping a

d snout-vent length (SVL) (measured from the anterior tip of e skin of rendered contours over all of the interstitial spaces in t the snout to the anterior lip of the cloaca); rostrum-clavicle a the digital template. The Application Visualization System, a d length (RCL) as an estimate of head length (measured from (

general-purpose visualization package for UNIX-based com­ r the anterior tip of the snout to the anterior aspect of the mid­ e puter systems, was used to visualize and render the resu1ting h line abutment of the clavicles; intergirdle length (IGL) as an s i isosurfaces. A detailied description of the methodology is l estimate of torso length (~ SVL - RCL); and rostrum-aditus b available elsewhere (Rittenhouse, Russell & Phillips 1996). u length (RAL) as an estimate of the placement of the larynx P

Infromation regarding call characteristics of Plenapus gar­

e (measured from the anterior tip of the lower jaw to the ante­ h ruluos maculatus and other taxa of Pfenopus was obtained t rior extremity of the glottal lips). These measurements were y made on a wide array of Afro-Madagascan geckos (see Rit­ form the publications of Haacke (1969,1974). b

d tenhouse 1995) and were compared with the measurements e t obtained for PlenaplIs. Results n a r Larynges were excised tTom six mature (three male, three In order to provide a contrast for the conditions found in g

e female) formalin-fixed, ethanol preserved specimens of Plenopus it is necessary to describe first the morphological c

n Plenopus garrulus maculatus on loan from the California features of a more 'typical' gekkonid, the tokay gecko, Gekko e c Academy of Sciences (CAS), San Francisco, California. Inci­ gecko (Figure I). Here the larynx is a pyramid-like elevation i l

r sions were made around the inner margin of the mandible and arising tTom the floor of the mouth. lying posterior to the e

d through the lingual and hyoid musculature to reflect the tongue and medial to the orbits (Figure la) (Moore, el al. n laryngeal complex (larynx, trachea, tongue, basihyoid). The 1991). It occupies a concavity in the palate. The anterior u

y larynx and trachea were then separated from the tongue and opening of the larynx is the glottis and at rest this opening is a

w the basihyoid by cutting the musculature and ligamentous tilted slightly dorsally. The lips of the glottis have a some­ e t attachments between these structures. Portions of the oral what lobu lar appearance and isolate the larynx form the oral a

G mucosa strongly adhering to the excised structures were not cavity (Figure I b). t e removed in order to prevent damage to them. Excised speci­ The laryngeal skeleton is cartilaginous, its main body com­ n i mens were subsequently cleaned of connective tissue and posed of a ring-shaped cricoid that bears a pair of lateral pro­ b a observed with the aid of a Wild M5 dissecting microscope fit­ cesses (Figure Ie). A pair of arytenoid cartilages articu late S ted with a camera lucida. y anteriorly with the dorsolateral parts of the cricoid and extend b One laryngeal specimen of each sex was prepared for rou- anteriorly and medially to support the glottal I ips. Posteriorly d e c u d o r p e R S. Afr. J Zool. 1998, 33( I) 25

,.. .. .'. .' , " '. .. ,": ' ...... ' . •.:. .- .- '.' '( '.: .. '.' t r . ) 9 0

0 Figure I Laryngeal stl1.!cture and position in a juvenile tokay gecko (Gekko gecko), (a) Parasaginal section through the rostrum of a tokay 2

= d indicating the positional relationships and orientation oflhe larynx within the oral cavity: scale bar 5 mm; (b) scanning electron micrograph e t of the dorsal view of the larynx oflhe tokay showing the major muscles and the glonallips; (c) diagram orlhe laryngeal cartilages and trachea, a d showing the courses oflhe arytenoid·cricoid ligaments and the vocal cords; (d) frontal section through Ihe trachea and larynx at the level orlhe (

r lateral processes orlhe cricoid cartilage: scale bar = 2 mm; (e) frontal section though the trachea and larynx at the level of the main body of the e h arytenoid cartilages: scale bar 2 mOl. Abbreviations: ad, course of the arytenoid-cricoid ligament; ar. arytenoid cartilage; cr, cricoid carti­ s = i l lage; g, glonis~ ai, glottal lips; hy, hyoid skeleton; I, larynx; Ip, lateral process of cricoid cartilage; mel, conslrlc/Or laryngis muscle; mdl, dila­ b u tor laryngis muscle; pc, concavity in roof of palate; t, tongue; tr, trachea; vc, course of vocal cords. Large arrow indicates anterior. For (a), (d) P

e and (e) th e stain employed was Milligan's trichrome~ h t y b

d the lumen of the larynx is continuous with the trachea (Figure The laryngeal skeleton of Pfenopus garrulus maculafus e t I d,e). The larynx is supported in the floor of the mouth by n The cricoid of Plenopus garrulus maculatus is a plate of car­ a r muscular and ligamentous attachments to the hyoid apparatus tilage which, with its extremely large, transversely oriented g

e (Figure I a). lateral processes, is diamond-shaped (Figure 2a,c,d). It is c n Embracing the anterior end of the laryngeal skeleton are obliquely oriented within the frontal plane, angling e c i two muscles (Figure I b), the m. cOrlStrictor laryngis that runs dorso-posteriorly from the floor of the buccal cavity. In both l

r sexes a large foramen exists about its longitudinal midline e from the basihyoid to the dorsal aspect of the cricoid, and the d (Figure 2c,d; Figure 3b,d) extending from the level of the lat­

n tn. dilator laryngis that runs from the lateral processes of the u cricoid to insert on the arytenoid cartilages. eral process to a point near the posterior border of the aditus y

a laryngis. This foramen has a transverse width equivalent to Internally the larynx is lined with respiratory mucosa. Elas­ w that of the trachea. In the female, this space appears some­ e t tin-rich ligaments run longitudinally between the arytenoid a what rectangular, and in the male is triangular. The posterior

G and cricoid cartilages (the arytenoid-cricoid ligaments) and portions of these foramina could not be observed macroscopi­ t e vertically, medial and lateral to the point of articulation, cally because they are occupied by the anterior ends of the n i between the arytenoids and cricoids (Figure Ic). The latter b tracheae. This occurs because of the cricoid's oblique angle a fonn the core of the vocal cords, but both sets of ligaments S of inclination relative to the trachea. The trachea does not

y may result in folds protruding into the laryngeal lumen and articulate with the cricoid cartilage so much as it inserts into b

d may be continuous with one another. the lumen of the cricoid (Figure 4a). e c u d o r p e R 26 s. Afc. 1. ZooL 1998, 33( I)

Figure 2 Isosurfaced reconstructions of the cricoid and right aryten~ aid of a female Ptenopus garrulus macula/us (CAS 167739) in (a) anterior, (b) lateral, (c) dorsal, and (d) perspective views. Shaded and stippled area.;; with da.:;hed borders and the open arrow depict the position and orientation of the fibers of the right half of the rn. con­ strictor laryngis in lateral and dorsal views. a, arytenoid; c, cricoid; cf: cricoid foramen; Jp. lateral process of cricoid. Scale bar = I mm.

, of . ) 9 0 0 2 d. d e t Figure 3 Camera lucida drawings of the dorsal and ventral views of a d

( the larynx and trachea of (8, b) female, and (c, d) male Ptenopus gar­ r /aryngis; e rufus macu/alus (CAS 167749, CAS 167747). ad, aditus h

s gl, glottal lip; mel, rn_ constrictor /aryngis; mdt, m. difator laryngis; i l

b t, trachea; tf, tracheal fold; trs, tracheal rings. Other abbreviations as u in Figure 2. Scale bar = I mm. Note sexual differences in the symme­ .a.t..tr\ ' P

e try of [he m. constrictor laryngis and in the shape of the cricoid ~.;t~~ h t

foramen. y Figure 4 Scanning electron micrographs of the trachea of Ptenopus b garrulus maculatus. (a) Sagittal view of the right half of the larynx d e t of P. g. macrdatus (CAS 167741), illustrating the manner in which

n The reconstructions of the arytenoids (Figure 2a,c,d) indi­

a the trachea inserts into the larynx. Dorsal is at the top of the figure r cate that these canilages are rod-shaped and project g

and the open arrow in this and subsequent figures points anteriorly. e antero-medially such that their anterior ends converge over the c fre, fold in the respiratory epithelium of the laryngeal mucosa; II. n dorsa-anterior surface of the cricoid. The posterior ends of the e laryngeal lumen. Other abbreviations as in Figure 3. Scale bar = c i arytenoids angle ventro-Iaterally to aniculate with the l

250 j.lm. (b) Dorsal view of the fold evident in the trachea of P g r dorso-medial surface of the cricoid at the level of the posterior e maculatus (CAS 167741), such that the left half of the trachea folds d border of its lateral processes (Figure 2c). The arytenoids are n over the right. Abbreviations as in Figure 3. Dorsal is up. Scale bar = u positioned such that their points of articulation with the cricoid 0.5 mm. (c) Enlargement of the fold observed in Figure 4(a) depict­ y a are immediately adjacent to the cricoid foramen and lie in ing a distinct transition in the epithelial structure over this mucosal w e close proximity to the anterior end of the trachea. fold. The dorsal region of the larynx is to the left. CC, ciliated cells; t a gc, goblet cells. Scale bar = 10 j.lm. G

t The trachea of Ptenopus garrulus maculatus e n i The trachea of P. garrulus is folded in on itself, producing a fold, along the entire length of the excised ponion of the tra­ b a longitudinal invagination, in which the left side of the trachea chea. In both sexes, the tracheal rings are relatively uniform in S tenns Df their anterior-posterior length. Those of the female y covers the right; a condition unique among gekkonid lizards b (Figures 3a,c; 4b). The tracheal rings are incomplete in this exhibit some intenracheal ring fusion (Figure 3b). The inter- d e c u d o r p e R S. Afr. J. Zoo I. 1998,33(1) 27

tracheal ring spaces are of variable thickness, dorsally and ventrally, relative to the rings that bound them. The anterior end of the trachea inserts deeply into the larynx (Figure 4a) and does not simply abut its posterior end.

The laryngeal musculature of Ptenopus garrulus maculatus The laryngeal musculature of Plenopus garrulus macu/aills consists of dilators which arise from the dorsal surface of the lateral processes of the cricoid and insert on the arytenoids, and constrictors that arise from the basihyoid and meet at the dorsal midline of the cricoid (Figure 3). In this species, the m. dilator /aryngis has a larger mass than the m. constrictor lar­ yngis. The fibres of the di lator muscles are transversely ori­ ented (Figure 3a,c) and insert into the glottal lips which delineate a dorsally-oriented aditus laryngis. The m. constric­ tor laryngis is longitudinally oriented and extends posteriorly over the trachea (Figure 3a,c) but inserts on the caudal border of the cricoid. Dorsally, the constrictor muscle is divided by a thin raphe. In the female, this strip is located in the dorsal midline of the posterior region of the cri.coid (Figure 3a) whereas in the male it is offset (Figure 3c), appearing on the right side of the specimen. Ventrally, the fibres of the con­ st rictor muscles run parallel to one another and are directed antero-m edia ll y. From a histological perspective, the m. con­ strictor laryngis of P. garrulus is composed of a deep layer and a superficial layer (Figure Sa), an apparently unique situ­ ation for geckos. Figure 5 (a) frontal section of the larynx of P g. maculatus (CAS Histology and SEM of the larynx of Ptenopus garrulus 167749) at the leve l of the dorsal-most point of the cricoid. NOie the . ) horizontally oriented voca l cords and the closu re of the laryngeal

9 maculatus 0 aditus anteriorly . vcs, vocal cords. Other abbreviations as in figures 0 The glottal lips are positioned dorsally in Ptenopus garrulus 2

2 and 3. Verhoeff's elastin stain . Scale bar = 500 llm. (b) Transverse

d maculatus (Figure 4a), medial to the dorsal halv es of the ary­ e section of the left glottal lip of P. g. maculatus (CAS 167739), half­ t tenoid cartilages, and extend from the anterior tips of the ary­ a way along the length of the arytenoid. e, elastin; am, oral mu cosa; re, d tenoids to the anterior, mid-dorsal margin of the dorsal­ ( respi ratory epit helium of the larynx ; rm, laryngeal respiratory r posterior part of the cricoid. The glottal lips, compared to the e mucosa . Verhoeffs elastin Slain. Scale bar =: 150 llm. h

s cond ition of other geckos (Moore, et al. 1991), contain a i l moderate amount of loose connective tissue (Figure 5b). A b u random distribution of longitudinally-oriented elastin fibers is

P glottal lips (Figure 4a). A distinct epithelial transition was e present in the loose connective tissue of each glottal lip. The seen on the cord-like structures found in Ptenopus garrulus. h t few venous spaces that are present indicate that the glottal The respiratory mucosa directly over these structures consists y

b lip s of Ptenopus garrulus maculatus do not have the struc­ entirely of goblet cells, but adjacent to these fold s, both dor­ d tural characteristics of erectile tissue, as is evident in certain e sally and ventrally, the goblet cells are interspersed with t other geckos (Moore, 1991; Rittenhouse 1995). n et al. numerous ciliated cells (Figure 4c). The epithelium consists a r The arytenoid-cricoid li gaments are located between the

g ofa glandular stratified cuboidal type medially, a pseudostrat­

e ventral surface of the arytenoids and the dorsal surface of the

c ified type ventro-mediall y, and simple cuboidal epithelium

n cricoid, and are elasticized along their medial sides.

e along the ventral border of the vocal cords. c

i The vocal cords are prominent, hori zontal bands of elastin l

r that run the entire length of the ventral aspects of the glottal e Discussion d li ps (Figure Sa). As such, the vocal cords are situated dorsal n The laryngeal morphology of Ptenopus garrulus maculalUs u to, rather th'an anterior to, the arytenoid -cricoid ligaments , the

y entire larynx having been rotated dorsally relative to the ' typ­ differs markedly from that of all other geckos examined. a

w ical ' condition. There is no continuity between the elastin From a phylogenetic perspective perhaps the most appropri­ e t present in the vocal cords and the arytenoid-cricoid liga­ ate taxa for comparison are members of the large radiation of a

G ments. The elastin fibres in the vocal cords are dense and lon­ African and Madagascan geckos that appears to constitute the t e gitudinally oriented, and li e beneath the lamina propria ofthe sister group of Ptenopus. The exact make-up of this sister n i laryngeal mucosa (Figure Sa). group is debatable, as Ptenopus may have its closest affinities b a The examination of the laryngeal mucosa by scanning elec­ either with a southern African-Madagascan clade (Joger S

y tron microscopy revealed a distinct horizontal fold in the res­ 1985; Bauer 1990) or with a more broadly construed b piratory epithelium along the ventro-medial border of the Pan-African clade as a whole (K lu ge & Nussbaum 1995). In d e c u d o r p e R 28 S. Mr J. Zool. 1998, 33(1)

practical tenns, however, the implications for the interpreta­ anteriorly. Consequently, the musculature of the larynx and tion of laryngeal morphology are identical; the character the buccal cavity may contribute to the production of the states illustrated by Ptenopus are virtually all autapomorphic, voice, especially if taut (Steck 1908). The elongated, plate­ and consequently the larynx and trachea of Ptenopus are no like cricoid cartilage is unique amongst geckos and is signifi­ more similar to closely-related taxa than they are to those of cant in the horizontal alignment of the vocal cords in the rest­ more distantly allied fonns. ing position of the larynx. The cricoid of Ptenopus is not ring-like but has instead Additionally, Ptenopus garrulus maculatus has a longitudi­ become flattened into a broad plate. Its posterior end receives nal invagination along the dorsal surface of its trachea. This rather than abuts with the trachea. The vocal cords, owing to suggests that the trachea is capable of being inflated, and of the flattened nature of the cricoid and its articulation pattern containing a relatively large volume of air that could be used with the arytenoid cartilages, are horizontally rather than ver­ to create more forceful exhalations. Also, the large membrane tically oriented in the resting position. The m. dilator /aryngis of the fold that separates the ends of tracheal rings could initi­ is extremely large, and it is this muscle that is responsible for ate vibrations that are amplified in the larynx and oral cavity the dorso-Iateral rotation of the arytenoid cartilages on the of this species. cricoid and the parting of the glottal lips. The m. constrictor How Ptenopus garrulus maculatus expands this fold is not laryngis, which is responsible for altering the shape of the known. One possibility is that the contraction of the longitu­ aditus and placing tension on the vocal cords, is unusual in dinally-oriented fibres of the m. constrictor laryngis could several respects. Firstly, it extends posteriorly as far as the cause the cricoid to rotate anteriorly, such that it, the aryten­ anterior extremity of the trachea. Secondly, its fibres are sig­ oids and the vocal cords become vertically oriented, lying at a nificantly longitudinally oriented. Thirdly. this muscle con­ near right angle to the trachea. Because the membrane lining sists of two distinct parts on each side. Fourthly, where the the laryngeal lumen is continuous with that present within the left and right neighbours of this pair unite there is apparent tracheal invagination, this rotation could cause the expansion sexual dimorphism. [n the female, the muscles of the two of the tracheal fold as the larynx becomes more upright. The sides meet in the sagittal plane, where they abut onto a tendi­ unique cricoid-tracheal 'articulation' in this species, the nous raphe, whereas in the male the belly of the left side almost spherical shape of the head that is relatively short crosses the sagittal plane so that the abutment of the pair lies when compared to postcranial body length (Figure 6a), the slightly to the right of the body long axis. In taxa, such as relatively anteriorly-displaced aditus laryngis (Figure 6b), the Gekko gecko the m. constrictor laryngis and the In. dilator free posterior end of the cricoid, and the large foramen that laryngis probably work in concert to carry out dorso-Iateral represents the lumen of this cartilage, would all seem to allow

. rotation of the arytenoids, parting of the glottal lips, alteration this anuran-like (Gans 1973), laryngeal gyration to occur. )

9 of the shape of the aditus, and tensing of the vocal cords. The Paulsen (1967) has stated that the cricoid of the tokay (Gekko 0

0 morphology of the situation in Ptenopus garrulus, however, gecko) is drawn forward and into a more upright position just 2 suggests that the 111. to d dilator laryngis dominates in elevating prior vocalization. Future in vivo laboratory observations e t the vocal cords dorsally and placing the glottal lips into appo­ are needed to detennine if this is also the case in the Pteno­ a d sition. pus. ( r

e In Ptenopus garrulous maculatus the aditus laryngis lies in The above-mentioned features of the larynx and trachea h s the horizontal plane, such that air exhaled from the respira­ and the potential results of the movements between them can i l

b tory tract is directed dorsally. [n this way, the sound that is be related to field observations. It has been noted that in asso­ u produced may have more opportunity to resonate within the ciation with calling, the throat is expanded and deflated P

e oral cavity than it would if the air flow was directed more (Brain 1962; Haacke 1964) and the mouth is opened and h t y b d e ~ .-,---,---.--.--,--. t

n II) a :::l r ~ g e c n

e 1 c

i E l

:::l

r .... e .... II) d

n o u

c::: y a w

e .9 t b. a G Log Intergirdle Length Log Intergirdle Length t e n i Figure 6 Geometric Mean RegreSSions representing the isometric relationships of (a) head size to body size, and (b) laryngeal position with b a the bucca! cavity to body size across 15 Afro-Madagascan genera (n = 123; taken from Rittenhouse 1995). The positions of the scatter plots for S

y PlenoplIs garrulus maculalUs relative to the GMR axes illustrate that the head of this species is comparatively short, and that the aditus laryn­ b gis is displaced anteriorly d e c u d o r p e R S. Afr J. Zool. 1998,33(1) 29

closed in a rhythmic fashion for the emission of each click. Acknowledgements This is accompanied by small jerks of the head. The sound Specimens for examination were kindly made available by emitted is very loud, especially for the size of the Jens Yin dum of the California Academy of Sciences. Funding involved, and "under ideal conditions can be heard for several for this project was provided from an NSERC operating grant hundred yards' (Haacke 1969). It is evident that considerable to A.P. Russell. Doug Phillips helped extensively with the force is needed to generate a call of such volume, and the computer reconstruction techniques and Doug Bray with the combination of an inflatable trachea and elongated vocal scanning electron microscopy_ Laboratory assistance was ren­ cords borne within a larynx capable of pivoting could well be dered by Yolanda de yilbis and Carl Scutz. significant in this regard. The jerking of the head could be involved with the explosive emission of air fTom a pre-pres­ References surized trachea. Further observations on the lungs and the BAUER, A.M. 1990. Phylogeny and biogeography of the geckos of complete airway system are necessary to evaluate this southern Africa and the islands of tile western Indian Ocean: A hypothesis further. preliminary analysis. In: Vertebrates in the tropics. (Eds) Peters. The fact that only male Plenapus seem to call spontane­ G. and R. Hutterer. Museum Alexander Koenig, Bonn. ously (Haacke 1969) is suggestive that there might be signifi­ pp. 275-284. cant sexual dimorphism in laryngeal structure. There are, BELLAIRS, Ad'A 1969. The life of reptiles. Wcidcnfeld and Nicolson, London. however, only two features that are noticeably sexually BLAIR, W.F. 1968. Amphibians and reptiles. In: Animal dimorphic - the location at which the posterior ends of the communication, (ed.) Sebeok, T.A. Indiana University Press. m. constrictor laryngis meet; at the midline in the females, Indianapolis. somewhat offset from the midline in males, and the anterior BOGERT, C.M. 1953. The tuatara: why is it a lone survivor? Sci. extremity of the cricoid foramen is squared off in the female Monthly, 86: 163-170. but triangular in the male (Figure 3a,c). These differences are BOGERT, CM. 1960. The intluence of sound on the behaviour of not, in themselves, suggestive of a major difference in func­ amphibians and reptiles. In: Animal Sounds and Communication tion. The morphology of the larynx and trachea, as far as we (cds.) Lanyon, W.E. and W.N. Tavolga. American Institute of can ascertain, is constructed in such a way as to allow phona­ Biological Sciences, Washington, D.C. tion. That the females do not do this may be determined either BOHME, W., MUTTERER, R. & BINGS, W. 1985. Die Stimme der I,acertidae, speziell der Kanareneidechsen (Reptilia: Sauria). by social interactions that inhibit it, or it may be reflective of Bonn. Zool. Beitr. 36: 337-354.' as yet unidentified anatomical dimorphism in terms of the BRAIN, C.K. 1962. A review of the gecko genus Ptenopus with the motor control of central pattern generators. Such neurologi­ description ofa new species. Cimbebasia I. 1-18. .

) cally-based sexual differences have been shown to be respon­ BROWN, AM. 1985. Ultrasound in gecko distress calls (Reptilia: 9

0 sible for differential vocal abilities between male and female Gekkonidae). Isr. 1. Zoo/. 33: 95-10 I. 0

2 Xenopus laevis (Tobias & Kelly 1988). BUSTARD, H.R. 1967. The comparative behavior of chameleons:

d fight behavior in Chameleo graciliS Hallowell.lferpetologica 23: e The combination of the circumstantial correlation between t a the highly modified vocal apparatus, the exceptionally 44-50. d

( CAMPBELL, H.A., & EVANS. W.E. 1972. Observations on the well-developed vocal abilities of Plenopus, and the model of r vocal behavior of chelonians. Herpelologica 28: 277-280. 17 e how sound production may be developed by such a system h

s COTI', H.B. 1961. Scientific results of an enquiry into the ecology i l strongly supports the contention of Haacke (1969) that the and economic status of the Nile crocodile (Crocodylus nita/ieus) b source of vocalization is the larynx. Further, it appears that u in Uganda and Northern Rhodesia. Trans. Zool. Soc. London 29' P the trachea and laryngotracheal connection of Plenapus are 211-356. e h also highly derived, and that the highly developed vocal capa­ DIETRICH, H.F.& FONTAINE, AR. 1975. A decalcification t

y bilities of this taxon are almost certainly associated with such method for ultrastructure of echinoderm tissues. Stain Technology b 40: 351-354.

d a specialized system as a whole. e t Why such a system should have evolved uniquely in Plen­ FALK, L. 1921. SOdwestafrikanische reptilien und ihrc Heimat. n Wschr. Aquar. Terrar. Knde. 18: 6-8,21-23,58-59, 114-115, a opus, or more broadly why a social system of this complexity r 125-127, 176-178,231-232,248-250.286-288,304-307. g should exist still remains unknown. Although hypotheses e FITZSIMONS, V.F. 1935. Notes on a collection of reptiles and c may be put forth for such evolutionary questions they will be n amphibians made in the southern Kalahari, Bushmanland. and e c difficult to test because phylogenetic patterns remain poorly i Great and Little Namaqualand. Ann. Transvaal Mus. 15: 519-550. l

r resolved and because no putative relatives appear to exhibit GANS, C. 1973. Sound production in the Salientia: mechanism and e

d similar morphologies or behaviours from which those of evolution ofthe emitter. Am. Zool. 13: 1179-1194. n GANS, C. & MADERSON, P.FA 1973. Sound producing

u Plenapus might be reasonably derived. Alternatively, the

y model of phonation outlined in this paper can be tested by the mechanisms in recent reptiles: review and comment. Am. Zool. a 13: 1195-1203. w application of dynamic morphological methods, in particular e GIESS, W. 1965. Chondrodaeiylus anguliji::r (Peters) and Ptenopus t a combination of electromyography, force and pressure trans­ a garruJus (Smith) from the Brandberg. Cimbebasia 12: 16-19.

G duction recording, sonograms, and high speed videography. If

t HAACKE W.O. 1964. Description of two new species of lizards and e our model of phonation is correct then the situation found in notes on Fitzsimonsia brevipes (Fitzsimons) from the central n i Ptenopus may be the closest to an anuran type of vocalization b Desert. Sci. Pap. Namib Res. SIn. 25: 1-15. a system yet identified in gekkonids. The considerable progress

S HAACKE,W.O. 1968. The burrOWing geckos of southern Africa.

y made in the study of anuran vocalization could then be M.Sc.Thesis. University of Pretoria. b adopted to further the understanding of gekkonid phonation. HAACKE, W.O. 1969. The call of the barking geckos (Gekkonidae: d e c u d o r p e R 30 S. Afr. J. Zool. 1998,33(1)

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