Detecting substrate engagement: responses of tarsal campaniform sensilla in cockroaches

Sensory signals of contact and engagement with the substrate are important in the control and adaptation of posture and locomotion. We characterized responses of campaniform sensilla, receptors that encode forces as cuticular strains, in the tarsi (feet) of cockroaches using neurophysiological techniques and digital imaging. A campaniform sensillum on the fourth tarsal segment was readily identified by its large action potential in nerve recordings. The receptor discharged to contractions of the retractor unguis muscle, which engages the pretarsus (claws and arolium) with the substrate. We mimicked the effects of muscle contractions by applying displacements to the retractor apodeme (tendon). Sensillum firing did not occur to unopposed movements, but followed engagement of the claws with an object. Vector analysis of forces suggested that resisted muscle contractions produce counterforces that axially compress the tarsal segments. Close joint packing of tarsal segments was clearly observed following claw engagement. Physiological experiments showed that the sensillum responded vigorously to axial forces applied directly to the distal tarsus. Discharges of tarsal campaniform sensilla could effectively signal active substrate engagement when the pretarsal claws and arolium are used to grip the substrate in climbing, traversing irregular terrains or walking on inverted surfaces.     

Walking on smooth or rough ground: passive control of pretarsal attachment in ants

The hymenopteran tarsus is equipped with claws and a movable adhesive pad (arolium). Even though both organs are specialised for substrates of different roughness, they are moved by the same muscle, the claw flexor. Here we show that despite this seemingly unfavourable design, the use of arolium and claws can be adjusted according to surface roughness by mechanical control. Tendon pull experiments in ants (Oecophylla smaragdina) revealed that the claw flexor elicits rotary movements around several (pre-) tarsal joints. However, maximum angular change of claws, arolium and fifth tarsomere occurred at different pulling amplitudes, with arolium extension always being the last movement. This effect indicates that arolium use is regulated non-neuronally. Arolium unfolding can be suppressed on rough surfaces, when claw tips interlock and inhibit further contraction of the claw flexor or prevent legs from sliding towards the body. To test whether this hypothesised passive control operates in walking ants, we manipulated ants by clipping claw tips. Consistent with the proposed control mechanism, claw pruning resulted in stronger arolium extension on rough but not on smooth substrates. The control of attachment by the insect claw flexor system demonstrates how mechanical systems in the body periphery can simplify centralised, neuro-muscular feedback control.     

Elasticity and movements of the cockroach tarsus in walking

Anatomical, kinematic and ablation studies were performed to evaluate the contribution of elasticity in use of the cockroach tarsus (foot) in walking. The distal tarsus (claws and arolium) engages the substrate during the stance phase of walking by the action of a single muscle, the retractor unguis. Kinematic and ablation studies demonstrated that tarsal disengagement occurs at the end of stance, in part via the action of elastic elements at the penultimate tarsal joint. In isolated legs, this joint exhibits very rapid (less than 20 ms duration) recoil to extension when released from the engaged position, and recoil is even more rapid (less than 10 ms) after removal of the retractor tendon (apodeme). The joint also possesses an enlarged cuticular condyle which is the attachment for ligaments and articular membranes, some of which fulfill morphological criteria consistent with the presence of the elastic protein resilin. Measurements of restoring forces generated by joint displacement indicate that they are graded but could readily lift the mass of the distal tarsus. This biomechanical design can facilitate efficient use of the tarsus in walking while under active control by only a single muscle and may also be highly advantageous when cockroaches very rapidly traverse irregular terrain. Accepted: 16 September 1998     

Tarsal movements in flies during leg attachment and detachment on a smooth substrate

In order to understand the attachment mechanism of flies, it is important to clarify the question of how the adhesive pad (pulvillus) builds and breaks the contact with the substrate. By using normal and high-speed video recordings, the present study revealed that pulvilli are positioned on the surface in a particular way. The pulvilli are apparently loaded or pressed upon the substrate after leg contact, as evidenced by splaying of the claws. Detachment of pulvilli from the substrate may be achieved in four different modes depending on the leg (fore-, mid- or hindleg): pulling, shifting, twisting, and lifting. Lifting is the only detachment mode depending on the claws' action. Kinematics of the tarsal chain is studied in leg preparations, in which the tendon of the claw flexor muscle was pulled by tweezers and video recorded. The morphological background of tarsal movements during attachment and detachment is studied by scanning electron microscopy, fluorescent microscopy, and bright field light microscopy followed by serial semithin sectioning of pretarsal structures. Several resilin-bearing springs are involved in the recoil of the tarsal segments to their initial position, when the tendon is released after pull.     

Pretarsus structure in relation to climbing ability in the ants Brachyponera sennaarensis and Daceton armigerum

We studied the external and internal pretarsus structure of the ants Brachyponera sennaarensis and Daceton armigerum in relation to their very different climbing ability. B. sennaarensis is a ground-dwelling species that is not able to climb vertical smooth walls. They have a pair of straight pretarsal claws with an average claw tip angle of 56 degrees, while the ventral tarsal surface lacks fine hairs that touch the substrate. They have no adhesive pad on the vestigial arolium, while the arolium gland is very small. D. armigerum, on the other hand, is an arboreal and thus well-climbing species with a very strong grip on the substrate. Their pretarsal claws are very hooked, with a claw tip angle around 75 degrees. They have dense arrays of fine hairs on the ventral tarsal surface, a well-developed arolium and arolium gland. These clearly different morphological characteristics are in line with the opposite climbing performance of both species.     

Insect walking techniques on thin stems

The attachment ability of insects on surfaces are associated not only with the micro- and nanostructure of the adhering part of an attachment device, but also with the global scale kinematics responsible for contact formation and release. In the present study, the locomotory techniques of several representatives of insects from four different orders (Orthoptera, Heteroptera, Coleoptera, and Hymenoptera), possessing different types of attachment structures, are described. The study is based on video recordings of insects walking on a flat surface and on cylindrical rods of various thickness, imitating plant stems. Attachment devices of tarsi and pretarsi were visualized using Scanning Electron Microscopy. The results show a different manner in the use of adhesive structures on substrates with various curvatures. Insects bearing attachment pads on proximal tarsomeres usually touch flat and curved substrates using all tarsomeres, whereas insects with their attachment devices on the distal tarsomeres usually walk on flat surfaces using the distal tarsomeres of the overextended tarsus. On substrates, with diameters comparable to or larger than the tarsus length, insects walk above the stem by clasping the stem with the bent tarsi. On thin stems, insects clasp the stem between their tarsi and hang under the stem. Thus, on thin and thick rods, forces applied to attachment organs act in opposite directions. There are two methods of leg positioning for walking on a rough flat substrate. In the first case, the tarsus is straightened and the rough substrate is gripped between the claws and the proximal complex of attachment devices (tarsal euplantulae, fossulae spongiosa, and terminal spurs of tibiae). In the second case the tibia does not touch the substrate; the insect is supported only by distal tarsomeres. The tarsus is in an overextended condition. On rods, with diameters comparable to or larger than the tarsus length, insects walk by clasping the stem with the bent tarsi. This posture is characteristic for the majority of insects independent of the tarsal position they normally use while walking on a plane. If the rod’s diameter is smaller than the tarsus length, walking insects usually clutch it between contralateral tarsi. Using such a posture they are supported by interlocking or by strong friction, generated by attachment devices of the proximal tarsomeres, and do not use attachment devices of the pretarsus. Contact with the substrate is reinforced due to the coordinated contralateral clutch using all supporting legs. It is concluded that the use of different types of attachment structures correlates with locomotory techniques. Handling Editor: Heikki Hokkanen     

Arcus as a tensegrity structure in the arolium of wasps (Hymenoptera: Vespidae)

The unfolding of the hymenopteran attachment pad (arolium) may be achieved in two ways, hydraulic and mechanical. The first was confirmed in experiments with pressure applied to more proximal leg parts and on immersion in hypotonic solutions. Presumably, this way of unfolding does not play an important role for a living hornet. Mechanical unfolding was studied experimentally with the aid of a micromanipulator pulling the tendon of the musculus retractor unguis. Ablation experiments on different parts of the arolium indicated that the arcus is the most crucial element for mechanical unfolding. The shape of the arcus in closed and open conditions was measured using a 3D measurement microscope and reconstructed by means of 3D computer graphics. The arcus coils up upon being freed from the arolium tissues, and coils up even more after immersion into a 10% aqueous solution of NaOH. Geometrical models of the arcus are proposed, from which the rotational moment of elasticity is derived. Conformations and deformations of the arcus are quantified in order to explain its role in the folding and unfolding processes of the arolium. The diversity of approaches supports the idea that the arcus is a prestressed (tensegrity) structure providing immediate, soft, and graded transmission of forces during folding and unfolding action of the arolium.     

Giant stick insects reveal unique ontogenetic changes in biological attachment devices

A strong modification of tarsal and pretarsal attachment pads during the postembryonic development is described for the first time. In the exceptionally large thorny devil stick insect Eurycantha calcarata a functional arolium is only present in the immature instars, enabling them to climb on smooth surfaces, especially leaves. Nymphs are also characterized by greyish and hairy euplantulae on tarsomeres 1–4. The gradual modifications of the arolium and the euplantula of tarsomere 5 in the nymphal development are probably mainly related to increased weight. The distinct switch in the life style between the leaf-dwelling nymphal stages and the ground-dwelling adults results in the final abrupt change of the adhesive devices, resulting in a far-reaching reduction of the arolium, the presence of a fully-developed, elongated euplantula on tarsomere 5, and white and smooth euplantulae on tarsomeres 1–4. The developmental remodelling of attachment pads also reflects a phylogenetic pattern. The attachment devices of the earlier instars are similar to those found in the basalmost lineage of extant stick insects, Timema, which is characterized by a very large pan-shaped arolium and a hairy surface of the tarsal and pretarsal attachment pads.     

Evolution of locomotory attachment pads in the Dermaptera (Insecta)

This contribution is the first comparative SEM study of tarsal and pretarsal structures of 18 dermapteran species, including epizoic Hemimeridae, rare Apachyidae, as well as basal Pygidicranidae. Our data reject the apparent uniformity of this taxon and show that representatives of Dermaptera have independently evolved both types of attachment mechanisms: hairy and smooth. Dermaptera possess a wide spectrum of attachment devices: arolia, euplantulae, tarsal surfaces covered with specialised tenent setae and other types of cuticular outgrowths. The groundpattern of the pretarsal and tarsal attachment structures was reconstructed by mapping their characters onto a cladogram, generated without tarsal characters. In the groundpattern of recent Dermaptera, the tarsus consists of three tarsomeres. Presumably, the last common ancestor of the Dermaptera possessed an arolium, since this structure occurs in the most basal taxa: Diplatyidae, Karschiellidae (partim, adults), Pygidicranidae partim, and Apachyidae. The absence of arolium in two of the pygidicranid taxa is probably due to a secondary loss. The arolium seems to be reduced in the 'higher Dermaptera' and amongst them, only the Geracinae, which belong to the Spongiphoridae and, hence, to the well supported Eudermaptera [European Journal of Entomology, 98 (2001), 445], evolved this structure convergently. The character state distribution for euplantulae suggests their evolution being similar to that of the arolium. All species of Tagalina possess a specialised tarsus with a strongly dilated second tarsomere. The same applies to the Forficulidae. However, their relatively remote phylogenetic position to Tagalina burri is a convincing reason to assume convergent evolution of this character. The Chelisochidae, with a slender, elongated second tarsomere, possess a unique structure, which supports their monophyly. The special, heart shaped structure of the second tarsal segments in the Forficulidae suggests their monophyly. The attachment structures of Hemimerus vosseleri are highly derived and probably autapomorphic for this taxon.     

Pushing versus pulling: division of labour between tarsal attachment pads in cockroaches

Adhesive organs on the legs of arthropods and vertebrates are strongly direction dependent, making contact only when pulled towards the body but detaching when pushed away from it. Here we show that the two types of attachment pads found in cockroaches (Nauphoeta cinerea), tarsal euplantulae and pretarsal arolium, serve fundamentally different functions. Video recordings of vertical climbing revealed that euplantulae are almost exclusively engaged with the substrate when legs are pushing, whereas arolia make contact when pulling. Thus, upward-climbing cockroaches used front leg arolia and hind leg euplantulae, whereas hind leg arolia and front leg euplantulae were engaged during downward climbing. Single-leg friction force measurements showed that the arolium and euplantulae have an opposite direction dependence. Euplantulae achieved maximum friction when pushed distally, whereas arolium forces were maximal during proximal pulls. This direction dependence was not explained by the variation of shear stress but by different contact areas during pushing or pulling. The changes in contact area result from the arrangement of the flexible tarsal chain, tending to detach the arolium when pushing and to peel off euplantulae when in tension. Our results suggest that the euplantulae in cockroaches are not adhesive organs but 'friction pads', mainly providing the necessary traction during locomotion.     

Locomotion and adhesion: dynamic control of adhesive surface contact in ants

Tarsal adhesive pads of insects are highly dynamic organs that play an important role in locomotion. Many insects combine fast running performance with strong resistance to detachment forces. This capacity requires an effective control of attachment forces at the tarsus and pretarsus. Here we investigate mechanisms of attachment control in Asian weaver ants (Oecophylla smaragdina) by measuring the dynamics of the adhesive contact area and the claws during locomotion. O. smaragdina ants walking upside down on a smooth substrate used only a fraction (approx. 14%) of their maximum possible contact area. When these ants were loaded with 30 mg weights (corresponding to approx. 6 times their own body weight), however, they employed much larger (but still submaximal; approx. 60%) contact areas. The increase of contact area was accompanied by a stronger flexion of the claws, which demonstrates the participation of the claw flexor muscle in the control of adhesive contact. However, only part of the contact area dynamics could be explained by the action of the claw flexor. During the stance phase, adhesive contact area changed while the claws remained motionless. Even when corrected for the effects of claw flexion, adhesive contact areas differed by a factor of 2.1 between loaded and unloaded ants. Our findings give evidence that running ants control their adhesive contact area by a combination of active movements of the claw flexor muscle and passive reactions of the mechanical system.     

Positive force feedback in development of substrate grip in the stick insect tarsus

The mechanics of substrate adhesion has recently been intensively studied in insects but less is known about the sensorimotor control of substrate engagement. We characterized the responses and motor effects of tarsal campaniform sensilla in stick insects to understand how sensory signals of force could contribute to substrate grip. The tarsi consist of a chain of segments linked by highly flexible articulations. Morphological studies showed that one to four campaniform sensilla are located on the distal end of each segment. Activities of the receptors were recorded neurographically and sensilla were identified by stimulation and ablation of their cuticular caps. Responses were characterized to bending forces and axial loads, muscle contractions and to forces applied to the retractor apodeme (tendon). The tarsal sensilla effectively encoded both the rate and amplitude of loads and muscle forces, but only when movement was resisted. Mechanical stimulation of the receptors produced activation of motor neurons in the retractor unguis and tibial flexor muscles. These findings indicate that campaniform sensilla can provide information about the effectiveness of the leg muscles in generating substrate adherence. They can also produce positive force feedback that could contribute to the development of substrate grip and stabilization of the tarsal chain.     

Distal leg structures of the Aculeata (Hymenoptera): A comparative evolutionary study of Sceliphron (Sphecidae) and Formica (Formicidae)

The distal parts of the legs of Sceliphron caementarium (Sphecidae) and Formica rufa (Formicidae) are documented and discussed with respect to phylogenetic and functional aspects. The prolegs of Hymenoptera offer an array of evolutionary novelties, mainly linked with two functional syndromes, walking efficiently on different substrates and cleaning the body surface. The protibial-probasitarsomeral cleaning device is almost always well-developed. A complex evolutionary innovation is a triple set of tarsal and pretarsal attachment devices, including tarsal plantulae, probasitarsomeral spatulate setae, and an arolium with an internal spring-like arcus, a dorsal manubrium, and a ventral planta. The probasitarsal adhesive sole and a complex arolium are almost always preserved, whereas the plantulae are often missing. Sceliphron has retained most hymenopteran ground plan features of the legs, and also Formica, even though the adhesive apparatus of Formicidae shows some modifications, likely linked to ground-oriented habits of most ants. Plantulae are always absent in extant ants, and the arolium is often reduced in size, and sometimes vestigial. The arolium contains resilin in both examined species. Additionally, resilin enriched regions are also present in the antenna cleaners of both species, although they differ in which of the involved structures is more flexible, the calcar in Sceliphron and the basitarsal comb in Formica. Functionally, the hymenopteran distal leg combines (a) interlocking mechanisms (claws, spine-like setae) and (b) adhesion mechanisms (plantulae, arolium). On rough substrate, claws and spine-like setae interlock with asperities and secure a firm grip, whereas the unfolding arolium generates adhesive contact on smooth surfaces. Differences of the folded arolium of Sceliphron and Formica probably correlate with differences in the mechanism of folding/unfolding.     

Ground reaction forces in vertically ascending beetles and corresponding activity of the claw retractor muscle on smooth and rough substrates

We measured ground reaction forces in fore–aft and normal directions of single hind and front legs in vertically ascending Sagra femorata beetles (Coleoptera, Chrysomelidae) on a smooth and a rough substrate. Simultaneously, we performed electromyographic recordings (EMGs) of the hind leg claw retractor muscle that partly controls the attachment structures. On both substrates, hind legs produced upward- as well as downward-directed forces during one stance phase. Forces were equivalent in both directions. Front legs generated only upward-directed forces. The main function of hind legs in ascending beetles in the second half of the stance thus probably prevented the animals from tilting away from the substrate. The EMGs of hind legs showed an early spike during stance with large amplitude. It was mostly followed by few additional spikes with large amplitude and in some cases of spikes with smaller amplitude distributed throughout the stance phase. We found significantly more spikes on the rough substrate than on the smooth one. This is probably due to the more important role of pretarsal claws than tarsal hairy attachment pads on the rough substrate or to the reduced adhesive forces on the rough substrate that have to be compensated by additional muscle activity.     

The Anatomy of the Tarsi of Schistocerca gregaria Forskål

Summary The tarsus of S. gregaria is divided into three units (here called segments) and an arolium set between a pair of claws. The first segment bears three pairs of pulvilli in the fore and middle legs, and one pair and two single pulvilli in the hind legs. Segment two bears a pair of pulvilli, segment three one long pulvillus and the arolium a similar pad on the undersurface. The outer layers of the arolium pad differ from those of the pulvilli in possibly lacking an epicuticle and in having a layer of cuticle which, unlike the corresponding layer in the pulvilli, does not stain with protein stains. The claws and dorsal surfaces bear trichoid sensilla, basiconic sensilla and campaniform sensilla. Smaller basiconic sensilla and canal sensilla occur on the proximal part of the pulvilli, and basiconic sensilla on the arolium undersurface. Internally the cuticle is modified in the arolium and pulvilli so that rods of probably chitin and resilin are formed. This would impart flexibility to the undersurfaces whilst retaining some degree of rigidity which might prevent damage to the small and delicate sense organs on the pulvilli. The tip of the arolium is specialised for adhesion, and there are two large neurones internally which could conceivably monitor attachment or detachment of the tip. There are chordotonal organs in segment three, and several other large neurones throughout the tarsus, some of which are associated with the slings of tissue holding the apodeme in a ventral position. Gland cells occurring in the dorsal epidermis of the adult mature male are also briefly described.     

Microscopic analysis of mechanosensory system monitoring the dynamic claw actions in the tenebrionid beetle Zophobas atratus

Many insects have a pair of claws on each leg. The distribution of mechanoreceptors that monitor claw actions was examined in the tenebrionid beetle Zophobas atratus. Each claw has 25–45 campaniform sensilla (CS) that detect the claw’s deformation due to substrate engagement. Five CS clusters are observed around the end of the 5th tarsomere (Ta5) in a concave, socket-like structure. The 1st cluster, containing 2–5 CS, is embedded in the unguifer to which the claws are articulated. The symmetrical 2nd and 3rd clusters, each containing two CS, are located bilaterally in the ventrolateral grooves of the sidewall of the socket, into which the unguis retractor plate slides. The 4th and 5th clusters, containing 1–2 CS with two hair sensilla, are localized near the ventrolateral ridges of the socket into which the basal portion of the claw is pressed during maximal claw flexion. In addition, Ta5 has a chordotonal organ of six sensory cells to monitor claw extension. These results suggest that the mechanoreceptor system may directly monitor the precise mechanical states of individual claws and provide the central nervous system with the sensory information required for fine feedback control of movements of the pretarsus and other leg segments for locomotion and other purposes.     

Adhesive properties of the arolium of a lantern-fly, Lycorma delicatula (Auchenorrhyncha, Fulgoridae)

The arolium in Lycorma delicatula is shaped as a truncated pyramid, tapering proximally. The base or the terminal area is corrugated, forming parasagittal wrinkles (period 1.5-5.0 microm), which are supported from inside by cuticular dendrites. Side faces of the arolium are made up of sclerotized dorsolateral plates. When claws slip on a smooth substrate and pronate, the dorsolateral plates diverge and expand the sticky terminal area. The real contact area with the glass plate was recognized by light reflection on its periphery. This area was measured and shown to be smaller when the leg was pressed perpendicularly to the substrate (0.02 mm(2)) than when it was sheared in a direction parallel to the substrate (0.05 mm(2)). Attachment forces were measured with the aid of dynamometric platforms during pulling of active insects from horizontal or vertical glass surfaces. Normal adhesive force (about 9-12 mN) was much less than friction force during sliding with velocity of 6-17 mm/s (50-100 mN); however, when expressed in tenacity per unit contact area the difference was less pronounced: 170 and 375-625 mN/mm(2), respectively. Sliding of the arolium during shear displacement was shown to be oscillatory in frame-by-frame video analysis. Relaxative oscillations consisted of periodical sticks-slips of the arolium along the glass surface.     

The pretarsus of salticid spiders

The pretarsus of Phidippus audax (Hentz) consists of two claws flexibly articulated to a central claw lever which is flanked on either side by a curved plate of tenent setae. The claw apparatus allows for retraction of the claws by means of a dorsal cuticular cable of the pretarsal levator, while extension involves the pull of the pretarsal depressor on a ventral cable attached to the claw lever. A series of slit sensilla are strategically situated on either side of this lever. The anterior and posterior claws of the pretarsus differ in the number and spacing of their constituent teeth. The claw tufts are composed of specialized setae which account for the mechanical traction of the foot-pads. Whorled and filamentous setae of the distal tarsus are associated with the pretarsus. Comparable structures are found on other salticids.     

Functionally Different Pads on the Same Foot Allow Control of Attachment: Stick Insects Have Load-Sensitive “Heel” Pads for Friction and Shear-Sensitive “Toe” Pads for Adhesion

Stick insects (Carausius morosus) have two distinct types of attachment pad per leg, tarsal “heel” pads (euplantulae) and a pre-tarsal “toe” pad (arolium). Here we show that these two pad types are specialised for fundamentally different functions. When standing upright, stick insects rested on their proximal euplantulae, while arolia were the only pads in surface contact when hanging upside down. Single-pad force measurements showed that the adhesion of euplantulae was extremely small, but friction forces strongly increased with normal load and coefficients of friction were 1. The pre-tarsal arolium, in contrast, generated adhesion that strongly increased with pulling forces, allowing adhesion to be activated and deactivated by shear forces, which can be produced actively, or passively as a result of the insects'' sprawled posture. The shear-sensitivity of the arolium was present even when corrected for contact area, and was independent of normal preloads covering nearly an order of magnitude. Attachment of both heel and toe pads is thus activated partly by the forces that arise passively in the situations in which they are used by the insects, ensuring safe attachment. Our results suggest that stick insect euplantulae are specialised “friction pads” that produce traction when pressed against the substrate, while arolia are “true” adhesive pads that stick to the substrate when activated by pulling forces.