Topography of the digital cutaneous sensilla of the tokay gecko, Gekko

Topography of the digital cutaneous sensilla of the tokay gecko, Gekko gecko (Reptilia, Gekkonidae), and their potential role in locomotion RANDOLPH F. LAUFF Department of Biology, McMaster University, 1280 Main Street W , Hamilton, ON L8S 4K1, Canada

ANTHONY P. RUSSELL~ Vertebrate Molphology Research Group, Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, AB 72N l N 4 , Canada AND

AARONM. BAUER

Can. J. Zool. Downloaded from www.nrcresearchpress.com by St. Francis X Univ on 09/17/15 For personal use only.

Biology Department, Villanova University, Villanova, PA 19085, U.S. A. Received June 29, 1993 Accepted September 24, 1993 LAUFF,R.F., RUSSELL, A.P., and BAUER, A.M. 1993. Topography of the digital cutaneous sensilla of the tokay gecko, Gekko gecko (Reptilia, Gekkonidae), and their potential role in locomotion. Can. J. Zool. 71: 2462-2472. The external morphology of the cutaneous sensilla of the dorsal digital scales of the tokay gecko, Gecko gecko, is described and the distribution of the various sensillar types is mapped. Three types of sensilla are identified: bristleless, bristled unbranched, and bristled branched. Bristleless sensilla occur only on glabrous scales and are largely restricted to the toe base and phalangeal scales. They may register stimuli other than those associated with scale-to-scale contact. Bristled unbranched sensilla are recessed and are located on the paralamellar, phalangeal, paraphalangeal, and toe base scales, but the bristled branched variety is largely restricted to the paraphalangeal region. The mechanoreceptive role of the bristle-bearing sensilla is related to their placement on individual scales and their distribution across the digit. Placement of the sensilla accords well with patterns of scale-to-scale and scale-to-substrate contact that occur during digital hyperextension and plantarflexion. Such proprioceptive monitoring of regions of the digit during locomotion may be of considerable significance in the control of the establishment and sundering of the adhesive bond that occurs between the setae and the locomotor substrate. LAUFF,R.F., RUSSELL, A.P., et BAUER, A.M. 1993. Topography of the digital cutaneous sensilla of the tokay gecko, Gekko gecko (Reptilia, Gekkonidae), and their potential role in locomotion. Can. J. Zool. 71 : 2462 -2472. La morphologie externe des sensilles cutanCes des Ccailles digitales dorsales a CtC CtudiCe chez le lCzard Gecko gecko; on en trouvera ici la description, ainsi qu'une carte de rdpartition des diffdrents types de sensilles. Trois types de sensilles ont CtC identifiis : les sensilles sans soies, les sensilles simples a soies et les sensilles ramifides a soies. Les sensilles sans soies sont situCes sur des Ccailles glabres et sont en grande partie restreintes aux Ccailles de la base des orteils et aux Ccailles des phalanges. Ces sensilles enregistrent peut-bre des stimulus autres que ceux qui sont associCs aux contacts Ccaille sur Ccaille. Les sensilles simples a soies sont enfoncCes et sont situCes sur les Ccailles paralamellaires, phalangiennes et paraphalangiennes ainsi que sur les Ccailles sises a la base des orteils, mais les sensilles ramifiCes a soies sont en majorit6 restreintes a la rCgion paraphalangienne. Le r61e mCcanorCcepteur des sensilles a soies est relid a la position de ces sensilles sur des Ccailles particulikres et a leur rCpartition sur le doigt. La position des sensilles correspond bien aux patterns des contacts Ccaille sur Ccaille et Ccaille sur substrat qui se produisent au cours de l'hyperextension du doigt et au cours de la flexion plantaire. Un tel sondage proprioceptif des rCgions du doigt au cours de la locomotion peut s'avCrer trks utile pour I'Ctablissement et le partitionnement du lien d'adhCsion qui s'Ctablit entre les soies et le substrat. [Traduit par la rddaction]

Introduction Sensory organs were first noted in lepidosaur skin over 100 years ago (Leydig 1868; Cartier 1872; Todaro 1878) and have since been described in detail. Such cutaneous organs have been reported from a wide array of lizard groups, including xantusiids (Peterson and Bezy 1985), scincids (Perret and Wuest 1982, 1983; Irish et al. 1988), and iguanians (Cohn 1914; Schmidt 1920; Scortecci 1937, 1941; Hiller 1978; Schleich and Kastle 1984, 1985; Ananjeva et al. 1986, 1991). The most data, however, are available for gekkonids (see Bauer and Russell 1988 and Ananjeva et al. 199 1 for a review of pertinent literature). Histological investigation has demonstrated a general uniformity of internal sensillar structure across gekkonid taxa (Schmidt 1911, 1912, 1913; Hiller 1971, 1976; Whimster 1980) and an overall structural resemblance to the sensilla of iguanians (Ananjeva et al. 1986, 1991). The surface morphol'Author to whom all correspondence should be addressed. Printed in Canada 1 lrnprirne au Canada

ogy of these organs varies considerably, however. Various sensillar architectures have been described for geckos, including bristleless (Russell and Bauer 1987), single- and multiplebristled (Hiller 197 1; Stewart and Daniel 1975), and bristled with secondary hairs (Hiller 197 1; Bauer and Russell 1988). Schmidt (19 13, 1920j also reported a fourth type in Uroplatus: a central bristle is lacking but a field of enlarged setules covers the surface of the organ. Other organ types have been reported for other squamate groups (Landmann 1975; Lang 1989), but have not been identified in geckos. Topographic variation in sensillar morphology and position and the functional implications of such variation have not been adequately addressed. Wherever the organs occur, however, they are usually positioned close to the edges of scales and are innervated and located so as to provide tactile sensory information (Miller and Kashahara 1967). The morphology of the sense organs may vary in a single individual (Peterson and Bezy 1985) and even across a single scale (Hiller 1971). Cartier (1 872) indicated the presence of single-, double-, and bifid-


LAUFF ET AL.

bristled sensilla on a single scale of the flank in Ptyodactylus natalensis. (Ptyodactylus natalensis is an unknown synonym, perhaps of Afroedura sp.) Overall regional variation in number and location of sensory organs in geckos was discussed by Cartier (1872) and Schmidt (1912, 1913, 1920). These structures occur on almost all areas of the body, but are most concentrated on the head and the dorsal aspects of the trunk and appendages. The prevalence of tactile receptors on the scales bordering the digits of geckos and other lizards has long been noted (Schmidt 1913; Audy 1953; Hiller 1968; Stewart and Daniel 1975; Schleich and Kastle 1985; Bauer and Russell 1988). Such organs have also been observed between the pairs of plates in the divided scansors of Hemidactylusfrenatus (Audy 1953) and on the proximal portions of the scansors themselves in Hoplodactylus maculatus (Bauer and Russell 1988) and Gekko gecko (Hiller 1971). Schleich and Kastle (1985) recorded single-bristled organs from subdigital scales distal to the scansorial pad and multiple-bristled organs on lateral digital scales in Anolis cybotes. In general, sensory structures are absent from the soles of the feet and from the fields of scansorial setae themselves (Hiller 1971; Stewart and Daniel 1975). Only one study to date has examined the variation in sensory organ structure with position on the digits. Gourvest (1960) found in Tarentola mauritanica that the dorsal and lateral scales of the toes generally bore lenticular organs on their distal margins. Bristled receptors with three stalks, similar to those reported by Todaro (1878), were found by Gourvest (1960) elsewhere on the body, including the paralamellar scales. This distribution has suggested to previous authors a role for the cutaneous sense organs in locomotion, although no explicit functional correlation between sensillar morphology and the locomotor cycle has been established (Hiller 1971). Hiller (1976) proposed that the sensilla might function in registering the degree of scansorial contact with the substrate and (or) in detecting whether the substrate is wet. Sensilla may be accompanied by subepidermal lamellated receptors that are vibration sensitive (Hiller 1977). In this paper we present information on the distribution of the several types of sensilla occurring on the scales of the dorsal surface of the digits of the tokay gecko. We propose that the topography of the sensillar types is related to the phenomenon of digital hyperextension that is typical of pad-bearing geckos during normal locomotion (Russell 1975, 1981a , 1981b, 1986). As the distal portions of the digits are curled back from the substrate during the release of the scansors from adhesive contact, the dorsal digital scales become deformed and impinge upon each other in a variety of ways (see below). From these observations we hypothesize that the dorsal digital scales should be well endowed with mechanoreceptors and that the distribution of these should reflect the patterns of distortion induced by hyperextension. Furthermore, we hypothesize that the distribution and (or) morphology of mechanoreceptive sensilla on the toe base and that part of the digit undergoing hyperextension should differ according to differential patterns of distortion. We also document the disposition of the sensilla borne by the paralamellar scales in relation to; the monitoring of contact during pedal plantarflexion.

Materials and methods Four female tokay geckos (Gekko gecko; snout vent length 118 f 3.5 mm) were euthanized by oral administration of sodium penta-

scales

FIG. 1. Oblique dorsal view of digit I11 of the left pes of Gekko gecko, showing regions examined for sensilla. The broken line delimits the portion of the digit illustrated in Fig. 4. barbitol, and the third digit of each pes was removed for processing for light microscopy (LM) and scanning electron microscopy (SEM). Toes were fixed in either neutral phosphate-buffered formalin (300 mosM) or 2.5 % buffered gluteraldehyde (pH 7.3; in 0.3 mosM cacodylate buffer; 4°C). Tissues for LM were stored in 70% EtOH. Specimens for LM were embedded using either paraffin wax or a JB-4 embedding kit (Polysciences, Warrington, Pa.). Transverse and longitudinal sections were cut on a rotary microtome at 10 pm or on Sorvall Porter-Blum JB-4 microtome, using glass knives at 3 pm. Mounted sections were stained with haematoxylin and eosin, periodic acid - Schiff s reagent with haematoxylin, or Masson's trichrome. Additional, previously prepared microscope slides were used to confirm results and to check a variety of details. Digits examined by SEM were postfixed in phosphate-buffered 1 % OsO, for 1 -2 h and dehydrated through a graded ethanol series before being critical-point dried (Polaron critical-point dryer) and mounted on aluminum stubs with either silver paint or epoxy. The samples were sputter-coated with gold to a thickness of 16- 19 nm. Samples were viewed on an ISI-DS 130 dual-stage scanning electron microscope. Photomicrographs were taken on Polaroid type 55 PIN film. The distribution of sensilla was mapped with respect to four categories of supradigital scales: paralamellar (subtending) scales at the digital margins, phalangeal scales (those overlying the phalanges), paraphalangeal scales (those lateral to the phalanges), and basal scales, proximal to the scansor-bearing region of the digit (Fig. 1). Additional, previously prepared specimens were employed to verify details.

Results Morphology Three morphologically distinct cutaneous mechanoreceptors were found on the dorsal scales of the toe (Table I). Bristleless lenticular sensilla are characterized externally by unadorned papillae that are flush with the scale surface or raised slightly above it, but separated from the remainder of the scale surface


CAN. J. ZOOL. VOL. 71, 1993

FIG.2. A cluster of scales on the toe base (a) and the most basal paralamellar ( A ) and paraphalangeal ( A ) scales. The toe base scales have only bristleless sensilla (BL); the paralamellar and lateral paraphalangeal scales have only bristled unbranched sensilla (BU). Distal lies to the left of the figure, lateral to the bottom. Scale bar = 150 pm.

TABLE1 . Distribution of receptor types among the scales of digit I11 of Gekko gecko Sensilla Scale type

BU

BB

BL

None

Total

Paralamellar Paraphalangeal Phalangeal Toe base Total

37 37 26 100 200

0 22 0 1 23

22 36 62 52 172

7 0 0 56 63

66 95 88 209 45 8

NOTE: BU, bristled unbranched; BB, bristled branched; BL, bristleless.

by a moderately deep groove (Fig. 2). These bristleless sensilla are found only on glabrous scales. The average diameter of this type of sensillum is 14.9 pm. Bristled unbranched sensilla are located in depressions that are at least deep enough to make the upper surface of the papilla flush with the surrounding scale, although the depression is often much deeper. This is especially the case in paralamellar scales (Fig. 3) and some of the phalangeal scales (Fig. 4). Papillae of this type of sensillum average 16.6 pm in diameter. Ornamentation similar to that found on the spinulate scales that possess these sensilla covers most of the papilla (Fig. 5), although the area within a 1.0-pm radius of the bristle-bearing center is devoid of spinulate microornamentation. At a radius of about 5 pm, there is a sharp delineation between a peripheral zone of dense microornamentation and a central zone of sparser microornamentatioh (Fig. 5). Bristled branched sensillar papillae are similar in most respects (size, ornamentation) to those of bristled unbranched sensilla (Figs. 6, 7), although they are never as deeply recessed as the sensilla of the paralamellar scales (Fig. 3). Of these sensillar bristles, 75% were bifid whereas 25% were found to have three primary branches. Some of these have secondary bifur-

cations (Fig. 7), although some do not (Fig. 6). Primary branches are of variable length, the branch base to tip length ranging from 10 to 25 pm. Ornamentation of the bristles is variable. Figure 6 shows one bristle that is almost naked and two (each on separate sensilla) with sparse ornamentation. In contrast, the bristle in Fig. 7 shows dense ornamentation up to the bifurcation of the secondary branches. Secondary branches tend to be devoid of adornment. Rarer scale organ types were found in two instances. These may be anomalous structures or may represent previously undescribed sensillar types occurring at low density. A single organ with two bristles (one branched the other not) arising from one papilla was found in one animal. The second instance involved a papilla with two circles of low-density ornamentation, each of which harboured two unbranched bristles (Fig. 8). In both cases the other sensilla of the scale on which these receptors occurred were bristled and unbranched.

Distribution and orientation In the specimens examined, each scale (except for those that bore the rarer scale organs) possessed only one type of sensillum (Fig. 2). As generally reported for squamates, scale organs are present chiefly at the free margins of scales (Figs. 2, 3, 4), although in some instances the bristleless sensilla were set back some distance from this edge (Fig. 2). Typically, scales that were located midsagitally on the digit had sensilla only on the distal margin (Fig. 4), whereas scales located parasagittally had sensilla located distolaterad (Figs. 2, 3, 4). Paralamellar scales, which have vertically disposed free margins, had sensilla only on their anteroventral and ventral margins (Figs. 3, 4, 9). Although there were similarities, the distributions of the three types of sensillum were not absolutely identical between the animals sampled. Figure 2 shows a series of bristleless sensilla that, in two animals, occurred on scales over the entire toe base as well as on the phalangeal scales to the base of the


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FIG.3. Dorsal view of paralamellar ( A )and lateral paraphalangeal ( A ) scales, showing the orientation and degree of recessing of the bristled unbranched sensilla (small arrows). Note the distal and lateral placement of these sensilla on the lateralmost row of paraphalangeal scales, and their anterolateral placement on the next most medial row (see the direction of the arrows). These sensilla may be canted within their recesses. The bristled unbranched sensilla of the paralamellar scales (large arrow) are more deeply recessed than those of the paraphalangeal scales. The close proximity of the bristled unbranched sensilla and their bristles to neighbouring scales is evident in both the paralamellar and paraphalangeal placements. Scale bar = 200 pm.

FIG. 4. Distolateral view of digit I11 (see Fig. 1 for clarification of the perspective). m, phalangeal scale; A , paraphalangeal scale; paralamellar scale. Note the orientation of the sensilla on the various scales. Scale bar = 400 pm.

A,

claw. Towards the base of the toe pad the paralamellar scales (of two animals) also showed bristleless sensilla (Fig. 2). No bristleless sensilla were found on the toe of a third animal.

Most paralamellar scales bore bristled unbranched sensilla, and these were always found on the ventral aspect of the anterodistal margin and on the ventral aspect. Bristled unbranched


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FIG. 5. Bristled unbranched sensillum from a phalangeal scale. Note that the scale surface is ornamented in a fashion similar to that of the papilla. Compare with Fig. 2. The particulate matter lying on the scale surface is detritus. Scale bar = 5 pm.

FIG. 6. Dorsal view of three bristled branched sensilla from a medial paraphalangeal scale. Only primary branches occur in these examples. The arrows indicate the scale border. Scale bar = 15 pm.

sensilla were also found on the phalangeal and paraphalangeal scales. On these, the sensilla were seated in'recesses that were oriented towards the distal and distolateral aspects of the digit (Figs. 3, 4). Within these recesses of the paraphalangeal scales, however, the papillae are canted with respect to the main axis of the recess (Fig. 3), so that the papilla and the base of the bristle are oriented laterally in the case of the distally

positioned recesses and distally in the laterally positioned recesses. The bristled unbranched sensilla were found predominantly on the medial paraphalangeal scales, although they were also found sporadically on some lateral paraphalangeal scales. Bristled branched sensilla were always located just proximal to the margin of the scale on the dorsal surface, never in deep


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FIG. 7 . A bristled branched sensillum with both primary and secondary branches. A nerve path aperture is evident on the sensillum (arrow). Scale bar = 10 pm.

FIG.8. Anomalous (?) sensillum from a paraphalangeal scale. All other sensilla on the scale were of the bristled unbranched type. The nerve paths (arrows) can be seen in both areas of low-density ornamentation. Scale bar = 5 pm.

recesses. A summary of the distribution of b e sensilla is presented in Fig. 10.

Discussion The presence of both bristleless and bristle-bearing sensilla on the digits of the tokay gecko confirms the presence of the

former type of sensillum in geckos. It also raises a number of phylogenetic questions. Williams (1988) regarded the lenticular scale type as primitive for iguanians, and Scortecci (1941) considered them to be so for agamids in particular, with bristled organs occurring as a derived type. If this is the case, the very similar scale organs of gekkonids and iguanians must have


CAN. J . ZOOL. VOL. 71. 1993

FIG. 9. Ventral view of two successive paralamellar scales (a)and the associated lateral extremity of a seta-bearing scansor (s). Note the two zones of clustering of bristled unbranched sensilla on the paralamellar scales (1, proximal and ventral; 2, distal and anterior) and the sensilla-free region between them (brace), and also the bristled unbranched sensilla in the hinge region anterior to the lateral extremity of the setal field of the scansor (arrow). Scale bar = 100 pm.

Bristleless

Bristled unbranched

Bristled branched

FIG. 10. Relative distributions of sensillar types on the dorsal digital scales of Gekko gecko. The stippled scales represent those upon which the specific type of sensillum is most prominently found. The stippling is not meant to represent universality of presence of the particular type of sensillum on that particular scale type, or to convey information about precise positioning (for the latter see the text and Figs. 2-4).

arisen convergently, with autarchoglossans retaining the primitive squamate condition (lenticular) or exhibiting a loss of bristled organs and spinulate scale microarchitecture relative to the scleroglossan ancestor. Schmidt (1920) and Ananjeva et al. (1991) suggested that these structures in gekkonids and

agamids may be parallel developments rather than synapomorphies. The presence of bristled cutaneous sense organs is apparently primitive for both the iguanian and gekkotan clades, but these are absent in the autarchoglossan lizards, which lack a spinulate scale microarchitecture (Perret and Wuest 1982,

LAUFF ET AL.

TABLE2. Statistics pertaining to the diameters of the three types o f sensillar papillae of Gekko gecko discussed in this study Sensilla type

n


Min. (pm) Max. (pm) Mean SE

14 15.5 23.4 19.1 0.59

12 14.8 17.8 15.9 0.30

14 14.3 19.5 17.3 0.54

Analysis of variance

F ratio

df

P

T statistics from Tukey honestly significant multiple comparisons BU

BB

NOTE:BU, bristled unbranched; BB, bristled branched; BL, bristleless. *, p < 0.05.

1983; Peterson and Bezy 1985; Irish et al. 1988). As these structures are lacking in Sphenodon (Peterson 1984), it is equally parsimonious to explain their derivation either as primitive for squamates with a reduction in autarchoglossans, or as having evolved twice, once in iguanians and a second time in gekkotans. Structures perhaps analogous to bristled sensory organs do occur in Shinisaurus, however (Harvey 1993). Structure The dimensions of the setal structures and scale organs of geckos have been summarized previously (Hiller 197 1 ; Bauer and Russell 1988). The bristles on the sensilla of Gekko gecko, at 60 pm long, and scale organ diameters of up to 27 pm (Hiller 1971), are among the largest known for geckos (Schmidt 1920; Hiller 1971; Bauer and Russell 1988). Digital bristleless sensilla were found to be intermediate in diameter (mean 17.3 pm, SE 0.54; n = 14) between bristled unbranched sensilla (mean 19.1 pm, SE 0.59; n = 14) and bristled branched sensilla (mean 15.9 pm, SE 0.30; n = 12) (Table 2). Bristled branched sensilla are not significantly different in diameter from bristleless sensilla, but there are significant differences when bristled unbranched and bristled branched sensilla are compared with bristled unbranched and bristleless sensilla (Table 2). Ornamentation was lacking on all bristleless sensilla and present on all bristled sensilla. This characteristic extended beyond the papilla to the scales themselves. Bauer and Russell (1988) expressed reservations with respect to the glabrous nature of scales possessing bristleless sensilla in Nephrurus. In the present study, however, the consistency with which unadorned scales with bristleless sensilla bordered scales with spinulate microornamentation and bristled sensilla suggests that the glabrous morphology is not artifactual. Differences are also present at the histological level.

2469

Bristled unbranched sensilla contain not only more central cells than the bristleless form, but also have an annular ring of sustentacular cells. Only one cell was ever confirmed in any mature bristleless sensillum. The relative degree of papillar recessing is noteworthy. Paralamellar bristled unbranched sensilla are very deeply recessed and have long, protruding bristles (50 pm exposed length) (Figs. 3, 9). At the other extreme, bristled branched sensilla are seldom recessed, the top of the papilla being reasonably flush with the scale surface proper (Fig. 7). Exposed papillae would be able to pick up a wider range of stimuli: both the bristle and the receptive surface may be able to receive stimuli. In contrast, it is probable that in deeply recessed papillae, only the bristle is exposed to stimuli. This may imply, therefore, that sensilla which bear long bristles and have a recessed papilla (everything else being equal) do not receive the same range of mechanical stimuli as those that are less recessed. Potential function in locomotion Renous and Gasc (1989) suggested that in lizards, microstructures, both across the surface of individual scales and between them, exhibit patterns of spatial heterogeneity that reflect the polarities of environmental gradients of significance to the animal. Given that not all sensilla on the dorsal digital surface of the tokay gecko are identical in either position or form, it is possible to extend this concept to the consideration of sensilla and to try to correlate form and position with potential functional specialization. Bristles act as force transducers (Hiller 1978; Bauer and Russell 1988). In sequence with the receptive surface of the papilla, they deform and depolarize underlying nerves, giving rise to a graded response to stimuli of different intensities (Hiller 1978). The topographic disposition of bristle-bearing sensilla (Figs. 4, 10) suggests a proprioceptive role for these structures. The functional advantage of a branched bristle may be to expand the potential receptive field of the organ. Bristled unbranched sensilla are always more deeply recessed than those of the bristled branched type, and in some cases, such as on the paralamellar scales, the former are very deeply recessed. Bristled unbranched sensilla are found on the paralamellar, the phalangeal, and the more lateral of the paraphalangeal scales, as well as on the toe base, while the bristled branched sensilla are largely restricted to the more medial of the paraphalangeal scales (Fig. 10). When the digits hyperextend, the phalanges bend the central axis of the digit dorsally (Fig. 1 l ) , and at the same time the dorsal interossei muscles, by way of sheets of connective tissue spanning from their dorsal surface to the margins of the pad (Russell 1975), result in medial curling of the edges of the pad (Fig. 12). The lateral and medial paraphalangeal scales are differentially affected by these actions, the medial ones suffering the greatest distortion, owing to their position close to the phalangeal axis (Fig. 4) and near the base of the medial curling. If the sensilla monitor scale-to-scale contact or associated distortions during such activities, then differentially positioned and constructed sensilla may be of significance in registering different degrees of distortion of the dorsal pad surface. On the dorsum of the digits, bristled unbranched sensilla are located on phalangeal and paraphalangeal scales (Fig. 10) and in these positions are moderately recessed (Figs. 3, 4). Such sensilla appear to be oriented in directions that would max-


CAN. J. ZOOL.VOL. 71. 1993

scansors

FIG. 11. Outline diagram of a sagittal section of the fourth digit of the pes of the tokay gecko, fixed in a hyperextended position. The outlines of the phalanges (I -V) are indicated for reference. Note the distortion and close proximity of the mid-dorsal scales. The position of the bristled unbranched sensilla is indicated by arrowheads (compare with Figs. 1 and 4 for orientation). The curved arrow indicates the direction of hyperextension.

phalangeal scales

penultimate phalanx (phalanx IV) long flexor tendon

lateral paraphalangeal scales

venous sinus /

phalangeal scales

scansors

FIG. 12. Outline diagram of a cross section of the fourth digit of the tokay gecko in the region of the penultimate phalanx. The location of the paralamellar, paraphalangeal, and phalangeal scales is indicated, and curved arrows indicate the direction of lateral to medial curling of the pad during hyperextension. The position of the venous sinus is also marked for reference.

imize the possibility of being impinged upon by adjacent scales during the process of hyperextension. Thus, the laterally positioned sensilla of the paraphalangeal scale row immediately adjacent to the paralamellar scales (Fig. 3) would be contacted by the dorsomedial edges of the adjacent paralamellar scales

as the pad edges curl medially (Fig. 12); the distally situated sensilla are positioned in such a way as to be impinged upon by the next most distal paraphalangeal scale. It is noteworthy that on the second most lateral row of paraphalangeal scales the sensilla are positioned only in areas where the proximal

247 1


LAUFF ET AL.

end of the abutting neighbouring scale will make contact upon hyperextension (Fig. 3). Thus, there is regional differentiation in the positioning of sensilla on the paralamellar scales, depending upon the location of the latter. This differential positioning is also evident in Fig. 4. On the phalangeal scales (Fig. 4) the positioning of the bristled unbranched sensilla is essentially restricted to the distal aspects of the scales. In this region of the digit, hyperextension will result in proximal curling only (Fig. 11). Unlike the bristled unbranched sensilla on the dorsal scales of the pad-bearing region of the digit, those borne on the paralamellar scales are positioned on the anteroventral and ventral edges of the scales and are much more deeply recessed (Figs. 3, 4, 9). Such sensilla expose only the bristles to their surroundings and probably serve to register contact of paralamellar scales with each other and with the substrate during adhesive contact of the digit. Hiller (1976) proposed that paralamellar sensilla act primarily to provide positional and substrate information (based upon examinations of Tarentola). Russell (198 1b) discussed the sequence in which scansors are brought into contact with the substrate and how the digital sinus system is pressurized during this process. As the digit is laid down, its underside conforms to the substrate. This results in adjacent paralamellar scales being brought into contact with each other and their ventral surfaces with the substrate. These interactions, in turn, may result in deflection of the bristles of the sensilla, permitting contact to be registered. Figure 9 indicates that each paralamellar scale has two areas of concentration of sensilla. The proximalmost cluster is borne on the ventral surface of the scale immediately lateral to the setal field of the scansor associated with that scale. These sensilla are presumably associated with registering contact of the scansor and its associated paralamellar scale with the substratum. Such sensilla are aligned with those borne on the anterior hinge region of the lateral aspect of the scansor itself. The distalmost cluster of sensilla is found on the anteroventral aspect of the free edge of the scale (Fig. 9). Such sensilla are positioned to register contact with the next most distal paralamellar scale. Such contact would occur during digital plantarflexion and substrate contact, and would be broken during hyperextension. The intervening region of each paralamellar scale bears no sensilla (Fig. 9). Bristleless sensilla are not recessed, but are flush with the scale surface or raised slightly above it. They are the only type found only on glabrous scales, and occur on the toe base and the phalangeal scales as well as on paralamellar scales situated closest to the toe base (Fig. 10). Figure 2 indicates that such sensilla may be situated at scale edges, but that this is not invariably so. Because they lack bristles, only direct contact between the papilla and an external source can result in the discharge of a nervous impulse. The location of these sensilla in relation to other scales suggests that they may not monitor scale-to-scale contact or proximity, but may register other stimuli. Russell and Bauer (1987) suggested that the bristleless sensilla of Nephrurus (diameter 10 pm) are better suited to areas that make direct contact with the substrate. This is probably not the case with the dorsal digital scqles of Gekko, but other direct contact from the environment, iuch as wandering ectoparasites in search of suitable attachment sites, could be significant. Figure 2 indicates that the bristleless sensilla may be aligned along the margins of vulnerable hinge regions where scales do not fully imbricate. It is apparent that the digits of tokay geckos are very sensitive and will be shaken

vigorously if the slightest contact with the dorsum of a digit is induced while the animal is at rest (personal observation). The bristleless sensilla may be the agencies through which such contact is monitored. Implications The foregoing points suggest a close correlation between the structure and placement of the sensilla of the dorsal digital scales of the tokay gecko and the processes of digital hyperextension and plantarflexion during locomotion. The mechanoreceptive properties of the digital sensilla (Diiring and Miller 1979; Hiller 1978) can thus be placed in the context of their positioning on the dorsal digital scales. Russell (1975) demonstrated that even on a smooth vertical surface, the limb cycle of a rapidly moving tokay gecko can be completed in less than 0.2 s. Effective proprioception of the adhesive apparatus and its adnexae during the locomotor cycle is apparently significant. Recognition of this proprioceptive complex adds one more component to the suite of morphological modifications (Russell 1975, 1981b, 1986) that characterizes the adhesive mechanism of Gekko gecko.

Acknowledgements We thank Dr. J.N.A. Lott for access to SEM equipment and preparation facilities. This work was supported by an operating grant from the Natural Sciences and Engineering Research Council of Canada to A.P. Russell, and this financial assistance is gratefully acknowledged. Laboratory assistance in various forms was rendered by Mlle. C. Bander, L. Barber, D. Flanigan, D. Milgheebar-Kidd, and K. Shultes. Ananjeva, N.B., Dilmuchamedov, M.E., and Matveyeva, T.N. 1986. The cutaneous receptors of the iguanomorphan lizards. [In Russian.] Proc. Zool. Inst. U.S.S.R. Acad. Sci. 157: 14-33. Ananjeva, N .B., Dilmuchamedov, M.E., and Matveyeva, T.N. 1991. The skin sense organs of some iguanian lizards. J. Herpetol. 25: 186-199. Audy, J.R. 1953. Strolling on the ceiling. Malays. Nat. J. 7: 182 190. Bauer, A.M., and Russell, A.P. 1988. Morphology of gekkonid cutaneous sensilla, with comments on function and phylogeny in the Carphodactylini (Reptilia: Gekkonidae). Can. J. Zool. 66: 1583- 1588. Cartier, 0. 1872. Studien uber den feineren Bau der Epidermis bei den Geckotiden. Verh. Wurzburg. Phys.-Med. Ges. 3: 281 - 301. Cohn, L. 1914. Die Hautsinnesorgane von Agama colonorum. Zool. Anz. 44: 145-155. During, M. von, and Miller, M.R. 1979. Sensory nerve endings of the skin and deeper structures. In Biology of the Reptilia. Vol. 9. Edited by C. Gans, G. Northcutt, and P. Ulinski. Academic Press, New York. pp. 407-439. Gourvest, N. 1960. Morphologie des doigts et locomotion chez le gecko ( Tarentola mauritanica). Bull. Soc . Zoo1. Fr . 84( 1959): 531 -540. Harvey, M.B. 1993. Microstructure, ontogeny , and evolution of scale surfaces in xenosaurid lizards. J. Morphol. 216: 161- 177. Hiller, U. 1968. Untersuchungen zum Feinbau und zur Funktion der Haftborsten von Reptilien. Z. Morphol. Tiere, 62: 307-362. Hiller, U. 1971. Form und Funktion der Hautsinnesorgane bei Gekkoniden. I. Licht- und rasterelektronenmikroskopische Untersuchungen. Forma Functio, 4: 240 -253. Hiller, U. 1976. Elektronenmikroskopische Untersuchungen zur funktionellen Morphologie der borstenfiihrenden Hautsinnesorgane bei Tarentola mauritanica L. (Reptilia, Gekkonidae). Zoomorphologie, 84: 21 1-221.


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