© 2002 by The Society for Integrative and Comparative Biology
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Integrative Functional Morphology of the Gekkotan Adhesive System (Reptilia: Gekkota)1
1 Department of Biological Sciences, University of Calgary, 2500 University Drive N.W., Calgary, Alberta, Canada, T2N 1N4
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SYNOPSIS |
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Climbing assisted by adhesive subdigital pads in gekkotan lizards has been the subject of intrigue and study for centuries. Many hypotheses have been advanced to explain the mechanism of adhesion, and recently this phenomenon has been investigated at the level of individual setae. The ability to isolate, manipulate and record adhesive forces from individual setae has provided new insights, not only into the mechanism of attachment, but also into the physical orientation of these structures necessary to establish attachment, maximize adhesive force, and effect subsequent release. This, in turn, has enabled a reassessment of the overall morphology and mode of operation of the adhesive system. Digital hyperextension has often been noted as a behavioral characteristic associated with the deployment of the gekkotan adhesive system—this is now understandable in the context of setal attachment and release kinematics, and in the context of the evolution of this pattern of digital movement from the primitive pattern of saurian digital kinematics. The perpendicular and parallel preloads associated with setal attachment are now reconcilable with other morphological aspects of the gekkotan adhesive system—the lateral digital tendon complex and the vascular sinus network, respectively. Future investigations of the integrated adhesive system will help to further elucidate the interdependence of its structural and functional components.
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INTRODUCTION |
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The presence of subdigital pads in geckos has been recognized in the scientific literature as the subject matter of functional speculation for at least 200 years (La Cépède in Buffon, 1802
). Anatomical observation of such structures, and experimental investigation into their function, dates to the latter part of the 19th century (Simmermacher, 1884; Tornier, 1899) and has been the subject of investigation more or less continuously ever since. Much of the published work has focussed on the structure and function of the setae, the epidermal outgrowths that are the organism-environment interface of the subdigital pads, either by attention being placed on these structures alone, or by attempting to integrate an understanding of them with overall digital and pedal structure.
Once the adhesive role of the pads and, by inference, the setae had been established (Simmermacher, 1884; Tornier, 1899), efforts to elucidate the mechanism by which adhesion is achieved passed through a number of conjectural and refutational cycles that have brought us to our current level of understanding. These approaches have been paralleled by series of observations that have addressed the functional integrity of the various anatomical components that constitute the adhesive system, and behavioral observations that document how the adhesive system is operated during the locomotor cycle. Recent observations conducted on the clinging mechanics of individual setae (Autumn et al., 2000) and the particular physical parameters that govern attachment, adhesive force maximization, and release, permit a fresh overview of how adhesive forces at the molecular level can be placed into a whole organism context. In this regard, setal structure and orientation, pedal structure and function, and cyclical behavioural patterns during locomotion are herein amalgamated to provide the framework for fuller understanding of the mechanism of adhesion and its potential evolutionary origins. Future directions of research investigation are proposed that will assist in the testing of newly emergent hypotheses.
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BACKGROUND TO SETA-BASED ADHESION |
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The setae encountered on the ventral surface of gekkonid (and anoline polychrotid and prasinohaemid scincid) subdigital adhesive pads (Maderson, 1970
; Williams and Peterson, 1982) are hypertrophied elaborations of the outer epidermal generation (the Oberhaütchen layer—Maderson, 1970). In most lizards the Oberhaütchen layer bears minute lamellae, but in gekkonids (Lange, 1931; Stewart and Daniel, 1972) and anoline polychrotids (Peterson, 1983) this layer is sculpted into spinules of approximately 1.5 µm in height (Maderson, 1970). There is a range of variation of this spinulate Oberhaütchen expressed across the body surface (Stewart and Daniel, 1972), and on the palmar and plantar surfaces of the feet there is an increase in height to about 2.5 µm in Gekko gecko (Stewart and Daniel, 1972). A gradation towards fully expressed subdigital setae has been recorded and documented for geckos (Russell, 1976) and anoles (Peterson, 1983), and an evolutionary transition from a general phenomenon of spinules assisting in the mechanics of skin shedding (Maderson, 1970) to these outgrowths being exapted for adhesive purposes has been postulated (Steward and Daniel, 1972).
Setal dimensions of geckos and anoles vary considerably across taxa (Maderson, 1970; Schleich and Kästle, 1986), but this variation in size is not simply an allometric effect, as there is no demonstrable correlation between snout-vent length and seta length (some small species have setae that are considerably longer, absolutely, than those of certain large-bodied forms). Similarly, setae may be simple stalks with single spatulate tips, or they may be sparsely or profusely branched (Ruibal and Ernst, 1965; Russell, 1976; Stork, 1983; Schleich and Kästle, 1986). The width of the setal tips also varies between taxa (Ruibal and Ernst, 1965; Russell, 1975, 1976).
The occurrence of setae in gekkonids (where their elaboration has been the result of several independent evolutionary pathways—Russell, 1976) and anoline polychrotids (and also, to a lesser known extent in prasinohaemid scincids) has led to the conclusion that these structures are reflective of patterns of parallelism (Russell, 1979) and convergence (Russell, 1976) that suggest that, in their mode of deployment, certain basic constraints have to be accounted for (Russell, 1979). Until recently, however, it was not understood how individual setae operated, and thus it was not possible to integrate setal function with whole foot structure and function.
This lack of integration has led to the proposal of a number of mechanisms of adhesion that have not been fully reconcilable with the operation of whole foot mechanics. Digital hyperextension has long been associated with the deployment of adhesive pads in geckos (for example, Dellit, 1934), and has been cited as a factor placing constraints on locomotor possibilities (Zaaf et al., 1999), but the association of digital hyperextension with setal adhesion has never been satisfactorily explained. More recent observations (Autumn et al., 2000) and syntheses (see below) of previous observations now permit new levels of integration and promise profitable new lines of investigation for the future.
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THEORIES OF SETA-BASED ADHESION |
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Due to the immediate associations that can be made between the presence of subdigital setae and the phenomenon of adhesion, much effort has been devoted to the elucidation of the means by which the adhesive bond is created. This has led, by successive approximations, to the hypotheses that are currently favoured (Autumn et al., 2000
; see below). Such investigations have also largely been laboratory based and have shed little light on the biological roles (Bock and von Wahlert, 1965) that these structures contribute to in nature (Maderson, 1970). Thus, elucidation of how setae work (see below) and the clinging ability that they endow their possessors with (Irschick et al., 1996) have, until recently, not been able to shed a great deal of light upon how the adhesive mechanism of these lizards may have arisen in the first place.
Early attempts at explaining seta-based adhesion advocated the establishment of vacuua (Simmermacher, 1884; Tornier, 1899; Gadow, 1901; Kunitzky, 1903; Tandler, 1903). Weitlaner (1902) and Dellit (1934) conducted experiments that demonstrated that vacuua alone could not account for the adhesive grip. Schmidt (1905) suggested electrical forces as the main agent of adhesion, but these were also dismissed by Dellit (1934) on the basis of experimental observations. This dismissal seems to have been premature, however, and Hiller (1968) pointed out that Dellit's (1934) experimental procedures mitigated against the testing of such ideas. The postulation that setae operated primarily by way of frictional interaction or interlocking (Riskin and Fenton, 2001) with the locomotor substratum was advanced by Hora (1923) and elaborated upon by Dellit (1934, 1949), Mahendra (1941), Altevogt (1954), and Nachtigall (1974). Maderson (1964) rejected this hypothesis on the basis that the structure of setae was incompatible with the mechanics required for frictional load-bearing.
With a fuller understanding of setal structure and form, particularly via scanning electron microscopical observations (Ruibal and Ernst, 1965; Hiller, 1968, 1971, 1972; Gennaro, 1969), and studies of their modes of growth and replacement (Maderson, 1964; Lillywhite and Maderson, 1968) came concepts of adhesion more compatible with setal structure. Such revelations led Hiller (1969) to devise experiments to test the clinging ability of geckos when exposed to locomotor surfaces of differing free surface energy. He found that adhesive force increased with increasing free surface energy and thus advocated intermolecular bonding as the main adhesive agent. He, and Cartmill (1985), explained this as being due to quantum electrodynamic phenomena that result from the coupling of electron motions in the electron "clouds" surrounding adjacent molecules. The strength of such forces depends upon the geometry of the apposed surfaces and the physical properties of their constituent molecules.
Such observations led to a general acceptance of these intermolecular forces as the main agency of adhesion, but without an understanding of the mode of operation of individual setae, the relationship of this pattern of bonding to whole foot architecture and to locomotor kinematics could not be further elucidated. Such reconciliation took a major step forward with the publication of Autumn et al.'s (2000) findings on the adhesive forces produced by, and the physical circumstances associated with attachment and release, of a single seta. Although these observations did not elucidate mechanisms of attachment of, or orientation of, individual setal spatulae, they did provide an entirely new perspective on the operation of setae. These observations were also of major importance because they addressed the mechanism of detachment of the setae as well as the establishment of the adhesive bond.
In brief (Fig. 1) Autumn et al. (2000) found that setal orientation and loading are both crucial to the adhesive force produced by a seta. They demonstrated that a perpendicular preload was necessary to effectively engage a seta with the surface, a parallel preload, with a sliding motion of about 5 µm, was necessary to induce maximal adhesive force, and an angle between the setal shaft and the locomotor substrate of 30.6° ± 1.8° was the trigger to setal release. Autumn et al. (2000) carried out experiments to determine the nature of the adhesive forces and were able to again reject hypotheses based upon vacuua and friction (although they did allow that microinterlocking may function as a secondary mechanism). They further refuted simple electrostatic attraction, as setae are still able to adhere in ionized air, and also rejected glue-based adhesion because of an absence of secretions. Adsorbed water as an agency of adhesion has also subsequently been ruled out (Autumn et al., 2002).
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) in relation to the substratum decreases below the critical angle (see text for details). C. Parallel preload results in sliding of the setal tip along the substratum for about 5 µm, whereby the seta obtains its maximal adhesive force (at D). Between D and E (which can range from milliseconds to hours) the maximal adhesive force is maintained. At E the setae are raised from the surface by digital roll off or hyperextension (see text), accompanied by a relaxation and release of the parallel and perpendicular preloads. Adapted from Autumn et al. (2000).The intramolecular forces initially advocated by Hiller (1969)
were corroborated, and the van der Waal's force of an individual setal spatula of a tokay gecko was calculated to be about 0.4 µN. Given the millions of setae available to an individual, when summed for all four feet (Schmidt, 1905; Maderson, 1966; Bauer and Good, 1986), the adhesive force estimates made on tokay geckos (Autumn et al., 2000) fell within the range of what can be accounted for by van der Waal's force bonding. This dry adhesion mechanism is geometry-dependent and is similar, in principle, to that encountered in the van der Waal's-based dry capture threads of araneomorph spiders (Hawthorn and Opell, 2002). |
GEKKONID PEDAL STRUCTURE IN RELATION TO THE ADHESIVE PROCESS |
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Russell (1976
, 1979) has documented the extensive patterns of parallelism within, and convergence between, lineages of geckos and anoline polychrotids in terms of adhesive pad structure. Morphological patterns of secondary symmetry of the pes (Russell et al., 1997) and anatomical systems devoted to the control and application of the setae (Russell, 1976) have arisen independently on numerous occasions (McCracken et al., 1999) within the Gekkota, and have been repeated, with variations, by the Polychrotidae (the anoles). Secondary symmetry of the gekkotan pes (the manus is primitively symmetrical) results in radiation of the digits about an arc of over 180° and, in turn, results in parallel loading of some of the digits that is more or less aligned with the vertical gravitational force acting on the body when moving on a vertical surface, regardless of body orientation (Russell et al., 1997). This is of major importance in terms of the application of the parallel preload on the setae (Autumn et al., 2000) that is necessary to induce maximal loading. Beyond the overall geometry of the foot there are aspects of form and function that can be deemed, in combination, necessary and sufficient for an operational adhesive system that employs intermolecular bonding as its main means of attachment. These are briefly considered, in turn, and then placed into the context of the reconciliation of morphology with the establishment and release of the intermolecular bonds.
Applying and releasing the grip
Studies of gekkonid locomotion have emphasized the peculiar pattern of digital engagement with and disengagement from the locomotor substratum, by way of digital hyperextension (Russell, 1975; Zaaf et al., 1999). In this pattern the digits are unfurled from the substratum from their distal end proximally as the grip is relinquished, and rolled down onto the substratum from proximal to distal during foot placement (Fig. 2A). In actuality it is only the distal part of the digit that undergoes this pattern of hyperextension; that part of the digit that contains the arcuate, elongate penultimate phalanx and the short ungual phalanx (Fig. 2A, digit fixed with the tip hyperextended; Fig. 3). Hyperextension is powered by hypertrophied digital muscles (Fig. 2A) that, in some taxa (Russell, 1976) extend along the dorsal aspect of the digit as far as the penultimate or ungual phalanx, and in others connect with these areas by way of elongate tendons.
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Peculiarly shaped, depressed and widened phalanges in the intermediate region of each digit (Fig. 2B) have been associated with the hyperextension mechanism and process (Russell, 1975
), but actually appear to be associated with the application and release of the intermediate region of the digit, which may or may not carry a portion of the subdigital pad beneath it (Russell, 1976, 1979). High speed videography of the pes of Gekko gecko (Fig. 3) reveals that the distal portions of the digits actively hyperextend and release (in a given sequence) and then the intermediate region of each digit rolls off the substratum, from proximal to distal, in the primitive lizard fashion (Brinkman, 1980, 1981; Rewcastle, 1980, 1981, 1983). Thus, if the subdigital pad is extensive and occupies the distal and intermediate regions of the digit, it is applied to and released from the locomotor substrate in the primitive pattern proximally, and in the modified hyperextensile pattern distally.
The subdigital adhesive pad itself is made up of a series of overlapping plates (Russell, 1975) termed scansors (Russell, 1981b) (Fig. 2A). These consist not only of a fold of the integument that carries the setae on its exposed outer surface, but also a more proximal expanded region that may contain expanded branches of the blood vascular system, accumulations of adipose tissue (Fig. 2A) or some similar device that can act as a hydrostatic cushion (Russell, 1981a, b). The scansors are served by branches of a lateral digital tendon system (Fig. 2C) (Russell, 1986) that merge directly with the stratum compactum of the dermis of the scansors (there is no stratum laxum of the dermis in this region). Scansors may, therefore, be influenced individually in the attachment and release process, resulting in fields of setae that can be sequentially raised from the substratum during release (including release via hyperextension), and placed into contact as the digits unfurl. During placement the lateral digital tendons, through a complex and stratified array of connective tissue sheets and muscles that make up the plantar aponeurosis (Russell, 1993), pull the scansors into close contact with the locomotor substratum. The lateral digital tendons apply the tensile loading induced in the setae directly to the skeleton via the dermis, themselves, and the plantar aponeurosis.
Making maximal surface contact
As mentioned above, each scansor may include (depending upon taxon) an expanded proximal region that is pervaded by branches of the digital sinus system (Russell, 1981a, b) or is filled with adipose tissue (Bauer and Russell, 1990). Such expansions, when the foot is adpressed to the locomotor substratum, align with each other to create an essentially continuous cushion that overlies the fields of setae (Fig. 2D, F). This cushion has been hypothesized to enable the setal fields to conform with irregularities in the locomotor substratum (Russell, 1981b) and thus increase the potential for setal tip contact with the surface. In many taxa with greatly expanded pads, control of the pad extremities and enhancement of intimate contact within the substratum is further assisted by the presence of paraphalangeal elements (Russell and Bauer, 1988; Mohammed, 1991) (Fig. 2E). These paraphalanges (Wellborn, 1933) are cartilaginous and in some taxa are intimately associated with the lateral digital tendons and/or peripheral parts of the digital vascular sinus or adipose tissue system.
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RECONCILIATION OF LOCOMOTION AND MORPHOLOGY WITH SETAL ADHESION |
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TOP
SYNOPSISINTRODUCTIONBACKGROUND TO SETA-BASED...THEORIES OF SETA-BASED ADHESIONGEKKONID PEDAL STRUCTURE IN... RECONCILIATION OF LOCOMOTION AND... QUESTIONS FOR FUTURE...CONCLUDING REMARKSReferences |
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Autumn et al. (2000)
indicated that the adhesive bond of each seta with the substratum was maximized when the perpendicular and parallel preloads were of the appropriate magnitude and direction with respect to the setal shaft, and when the angle of the setal shaft was depressed below 30° with reference to the substratum. How might this be integrated into what is known of the pattern of digital movement through the locomotor cycle and the morphological and functional characteristics of digital anatomy?
In order to address this, the integration of digital structure and the patterns of digital movement throughout the stance phase of the locomotor cycle must be reconciled with setal placement, orientation and loading (Fig. 4). It should be noted that at present virtually all of the in vivo and in vitro functional interpretations of setal adhesion have been made on a single species (Gekko gecko) and that the wide variety of gekkotan setal form and digital structure (Russell, 1976, 1979) may reveal different outcomes with regard to specifics, although it is likely that the general concepts will be corroborated.
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The setae are borne on the epidermis which makes intimate and tight interdigitating contact with the stratum compactum of the dermis of the ventral surface of the scansor (Fig. 4). Each seta consists of a flexible shaft, the angle of which can be deflected with respect to the locomotor substratum and the ventral surface of the scansor as contact is made with the substratum. If contact in a given region of a scansor is effective, the angle that the seta makes with the substratum will be depressed below the critical release angle of 30.6° ± 1.8°. When this happens, adhesion can begin to occur (Fig. 1).
Autumn et al. (2000) also found that a perpendicular preload (Fig. 1) applied to the setal tips upon contact was probably necessary to engage adhesion, but that if this preload is too great the setal shaft would buckle. The connection that can be made here with anatomical design is that the cushioning effect provided by the branches of the blood sinus system (Russell, 1981b) may not only enhance the pattern of contact by taking up surface irregularities, but may also be able to provide an appropriate perpendicular preload (Fig. 4). The compliance provided by a vascular, or adipose, cushioning system may be related to provision of a perpendicular preload that does not exceed the tolerance levels of the setal shaft.
Once the perpendicular preload has been applied and the critical angle has been reduced sufficiently to enable setal attachment (Fig. 1), the magnitude of the attachment force is increased to peak value by the application of a parallel preload (Fig. 1). In the context of entire digital and pedal structure, the lateral digital tendons (Fig. 4) are situated in such a way as to be able to apply an active parallel preload at the appropriate time, although passive parallel preloading via gravitational force may be effective in suitably aligned digits (see above). Contraction of crural and pedal flexor muscles operating through the plantar aponeurotic complex (Russell, 1993) will apply tensile loading to the lateral digital tendons, and this loading will be directly transmitted to the stratum compactum of the dermis of the ventral surface of the scansors, and thence directly to the epidermis and setae. Such a linkage system is likely related directly to the preload mechanism and also provides resistance to the tensile loading placed upon the setae.
Observations of locomotion (Fig. 3) reveal that only the distalmost scansors are subjected to active (muscularly-powered) hyperextension. As the distal tip of the digit is raised from the substratum (Fig. 4), the setal shafts will be raised until the critical angle of 30.6° ± 1.8° is reached, resulting in setal detachment. This will take place in a coordinated fashion across fields of setae, thus resulting in a staged detachment process and allowing for controlled weight transference during the locomotor cycle. Such detachment will also be associated with controlled and staged depressurization of the scansorial sinus networks, with the distal regions being depressurized first (Russell, 1981b).
At the articulation between the penultimate and antepenultimate phalanx (Fig. 2A), the nature of the scansors changes as the sinus system quickly diminishes (Fig. 2F). From here proximally the phalanges are broad and depressed (Fig. 2B) and the scansors extend towards the base of the digits beneath these highly modified phalanges. Once hyperextension of the distal regions of the digits has occurred, locomotion continues by the gecko rolling onto the bases of its more medial digits before release is achieved (Fig. 3). This pattern essentially conserves the primitive pattern of roll off of pedal digits (Brinkman, 1980; Rewcastle, 1983). Regardless of whether digits are hyperextending distally or undergoing proximal to distal roll off more proximally, the effect of raising the setal shafts to the critical detachment angle is the same (Fig. 4). It is likely that the depressed intermediate phalanges adpress the more proximal scansors and the associated setae to the substratum at the time that distal hyperextension is taking place, thus enhancing the adhesive capacities of this region of the digits prior to roll off and final digital detachment.
Observations of anoline polychrotids are valuable in this regard (Russell and Bels, 2001a) as they reveal that although digital hyperextension does occur here, it is not powered actively—the distal end of the digit does not detach before the proximal end. Instead, digital roll off occurs in the primitive squamate fashion, with the digits rising from proximal to distal and the distalmost phalanges losing contact with the substratum last. In this process the digits are bent into a hyperextended configuration prior to release, but the hyperextended configuration is held throughout the swing phase. Thus, anoline scansors detach from proximal to distal throughout the length of the subdigital pad, but also attach from proximal to distal as the hyperextended digit is unfurled upon footfall.
The subdigital pads of anoles do not extend as far distally as do those of many geckos. These observations suggest that setal attachment and detachment occurred initially by employing the more primitive pattern of digital roll off, from base to tip, and only later did some taxa develop active hyperextension of the distal digital regions. Digital hyperextension in normal locomotion (Russell and Bels, 2001b) is common to both fast running (for example Uma scoparia and Dipsosaurus dorsalis, Irschick and Jayne, 1999; Fig. 4D and B, respectively; Sceloporus clarkii, Reilly and Delancey, 1997, Fig. 2) and climbing (Lacerta oxycephala, Arnold, 1998; Fig. 17) lizards (Fig. 5). It appears that active hyperextension was exapted from this in two stages—firstly by maintaining the distal end of the digit in the hyperextended configuration through the swing phase, and later employing hypertrophied muscles to actively hyperextend the distal ends of the digits prior to lift off of the basal digital regions. This has entailed changes in both the timing of events during locomotion, and morphological systems to permit this. Attainment of the critical release angle was possible at all times, but the way of bringing this about changed. It is likely that certain taxa of geckos employ mechanisms of pedal kinematics similar to those of anoles, but sufficient kinematic observations have yet to be made.
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QUESTIONS FOR FUTURE INVESTIGATION |
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The evolution of setae
Observations that have been made on both the anatomical configuration of the gekkonid adhesive system and the mechanism of bonding at the seta-substrate interface raise new questions for investigation. It is evident that the setae are homologs of the general spinules that cover the body surface via sculpturing of the Oberhaütchen layer (Maderson, 1970
; Stewart and Daniel, 1972). Furthermore, it is apparent that there is a gradation in the elaboration of these surface microornamentations from spinules to spines to spikes to prongs and finally to setae, in anoline polychrotids (Peterson, 1983) and geckos (Russell, 1976). It is also evident that the morphology of these structures, including their distal tips, changes over this range of expression. Autumn et al. (2000) demonstrated that it is not simply the material properties of these epidermal outgrowths that provide them with their adhesive properties, because they found that setae brought into contact with a suitable substratum with the spatulae directed away from the surface induced negligible adhesive interaction. Thus, it appears that a combination of changes in stalk dimensions and elaboration of the setal tip into at least one spatula is necessary for bringing about usable intermolecular force that can be regarded as having adhesive properties and, therefore, selective value in this regard. Subdivision of the setal tip into fields of setae enhances the adhesive properties further.
The questions that need to be approached next in this regard are those that investigate the functional properties, and thus the potential selective value, of the enlarged spines, spikes and prongs on subdigital surfaces before setae are fully elaborated. Here an interlocking (Emerson and Diehl, 1980; Riskin and Fenton, 2001) mode of action can be erected as a hypothesis to explain the favouring of these "intermediate" stages. Testing can be achieved by examining the surfaces on which such animals move in their natural environments, and examining them for their surface properties. A morphotypic series, such as that outlined for Cyrtodactylus (sensu lato) by Russell (1976: Fig. 13), could be employed to test such circumstances. Emerging from this is a question about the development of setal spatulae and whether the enhancement of a van der Waal's forces adhesive system comes about gradually or dramatically during this transitional sequence. It is evident that the Oberhaütchen outgrowths have been exapted for this new adhesive role, but at what stage it becomes operative, and whether this represents a quantum shift in adhesive properties is, as yet, unknown.
The morphotypic series depicted for Cyrtodactylus (sensu lato) (Russell, 1976: Fig. 13) also indicates that along with a trend in modification of the Oberhaütchen outgrowths towards a setal configuration, comes an elaboration of external digital form and internal anatomy that is reflected in the development of incipient scansors, changes in phalangeal morphology, and changes in the musculotendinous characteristics of the digits. Such a sequence leads to the raising of parallel questions about the integrated evolution of the adhesive system.
The origins of active hyperextension
As suggested above, on the basis of comparative observations of the kinematics of lizard digits in general (e.g., Arnold, 1998; Irschick and Jayne, 1999), those of anoline polychrotids (Russell and Bels, 2001a), and those of tokay geckos in particular (Russell, 1975; unpublished) primitive digital kinematics have been co-opted for hyperextension in two stages. The first is similar to that described for Anolis sagrei (Russell and Bels, 2001a), in which the digit is passively hyperextended as a result of gross pedal movements during the latter phases of the stance phase, and is then carried through the swing phase in the hyperextended configuration. Beyond this, some geckos have altered the timing of events such that the distal portions of the digits hyperextend actively from the substratum before the basal portions of the digits have begun to lift away. This entails modifications of the musculotendinous systems of the digits (Russell, 1975) (Fig. 2A) and enables locomotion on horizontal surfaces with the distal ends of the digits held in a permanently hyperextended configuration (personal observation). Such a transition may be of significance in performance outcomes. While anoles and geckos, when corrected for size, have been reported to exhibit similar clinging performance (Irschick et al., 1996), it is evident that not all digital plans and modes of operation result in equivalent locomotor performance on identical surfaces (personal observation). Performance measures of locomotion, rather than just static clinging, and their correlation with passive versus active hyperextension may again be instructive in the understanding of the evolution of the adhesive system as a whole.
Development of the perpendicular and parallel preloads
It was suggested above that a controlled perpendicular preload for the setae may be mediated through the digital sinus system (Russell, 1981b), or some other cushioning mechanism (see above). This hypothesis can be tested by measuring pressure changes in the digital sinus system and comparing these to kinematic analyses of digital movement, and force plate recordings of digital contact patterns. Comparative studies of taxa with different pad configurations and sinus architecture (Russell, 1976) may be instructive in this regard.
Similarly, the lateral digital tendon system has been implicated in the establishment of the parallel preload (Autumn et al., 2000) that is involved in maximizing the adhesive grip of the setae. This involvement can be tested by manipulative experiments in which the lateral digital tendon system is impaired in its activities, either directly or by modifications of the appropriate parts of the plantar aponeurosis (Russell, 1993).
Load distribution
It was argued above, and has been presented elsewhere (Russell et al., 1997), that the symmetry of the manus and the secondary symmetry of the pes of geckos enhances locomotor performance on vertical surfaces by always aligning at least some digits with maximal loading via gravitational forces acting along the long axes of these digits. If this is so, it is predicted that digital kinematics, especially in terms of release patterns, will change with body orientation, so that the digits playing the greatest role in support in that particular body configuration will maintain contact longer. In inverted locomotion on horizontal surfaces the loading regime of the digits cannot be influenced by vertical gravitational effects, and in such orientations the entire locomotor cadence and digital release sequence may change markedly. It is also predicted that in microgravity situations locomotor control and adhesive effectiveness will be severely compromised as there will be inappropriate sensory feedback (Lauff et al., 1993) and insufficient passive loading on the digits.
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CONCLUDING REMARKS |
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Recent demonstrations of the adhesive capacity of individual gecko setae and the loading regimes and three-dimensional orientation under which they operate (Autumn et al., 2000
), have permitted integration of our understanding of locomotor kinematics and anatomical configuration of the adhesive system with a clearer understanding of the adhesive process. An integrative overview of the system, from morphology to molecular bonding, permits a fuller understanding of what is necessary and sufficient for its operation, and leads to a clearer understanding of how such a configuration has arisen via multiple evolutionary pathways (Bock, 1959; Russell, 1976). This integration (Magwene, 2001) raises new questions about the evolution of such a system, and the morphological and functional transitions that may have occurred.
Comparative observations on a broader array of gekkonid taxa will assist in elucidating evolutionary sequences and functional integration and transformation. The gecko example that has been most fully studied is the tokay, Gekko gecko. This taxon exhibits a highly complex adhesive system. There are many taxa of geckos that have less complex arrangements (Russell, 1976), and it may be instructive to investigate some of these in parallel to determine the degree of functional variation that is possible in this taxon. It will also be necessary to conduct extensive and well-planned field work to begin to understand under what circumstances, such adhesive systems, play a significant role in nature, thus answering Maderson's (1970) plea for a better understanding of the selective value of such systems.
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ACKNOWLEDGMENTS |
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I wish to thank the symposium organizers, Kellar Autumn and Bob Full, for inviting me to participate, and the symposium sponsors for their financial support. I wish to acknowledge individuals who were responsible for kindling my interest in geckos and their locomotion—Angus Bellairs, Garth Underwood and Nick Arnold—more years ago than I care to remember. I thank Vincent Bels for the opportunity to conduct high speed videography of geckos in his laboratory. Financial support for my work over the years has been provided by the Natural Sciences and Engineering Research Council of Canada (grant no. OGP009745)—this is gratefully acknowledged, as is the excellent service of my long-suffering secretary, Eileen Muench.
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FOOTNOTES |
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1 From the Symposium Biomechanics of Adhesion presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 2–6 January 2002, at Anaheim, California.
2 E-mail: arussell{at}ucalgary.ca
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References |
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