Stick Insect Antennae
Insects have an elaborate sense of touch. Their most important source for tactile information is the pair of feelers on the head: the antennae (Fig. 1; singular: antenna). The stick insect Carausius morosus is one of four major study organisms for the insect tactile sense. Accordingly, the stick insect antenna (or feeler), together with the antennae of the cockroach, cricket and honeybee, belongs to the best-studied insect antennae. The aim of the present article is to provide an overview over the behavioural relevance, adaptive properties and sensory infrastructure of stick insect antennae, along with a complete bibliography thereof. For a more general treatment of the topic, please refer to the review by Staudacher et al. (2005).
As most stick insects are nocturnal, flightless insects, tactile sensing is of prime importance for exploration of the space immediately ahead of the animal. For example, obstacle detection and path-finding in the canopy at night are likely to be tasks where tactual near-range information is highly valuable to the animal.
Moreover, the stick insect is an important study organism in motor control of invertebrates and the neuroethology of insect walking. Nearly a century of research has led to a host of information about its walking behaviour and leg coordination (Buddenbrock, 1920; Wendler, 1964; Bässler, 1983; Cruse, 1990), central and sensory contributions to motor pattern generation (Graham, 1985; Bässler and Büschges, 1998; Büschges and Gruhn, 2007) the neural and muscular infrastructure (Jeziorski, 1918; Marquardt, 1939; Schmitz et al., 1991; Kittmann et al., 1991), and so on. On that background, the neuroethology and physiology the stick insect’s tactile near-range sense can serve as a model for understanding the significance of the arthropod antenna in sensory-guided behaviour.
Antennae are active near-range sensorsMovie 1: Stick insects continuously move their antennae during walking. The video shows a blindfolded stick insect walking towards a block of wood. Note that the video was slowed down five-fold. Next to the walkway, there was a mirror mounted at an angle of 45 degrees, allowing synchronous recording of top and side views. If an antenna touches an obstacle, as the right antenna does in this video, then this touch event leads to an appropriate action of the front leg on the same side.
Like many other insects, C. morosus continuously moves its antennae during locomotion. By doing so, it actively raises the likelihood of tactile contacts with obstacles because each up-down or rear-to-front sweep of an antenna samples a volume of space immediately ahead. Accordingly, the antennal movement pattern can be considered an active searching behaviour. During this searching behaviour, antennal movement is generated by rhythmic movement of both antennal joints with the same frequency and a stable phase shift (Krause et al., 2013). Moreover, it is clear that this searching movement is generated within the brain, despite the fact that the brain requires additional activation, possibly through ascending neural input from the suboesophageal ganglion (Krause et al., 2013). Antennal searching movements have been shown to be adapted according to the behavioural context, e.g., when the insect steps across an edge and searches for foothold (Dürr, 2001). Similarly, the beating field (or searched volume) of the antennae is shifted into the walking direction during turning (Dürr and Ebeling, 2005).
Experiments have shown that the movement pattern of the antennae is rhythmical and may be coordinated with the stepping pattern of the legs (Dürr et al., 2001). This can be seen in Movie 1, showing a blindfolded stick insect that walks towards a block of wood. During approach of the obstacle, the top view shows how both antennae are moved rhythmically from side to side. Soon after a brief contact of the right antenna, the insect lifts its ipsilateral leg higher than normal and steps onto the top of the block (same trial as in Fig. 2, top right).
Examples like this show that stick insects respond to antennal tactile contact with appropriate adaptation of their stepping pattern and leg movements. Depending on the timing of the antennal contact with respect to the step cycle of the ipsilateral leg, three kinds of behavioural responses are easily distinguished:
- The first kind is the one shown in the video Movie 1. If the antennal contact occurs during early swing, the foot trajectory often reveals a distinct upward kink, indicating re-targeting of an ongoing swing movement (Fig. 2, top right). Essentially this means that antennal touch information can interfere with the cyclic execution of the normal stepping pattern of the front legs, such that it can trigger re-targeting of an ongoing swing movement.
- The second kind occurs when the antennal contact happens during late swing. In this case, reaction time appears to be too short for re-targeting and the foot hits the obstacle, only to be raised in a second, correcting step (Fig.2, middle right).
- Finally, in the third kind of response, antennal contact occurs during stance. Then, stance movement is completed and the following swing movement is higher than a regular step (Fig. 2, lower right).
The analysis of adaptive motor behaviour in response to antennal touch can be simplified if the touched obstacle is nearly one-dimensional, e.g., a vertical rod (Schütz and Dürr, 2011). In this case, it can be demonstrated that antennal touch information is not only used for rapid adaptation of goal-directed leg movements, but also triggers distinct changes of the antennal tactile sampling pattern, including an increase in cycle frequency and a switch in inter-joint coupling. Therefore, tactile sampling behaviour is clearly distinct from searching behaviour.
Tactile sampling of other obstacles, e.g., stairs of different height, bears very similar characteristics (Krause and Dürr, 2012). During crossing of large gaps, antennal contacts of the species Aretaon asperrimus (Brunner von Wattenwyl 1907) have been shown to 'inform' the animal about the presence of an object in reach (Bläsing and Cruse, 2004a; Bläsing and Cruse, 2004b, though antennal movements have not been analysed in detail in this animal. In both Carausius and Aretaon, antennal contact information ensues a change in leg movement, as necessary during climbing. Similar tactually mediated climbing behaviour has been described in the cockroach.
In summary, tactile information from the antenna induces an adjustment of leg movements in a context-dependent manner. Moreover it induces changes in the antennal movement itself.
Antennae are dedicated sensory limbs
The antenna of the Arthropoda (crustacea, millipedes and insects carry antennae, arachnids do not) is considered to be a true limb that evolved from a standard locomotory limb into a dedicated sensory limb. Various lines of evidence suggest that the segmented body structure of the arthropods once carried leg-like motor appendages on each segment. As some body segments adopted specialised functions during the course of evolution, their motor appendages changed their function accordingly. For example, the insect head is thought to have evolved by fusion of the six most frontal body segments, with three pairs of limbs having turned into mouthparts that specialised for feeding, two pairs having been lost, and one pair having turned into dedicated, multimodal sensory organs – the antennae. This common theory is supported by palaeontological, morphological, genetic and developmental evidence.
For example, a simple experiment on stick insects illustrates the close relationship between walking legs and antennae: if a young stick insect larva loses an antenna, it often regenerates a walking leg instead of an antenna (Schmidt-Jensen, 1914). This "faulty" regeneration is called an antennapedia regenerate (literally: "antennal feet") It happens during the next moult and becomes more pronounced with each successive moult. Antennapedia regenerates can be induced experimentally by cutting an antenna of a stick insect larva (e.g., 3rd instar) at the second segment, the pedicel (Fig. 3). The site of the cut determines the outcome of the regeneration: distal cuts lead to a "correct" antenna regenerate, proximal cuts lead to complete failure of regeneration. Only cuts through a narrow region of the pedicel reliably induce an antennapedia regenerate (Cuénot, 1921; Brecher, 1924; Borchardt, 1927). Note that there is also a Drosophila gene called Antennapedia.
Morphological similarity between walking legs and antennae concerns the structure of joints, musculature, innervation and most types of mechanoreceptors and contact chemoreceptors (Staudacher et al., 2005). Differences concern the number of functional segments (five in legs, three in antennae), cuticle properties (see below) and sensory infrastructure (e.g., olfactory receptors on antennae, only).
The antenna has three functional segments: they are called scape, pedicel and flagellum, from base to tip. In the stick insect, only the scape contains muscles (Dürr et al., 2001). This is the same in all higher insects (the Ectognatha; see Imms, 1939). In other words, true joints that are capable of active, muscle-driven movement occur only between head and scape (HS-joint) and between scape and pedicel (SP-joint). The HS-joint is moved by three muscles inside the head capsule (so-called extrinsic muscles, because they are outside the antenna), the SP-joint is moved by two muscles inside the scape (so-called intrinsic muscles, because they are located inside the antenna).
Four adaptations improve tactile efficiency
Several morphological, biomechanical and physiological properties of the stick insect antenna are beneficial for its function in tactually guided behaviour. Four of such adaptations are:
- Matching lengths of antennae and front legs (in all developmental stages)
- Co-ordinated movement of antennae and legs
- Non-orthogonal, slanted joint axes
- Special biomechanical properties, such as damping
Matching lengths of antennae and front legs
As active tactile sensors are particularly well-suited for exploration of the near-range environment, it is reasonable to assume that their action range tells us something about the animal’s behavioural requirements to react to near-range information. Since stick insects generally are nocturnal animals, their antennae are likely to be their main "look-ahead sense" (rather than the eyes). Moreover, as many stick insect species are obligatory walkers, tactile exploration is likely to serve obstacle detection and orientation during terrestrial locomotion. In C. morosus, the length of the antenna matches that of a front leg such that the action radii of the antennal tip and the end of the foot are nearly the same (See Fig. 4). Thus, potentially, anything the antenna touches is located within reach of the front leg. As Fig. 4 shows, this is the case throughout development. Owing to this match, the stick insect is able to adapt its locomotory behaviour to a touch event within the action distance of one length of a leg, and with a look-ahead time of up to one step cycle period. In fact, reaction times of a front leg reacting to an antennal touch event is in the range of 40 ms (Schütz and Dürr, 2011), and several classes of descending interneurons have been described that convey antennal mechanosensory information from the antenna to the motor centres of the front leg (Ache and Dürr, 2013). Some of these descending interneurons have been characterized individually to quite some detail. For example, a set of three motion-sensitive descending interneurons encodes information about antennal movement velocity in a complementary manner: two of them respond by increases in spike rate, the third one responds by a decrease in spike rate (Ache et al., 2015). Because these movement-induced changes in spike rate occur with very short latency (approx. 15 ms at the entry of the prothoracic ganglion) they are suitable candidates for mediating the fast, tactually induced reach-to-grasp reaction described above.
Note that the length of the antennae does not match the length of the front legs in all stick insect species. In some species, like Medauroidea extradentata (Redtenbacher 1906), the antennae are much shorter than the front legs, indicating that their antennae are not suited for tactile near-range searching (because the feet of the front leg will nearly always lead the antennal tips). In the case of M. extradentata (= Cuniculina impigra), it has been shown that the front legs execute very high swing movements during walking and climbing (Theunissen et al., 2015). Thus, in these animals the front legs appear to take on the function of tactile near-range searching.
Coordinated movement of antennae and legs
Antennae and front legs not only match in length, their movement may be coordinated in space and time, too (Dürr et al., 2001). Temporal coordination is revealed by the gait pattern of a straight walking stick insect in Fig. 5 (left), where the rhythmical protraction phases of the antenna (red) are shifted relative to the rhythmical retraction phases of the legs (blue). The pattern is the same for left and right limbs. In both cases, coordination is well-described by a rear-to-front wave travelling along the body axis (indicated by grey arrows). As if activated by such a wave, the middle legs follow the hind leg rhythm, the front legs follow the middle legs, and the antennae follow the front legs. Note that this pattern depends on walking conditions and behavioural context.
Antennae and front legs are also coordinated spatially (Fig. 5, right) such that the antennal tip leads the foot of the same body side (in the top view plot, grey lines connect coincident points). Moreover, the lateral turning points of the antennal tip’s trajectory are always very close to the most lateral position of the foot during the next step. Both, temporal and spatial coordination support the hypothesis that the antenna actively explores the near-range space for objects which require the ipsilateral leg to adapt its movement. Indeed, it has been shown that the likelihood of the antenna to detect an obstacle before the leg gets there, i.e., in time for the leg to react, increases with the height of the obstacle, and gets very large for obstacles that are so high that climbing them requires an adaptation of leg movements (Dürr et al., 2001).
Non-orthogonal, slanted joint axes
As mentioned above, all higher insects have only two true joints per antenna (Imms, 1939), meaning that only two joints are actively moved by muscles. In stick insects, both of these joints are revolute joints (hinge joints) with a single, fixed rotation axis. Because of the fixed joint axes, a single joint angle accurately describes the movement of each joint (they have a single Degree Of Freedom, DOF). Therefore, the two DOF associated with the two revolute joints of a stick insect antenna, fully describe its posture.
The spatial arrangement of the two joint axes determines the action range of the antenna (Krause and Dürr, 2004). For example, if both joint axes were orthogonal to each other, and if the length of the scape was zero, the antennal joints would work like a universal joint (or Cardan joint): the flagellum could point into any direction. Because the scape is short relative to the total length of the antenna, its length has virtually no effect on the action range of the antenna. However, the joint axes of sick insect antennae are not orthogonal to each other (Dürr et al., 2001; Mujagic et al., 2007), which has the effect that the antenna can not point into all directions (Fig. 6). Instead, there is an out-of reach zone, the size of which directly depends on the angle between the joint axes (Krause and Dürr, 2004).
This is different than in other insect groups, for example crickets, locusts and cockroaches. Mujagic et al. (2007) argued that this non-orthogonal arrangement of the joint axes might be an adaptation to efficient tactile exploration. Their argument goes as follows: For a given minimal change in joint angle, the resulting change in pointing direction will be smaller in an arrangement with out-of-reach zones than in an arrangement without (Dürr and Krause, 2001). Essentially, this is because the surface of the area that can be reached by the antennal tip decreases (due to the out-of-reach zone), but the number of possible joint angle combinations stays the same. Therefore, theoretically, an arrangement with out-of-reach zones has improved positioning accuracy. Since the order of the stick insects (Phasmatodea) is thought to have evolved as a primarily wingless group of insects (Whiting et al., 2003), and because all Phasmatodea are nocturnal, tactile exploration must be expected to be their prime source of spatial information. The finding that slanted, non-orthogonal joint axes are an autapomorphy of the Phasmatodea suggests that this insect order has evolved an antennal morphology that is efficient for tactile near-range sensing (Mujagic et al. 2007; strictly, is has been shown for the so-called Euphasmatodea, only).
Special biomechanical properties
Last but not least, there are particular biomechanical features that support the sensory function of the antenna. In particular, this concerns the function of the delicate, long and thin flagellum that carries thousands of sensory hairs. In Carausius morosus, the flagellum is about 100 times as long as its diameter at the base. If this structure was totally stiff, it would break very easily. In the other extreme, if it was too flexible, it would be very inappropriate for spatial sampling, simply because its shape would change all the time. As a consequence, much of the sensory resources would have to go into monitoring the own curvature, at least if contact locations in space were to be encoded. In C. morosus, the skeletal properties of the antenna are such that the flagellum remains stiff during self-generated movement (e.g., during searching) but is very compliant when in contact with obstacles (e.g., during tactile sampling). For example, the flagellum frequently bends very much as the stick insect samples an obstacle during climbing.
The structure of the cuticle, i.e. the layered material of the external skeleton, suggests that this combination of features is caused by the balanced function of a stiff outer cone (of exocuticle) that is lined by a soft inner wedge (of endocuticle, see Fig. 6). Owing to the different material properties of the inner and outer cuticle layers, the water-rich inner endocuticle supposedly acts like a damping system that prevents oscillations that would be caused by the stiff material alone. As a result, a bent antenna can snap back into its resting posture without over-shoot, a sign of over-critical damping. Indeed, experimental desiccation of the flagellum (a method known to reduce water content and, therefore, damping of the endocuticle) strongly changes the damping regime of the antenna, to under-critical damping (Dirks and Dürr, 2011).
There are specialised sensors for pointing direction, contact site, bending, vibration, and more
The antenna is the most complex sensory organ of an insect (Staudacher et al., 2005). It carries thousands of sensory hairs, the sensilla, that subserve the modalities of smell (olfaction: Tichy and Loftus, 1983), taste (gustation), temperature (thermoreception: Cappe de Baillon, 1936; Tichy and Loftus, 1987; Tichy, 2007), humidity (hygroreception: Tichy, 1979; Tichy, 1987; Tichy and Loftus, 1990), gravity (graviception: Wendler, 1965; Bässler, 1971), and touch.
With regard to touch, there are at least four mechanosensory submodalities that contribute to touch perception in insects. Each one of them is encoded by different types of sensory hairs (sensilla) or modifications thereof (for review, see Staudacher et al., 2005). At least one of these sensory structures, the hair fields, must be considered as proprioceptors, as they encode the (actively controlled) antennal posture. On the other hand, there are also genuine exteroceptive sensory structures, the tactile hairs, that encode touch location along the antenna. As yet, there are also sensory structures that convey both proprioceptive and exteroceptive information: Campaniform sensilla and a chordotonal organ are thought to encode the bending and vibration of the flagellum and, therefore, postural changes. The energy required to bring about the postural change may be of external cause (e.g., wind) or self-generated during locomotion and/or active searching (e.g., self-induced contact with an obstacle). As a consequence, the distinction between exteroception and proprioception vanishes for these sensory structures for as long as there is no additional information about whether the flagellum had been moved or relocated by self-generated movement.
Pointing direction (Hair fields)
Hair fields are patches of sensory hairs that are located near the joints. Essentially, they serve as joint angle sensors in which individual hairs get deflected if it is pressed against the juxtaposing joint membrane or segment. The number of deflected hairs and the degree of deflection causes mechanosensory activity that encodes the joint angle and, possibly, joint angle velocity. The encoding properties of antennal hair fields have been nicely demonstrated for the cockroach antenna.
Hair fields at the antennal joints are sometimes referred to as Böhm's bristles or Böhm's organ. This is a relict from a time when sensory organs were named after the person who first described them. In this case, Böhm (1911) described tactile hairs on the antenna of the moth Macroglossum stellatarum, although not all of these hairs belong to what we call hair field today.
Hair fields come in two kinds: hair plates are patches and hair rows are rows of hairs. It is not known whether these subtypes differ functionally. In the stick insect C. morosus there are seven antennal hair fields (Fig. 8), three on the scape (monitoring the HS-joint) and four on the pedicel (monitoring the SP-joint). For a detailed description and revision see Urvoy et al. (1984) and Krause et al. (2013). Ablation of all antennal hair fields severely impairs the inter-joint coordination of antennal movement and leads to an enlargement of the working-range. In particular, the hair plate on the dorsal side of the scape appears to be involved in the control of the upper turning point of antennal movement (Krause et al., 2013).
The properties of hair field afferents are unknown for the stick insect antenna, but it is not unlikely that their encoding properties are similar to those of cockroach hair plate afferents (Okada and Toh, 2001). This is supported by a recent characterisation of descending interneurons, where some groups were shown to convey antennal mechanoreceptive information reminiscent of what has been described for the cockroach hair plates (Ache and Dürr, 2013). Indeed, the terminals of hair field afferents arborize in close vicinity to the dendrites of two motion-sensitive descending interneurons in the suboesophageal ganglion (Ache et al., 2015). Assuming that hair field afferents drive at least part of the observed activity in descending interneurons in stick insects, they may provide an important input to the coordinate transfer that is necessary for tactually induced reaching movements as observed by Schütz and Dürr (2011). In order to execute such aimed leg movements, the motor centres in the thorax that control leg movement need to be informed about the spatial coordinates of the antennal contact site, and antennal pointing direction encoded by descending interneurons may be part of that.
Contact site (Tactile hairs)
The flagellum of an adult stick insect carries thousands of sensilla or sensory hairs (Weide, 1960), and several different sensilla types have been described (Slifer, 1966), some of which can only be distinguished electronmicroscopically. According to (Monteforti et al. (2002), the flagellum carries seven types of hair-shaped sensilla. Two types are innervated by a mechanosensory neuron, the other five are purely chemoreceptive sensilla. As a consequence, there are two kinds of mechanoreceptive tactile hairs on the flagellum that may encode touch location. Assuming that the occurrence of spikes in any given mechanoreceptor afferent would code for a certain distance along the flagellum, the identity of active afferents would encode the size, location and, potentially, the structure of the contacted surface. As yet, to date, nobody has recorded the afferent activity of a population of antennal touch receptors to verify this idea.
What is known is that sensilla density (irrespective of their morphological type) increases towards the tip. Moreover, sensilla density decreases during development, because sensilla number increases less than the surface area of the flagellum (Weide, 1960; for a graphical presentation of his data, see Fig. 9).
Bending (Campaniform sensilla)
Campaniform sensilla are coffee-bean-shaped structures that are embedded within the cuticle. Essentially, they serve as strain sensors. Depending on their location in the exoskeleton they may encode different kind of information. Quite often, they are found at the base of a long body segment, an ideal location for sensing shear forces induced by bending of the segment: If the tip of the segment is deflected, the long segment acts like a lever that increases the torque acting on the base of the structure. On the insect antenna, a prominent site for campaniform sensilla is the distal pedicel. Given the long flagellum that is "held" by the pedicel, bending of the flagellum exerts a torque at the pedicel-flagellum junction that can be picked up by the strain sensors embedded in the cuticle of the distal pedicel (remember that this junction is not a true joint as it is not actuated and has little slack.
The ring of campaniform sensilla at the distal pedicel is sometimes called Hicks' organ, a similar relict as mentioned above for the hair fields: Hicks described this structure for the locust antenna (Hicks, 1857). More than a century later, Heinzel and Gewecke, (1979) recorded the activity of Hicks' organ afferents in the antenna of the locust Locusta migratoria. They found a strong directional selectivity of the sensilla, depending on their location within the ring around the pedicel. This property makes Hicks' organ very suitable for encoding bending direction of the flagellum. In locusts this is thought to be important for measuring air flow direction and speed during flight.
In stick insects, campaniform sensilla can be found on the distal pedicel, too (see enlargement in Fig. 10, top right), but there they are much less pronounced than in the locust. Moreover, campaniform sensilla are sparsely distributed along the flagellum of C. morosus (Urvoy et al., 1984).
Vibration (Johnston’s organ)
Finally, there is at least one chordotonal organ in the pedicel of an insect antenna. As in the cases mentioned above, a historical relict determines the naming of this organ until today: Johnston's organ originally referred to a conspicuous swelling at the base of the mosquito antenna (Johnston, 1855) which was later described in more detail by Child (1894). Eggers (1924) then correctly placed Johnston's organ in the group of sensory organs containing so-called scolopidia, small rod-like structures that are characteristic of all chordotonal organs.
In several insect species, most importantly in mosquitoes, fruit flies and bees, Johnston's organ is known to be an auditory organ that can pick up vibrations generated by the wing beat (in mosquitoes and flies) or whole-body movements (in bees) of a conspecific Staudacher et al. (2005). Therefore, they serve intraspecific communication by means of sound.
In the stick insect C. morosus, there is a large chordotonal organ in the ventral part of the pedicel. Other than the 'classical' Johnston's organ of the mosquito, it does not attach to the entire ring of the pedicel-flagellum junction. Instead, all scolopidial cells appear to attach at a single cuticular indentation. This dent is formed by the sclerotised ventral cuticle of the pedicel. It can be seen from the outside, as on the SEM of pedicel-flagellum junction in Fig. 10, top right (there, the ventral side is pointing upwards). The flagellar cuticle forms two sclerotised brace-like structures that surround the dent. Both the dent and the brace are embedded in soft endocuticle. The function of this structure is unknown but the focal attachment of the chordotonal organ at a single point (see schematic in Fig. 10, bottom) indicates that it is not equally sensitive in all directions.
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