Insects typically have three pairs of legs, one pair on each of the thoracic segments. From this, the alternative name for insects, the ‘hexapods’, is derived, although not all hexapods are now regarded as insects.
8.1 BA S I C S T RU C T U R E O F T H E L E G S
Each leg consists typically of six segments, articulating with each other by mono- or di-condylic articulations set in a membrane, the corium. The six basic segments are coxa, trochanter, femur, tibia, tarsus and pretarsus (Fig. 8.1a).
The coxa is often in the form of a truncated cone and articulates basally with the wall of the thorax. There may be only a single articulation with the pleuron (Fig. 8.2a), in which case movement of the coxa is very free, but fre-quently there is a second articulation with the trochantin (Fig. 8.2b). This restricts movement to some extent, but, because the trochantin is flexibly joined to the episternum, the coxa is still relatively mobile. In some higher forms there are rigid pleural and sternal articulations limiting movement of the coxa to rotation about these two points (Fig. 8.2c). In the Lepidoptera the coxae of the middle and hind legs are fused with the thorax and this is also true of the hind coxae in Adephaga.
The part of the coxa bearing the articulations is often strengthened by a ridge indicated externally by the basi-costal sulcus which marks off the basal part of the coxa as the basicoxite (Fig. 8.3a). The basicoxite is divided into anterior and posterior parts by a ridge strengthening the articulation, the posterior part being called the meron.
This is very large in Neuroptera, Mecoptera, Trichoptera and Lepidoptera (Fig. 8.3b), while in the higher Diptera it becomes separated from the coxa altogether and forms a part of the wall of the thorax.
The trochanter is a small segment with a dicondylic articulation with the coxa such that it can only move in the vertical plane (Fig. 8.1b). In Odonata there are two trochanters and this also appears to be the case in Hymenoptera, but here the apparent second trochanter is, in fact, a part of the femur.
The femur is often small in larval insects, but in most adults it is the largest and stoutest part of the leg. It is often more or lessfixed to the trochanter and moves with it. In this case, there are no muscles moving the femur with respect to the trochanter, but sometimes a single muscle arising in the trochanter is able to produce a slight backward movement, or reduction, of the femur (Fig.
8.5b).
The tibia is the long shank of the leg articulating with the femur by a dicondylic joint so that it moves in a vertical plane (Fig. 8.1c,d). In most insects, the head of the tibia is bent so that the shank can flex right back against the femur (Fig. 8.1a). The tarsus, in most insects, is subdivided into from two to five tarsomeres. These are differentiated from true segments by the absence of muscles. The basal tar-somere, or basitarsus, articulates with the distal end of the tibia by a single condyle (Fig. 8.1e), but between the tar-someres there is no articulation; they are connected by flexible membrane so that they are freely movable. In Protura, some Collembola and the larvae of most holometabolous insects, the tarsus is unsegmented (Fig.
8.4c) or, in the latter, may be fused with the tibia.
The pretarsus, in the majority of insects, consists of a membranous base supporting a median lobe, the arolium, which may be membranous or partly sclerotized, and a pair of claws which articulate with a median process of the last tarsomere known as the unguifer. Ventrally there is a basal sclerotized plate, the unguitractor, and between this and the claws are small plates called auxiliae (Fig. 8.4a). In Diptera, a membranous pulvillus arises from the base of each auxilia while a median empodium, which may be spine- or lobe-like, arises from the unguitractor (Fig.
8.4b). There is no arolium in Diptera other than Tipulidae. The development of the claws varies in different insect groups. Commonly they are more or less equally well-developed, but in Thysanoptera they are minute and the pretarsus consists largely of the bladder-like arolium. In other groups, the claws develop unequally; one may fail to develop altogether, so that in Ischnocera, for instance, there is only a single claw. In
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Protura, some Collembola and many holometabolous larvae the entire pretarsus consists of a single claw-like segment (Fig. 8.4c).
8.1.1Muscles of the legs
The muscles which move the legs fall into two categories:
extrinsic, arising outside the leg, and intrinsic, wholly within the leg and running from one segment to another.
The coxa is moved by extrinsic muscles arising in the
thorax and a fairly typical arrangement is shown in Fig.
8.5a with promotor and remotor muscles arising on the tergum, abductor and adductor muscles from the pleuron and sternum, and rotator muscles also from the sternum (see section 8.4.1.1. for definitions). The roles of the muscles vary, depending on the activities of other muscles and also on the type of articulation. In Apis (Hymenoptera), which has rigid pleural and sternal articulations, promotor and remotor muscles from the Fig.8.1.Leg and articulations. Points of articulation shown by bold arrows (mainly after Snodgrass, 1935, 1952). (a) Typical insect leg. (b) Dicondylic articulation of trochanter with coxa and the apodemes of muscles moving the trochanter. Notice that the femur is united with the trochanter; there is no moving joint. (c), (d) dicondylic articulation of tibia and femur, (c) side view, (d) end view. (e) Monocondylic, ball articulation of tarsus with tibia.
coxa
trochanter
femur
tibia
tarsus
pretarsus a)
proximal end of femur
trochanter apodemes of
levator muscles
apodemes of depressor muscles
b)
articulation with coxa
distal end of femur
proximal end of tibia extensor
muscle
flexor muscle c)
distal end of femur
proximal end of tibia d)
apodeme of levator muscle
apodeme of depressor muscle
e)
basitarsus articulation
with tibia
BA S I C S T RU C T U R E O F T H E L E G S 153
Fig.8.2.Three types of coxal articulation with the thorax. Points of articulation shown by arrows. Membranous regions stippled (after Snodgrass, 1935).
pleural sulcus pleural
articulation
trochantin trochantinal articulation coxa
episternum
epimeron
sternal articulation sternum
anterior
pleural articulation flexible
connection
a) b) c)
Fig.8.3.Coxa, oblique lateral view (after Snodgrass, 1935): (a) typical
insect ; (b) coxa with a large meron. basicostal
ridge pleural
articulation
basicoxite basicostal sulcus coxal
sulcus
articulations with trochanter
meron
a) b)
membrane
Fig.8.4.Pretarsus. (a) Pretarsus of Periplaneta, ventral view (after Snodgrass, 1935). (b) Pretarsus of a dipteran, ventral view (after Snodgrass, 1935). (c) Distal part of prothoracic leg of larval Triaenodes (Trichoptera) showing a simple pretarsal segment (after Tindall, 1964).
femur
tibia
tarsus
pretarsus spur
tarsal depressor muscle
pretarsal depressor muscles c) Triaenodes
a) Periplaneta
arolium claw
auxilia unguitractor
apodeme for attachment of pretarsal depressor
muscle distal tarsomere
auxilia b) Diptera
claw empodium
pulvillus
unguitractor distal tarsomere
tergum are absent. In the pterothoracic segments, muscles (insertions marked with oblique hatching in Fig. 8.5a) run from the coxae to the basalar and subalar sclerites. They are concerned with movements of the wings as well as the legs.
The intrinsic musculature is much simpler than the coxal musculature, consisting typically only of pairs of antagonistic muscles in each segment (Fig. 8.5b). In Periplaneta, there are three levator muscles of the trochanter arising in the coxa and three depressor muscles, two again with origins in the coxa and a third arising on the pleural ridge and the tergum.
The femur is usually immovably attached to the
trochanter, but the tibia is moved by extensor and flexor muscles arising in the femur and inserted into apodemes from the membrane at the base of the tibia (see Fig. 8.21a).
Levator and depressor muscles of the tarsus arise in the tibia and are inserted into the proximal end of the basitar-sus, but there are no muscles within the tarsus moving the tarsomeres.
It is characteristic of the insects that the pretarsus has a depressor muscle, but no levator muscle. The fibers of the depressor occur in small groups in the femur and tibia and are inserted into a long apodeme which arises on the unguitractor (Figs. 8.5b, 8.21a). Levation of the pretarsus results from the elasticity of its basal parts.
Fig.8.5.Leg muscles. (a) Extrinsic muscles of coxa as seen from the midline of the insect. Muscles arising from the areas marked with diagonal hatching are omitted (from Snodgrass, 1935). (b) Intrinsic muscles. Note that one trochanter depressor muscle is extrinsic (after Snodgrass, 1927).
Innervation of the musclesThe innervation of the leg muscles is complex. Most muscles are innervated by both fast and slow axons and by inhibitory axons (section 10.1.5), but not all the fibers within a muscle are inner-vated by all three types of motor neuron. For example, in Periplaneta, each of the meso- and metathoracic coxae has four muscles which depress the trochanter (Fig. 8.6). Two of these, 136 and 137, are innervated only by a fast axon which also goes to parts of the other two muscles, 135d´, 135e´. These parts are also innervated by a slow axon, which also supplies other parts of these muscles, 135d and e, which have no fast nerve supply. In addition, three inhibitory fibers innervate these parts of the muscles;
inhibitory fibers do not run to parts of the muscles that receive input from the fast axon.
The extensor tibiae muscle in the hind leg of a grass-hopper has an even more complex supply. In addition to fast, slow and inhibitory axons, it receives input from an axon which releases the neuromodulator, octopamine (section 10.3.2.4). This axon is called the dorsal unpaired median axon of the extensor tibiae muscle (DUMETi). A majority offibers are innervated only by the fast axon, but this is probably not a general feature of leg muscles as the extensor tibiae muscle of grasshoppers is specialized for jumping.
Nearly all the muscles moving the coxa, trochanter and tibia in each leg of a locust are innervated by the same
inhibitory neuron which is consequently known as the common inhibitor (see Fig. 10.9). Two other inhibitory neurons innervate the muscles of the distal parts of the legs, both running to the same muscles.
8.1.2 Sensory system of the legs
The legs of insects have an extensive sensory system. Some of the sensory elements are proprioceptors, monitoring the positions of the leg segments and the stance of the insect.
Other mechanoreceptors and chemoreceptors are involved in the perception of environmental stimuli.
Review: Seelinger & Tobin, 1981 – cockroach
8.1.2.1 Proprioceptors
The proprioceptors include hair plates and campaniform sensilla (section 23.1.3.2) and chordotonal organs (section 23.2.1). Periplaneta has hair plates at the proximal end of the coxa and also at the coxa–trochanter joint (Fig. 8.7a).
There are groups of campaniform sensilla on the trochanter, a group proximally on the femur and another on the tibia, and a small number on the dorsal surface at the distal end of each tarsomere. In total, there are about 140 sensilla in hair plates and 80 campaniform sensilla on each front leg. The other legs have similar numbers. In addition, Periplaneta has a chordotonal organ associated with each joint of the leg, and multipolar neurons at the trochanter-femur and femur–tibia joints. There may also be strand receptors like those described in the locust (section 23.3.2). Similar arrangements of proprioceptors occur on the legs of the migratory locust, Locusta (Field &
Pflüger, 1989; Hustert, Pflüger & Bräunig, 1981), the stick insect, Carausius (Bässler, 1983), and the adult tobacco hornworm, Manduca (Kent & Griffin, 1990).
8.1.2.2 Exteroceptors
Many exteroreceptive sensilla are also present on the legs.
Mechanosensitive trichoid sensilla are distributed all over the legs, and the final larval stage of the grasshopper, Schistocerca americana, has about 140 of these sensilla on each tarsus (Fig. 8.7b); others are present on the femur and tibia. The axons from the sensilla in different areas of the leg converge to separate interneurons so that spatial information is maintained within the central nervous system (Fig. 20.24). This is true not only of the first order spiking local interneurons, but also of non-spiking inter-neurons and spiking intersegmental inter-neurons (see Fig.
8.20) (Burrows, 1989). This ensures that the insect
BA S I C S T RU C T U R E O F T H E L E G S 155
Fig.8.6.Muscle innervation. Diagrammatic representation of the motor neurons to the depressor muscles of the trochanter in the mesothoracic coxa of Periplaneta. Muscle units are numbered as in the text (after Pearson & Iles, 1971).
inhibitory axons slow axon
fast axon
136 135d' 135d 135e 135e' 137
inhibitory synapse excitatory synapse
responds in an appropriate manner when a particular part of a leg is touched.
In addition, each leg has many contact chemo-receptors. S.americana has about 200 on the upper surface of the tarsus and over 100 on the pulvillar pads on which the insect normally stands (Fig. 8.7b). Although some contact chemoreceptors may be present on the femur and tibia, most are on the tarsus. Tarsal chemoreceptors are of general occurrence in hemimetabolous insects and adult holometabolous insects, but there is no evidence that they occur on the legs of holometabolous larvae. The thoracic legs of caterpillars possess only small numbers of mechanosensitive hairs. Most insects also have a sub-genual organ, sensitive to substrate vibration (section 23.2.3.1).
Review: Chapman, 1982 – chemoreceptors
8.1.3Adhesion
Many insects are able to climb and hold on to smooth sur-faces. Different insects use different structures and proba-bly different mechanisms for adhesion, but many use adhesive setae, also sometimes called tenent hairs. These setae are grouped together to form adhesive pads which occur on various parts of the legs. Rhodnius and some other Reduviidae have adhesive pads at the distal ends of the tibiae of the front and middle legs. Amongst the flies, the pulvilli have adhesive properties, and many beetles have pads of setae on the underside of the tarsomeres. In each of these cases the adhesive structures are areas of membra-nous cuticle covered by large numbers of small setae. For example in the lady beetle, Epilachna, there are two pads on the underside of each tarsus. Each pad carries about 800 setae which are 70–120m long. Many of the setae are expanded at the tip to formflattened, foot-like structures 5–10m in diameter (Fig. 8.8a). In the fly, Calliphora, the adhesive setae are also on the tarsi. They are much smaller than those in the beetle, only 9–15m high with a ‘foot’
about 1m in diameter. The fly has about 42 000 adhesive hairs altogether. The flexibility of the setae enables them to make contact with irregular surfaces much more efficiently than would be true of a single, larger structure. This greatly increases the power of adhesion. The males of many species of beetle have more adhesive setae than the females. These additional setae are used by the male to grasp the female during mating.
Hairless adhesive pads occur in a number of insects.
The arolia of cockroaches and grasshoppers can function Fig.8.7.Sensory system of the leg. (a) Proprioceptors on the
foreleg of Periplaneta. Numbers in brackets show the number of sensilla in each group. Ellipses show orientations of campaniform sensilla. (b) Exteroreceptors on the fore tarsus of the
grasshopper, Schistocerca americana. Posterior view: there are 140 long mechanosensitive sensilla and 200 small chemosensitive sensilla on the upper surface and sides of the tarsus. Ventral view:
sensilla on the pulvilli and arolium. There are 180 sensilla. About 60% are chemoreceptors.
as adhesive organs, and in the latter group they are bigger in habitually climbing species. Some aphids have an ever-sible pulvillus at the tibio-tarsal articulation and plant-hoppers have a pair of pulvillus-like pads on the pretarsus which function as adhesive organs.
Adhesion is the result of surface tension of a fluid at the tips of the hairs or on the pads. It contains lipoproteins and is produced by gland cells closely associated with the adhesive organs, probably reaching the surface of the cuticle through wax canals. In many beetles, however, there is no evidence offluid and it is possible that adhesion results from molecular forces operating when the two sur-faces, substrate and tips of the adhesive setae, are very closely applied together (Lees & Hardie, 1988; Stork, 1983).
The pulling force exerted by several of these insects when walking vertically up a pane of glass is often well in excess of 10 times the insect’s own body mass.
In male dytiscid beetles a different mechanism of adhe-sion occurs. The first three tarsomeres of the foreleg of male Dytiscus are enlarged to form a circular disc. On the inside, this disc is set with stalked cuticular cups, most of which are only about 0.1 mm in diameter, but two of which are much larger than the rest, one being about 1 mm across (Fig. 8.8b). It seems that these cups act as true suckers, although it is not certain how the suction is created. The suckers are used by the male to grasp the female, but may also be used occasionally to grasp prey.
8.2 M O D I F I C AT I O N S O F T H E BA S I C L E G S T RU C T U R E
The basic insect walking leg may be modified in various ways to serve a number of functions. Amongst these are jumping, swimming, digging, grasping, grooming and stridulation. Modifications associated with jumping and swimming are considered in sections 8.4.2.1. and 8.5.2.2.
Digging Legs modified for digging are best known in the Scarabaeoidea and the mole cricket, Gryllotalpa. In Gryllotalpa, the forelimb is very short and broad, the tibia and tarsomeres bearing stout lobes which are used in excavation. In the scarab beetles, the femora are short, the tibiae are again strong and toothed, but the tarsi are often weakly developed. Larval cicadas are also burrowing insects. They have large, toothed fore femora, the principal digging organs, and strong tibiae which may serve to loosen the soil (Fig. 8.9a). The tarsus is inserted dorsally on the tibia and can fold back. In the first stage larva it is three-segmented, but it becomes reduced in later instars and may disappear completely.
Grasping Modifications of the legs for grasping are fre-quent in predatory insects. Often pincers are formed by the apposition of the tibia on the femur. This occurs in the forelegs of mantids (see Fig. 2.9) and mantispids (Neuroptera), in some Heteroptera such as Phymatidae and Nepidae, and in some Empididae and Ephydridae M O D I F I C AT I O N S O F T H E BA S I C L E G S T RU C T U R E 157
Fig.8.8.Adhesive pads. (a) Tip of tenent hair of Philonthus (Coleoptera, Staphylinidae) (after Stork, 1983). (b) Suckers on the foreleg of male Dytiscus (Coleoptera, Dytiscidae) (after Miall, 1922).
amongst the Diptera. In some Empididae the middle legs are modified in this way, while in Bittacus (Mecoptera) the fifth tarsomere on all the legs closes back against the fourth to form a grasping structure.
The ability to hold on is important in ectoparasitic insects. These usually have well-developed claws and the legs are frequently stout and short as in Hippoboscidae, Ischnocera and Anoplura. In the latter two groups, the tarsi are only one or two segmented and often there is only a single claw which folds against a projection of the tibia to form a grasping organ (Fig. 8.9b).
GroomingInsects commonly use the legs or mandibles to groom parts of the body, removing particles of detritus in the process. The eyes and antennae are often groomed, and so are the wings. Cockroaches clean their antennae by passing them through the mandibles, which chew lightly at the surface, but many insects use the forelegs for this purpose, then cleaning the legs with the mandibles. Neuroptera and Diptera hold an antenna between the two forelegs, which are drawn forwards together towards its tip. Mosquitoes have a comb,
GroomingInsects commonly use the legs or mandibles to groom parts of the body, removing particles of detritus in the process. The eyes and antennae are often groomed, and so are the wings. Cockroaches clean their antennae by passing them through the mandibles, which chew lightly at the surface, but many insects use the forelegs for this purpose, then cleaning the legs with the mandibles. Neuroptera and Diptera hold an antenna between the two forelegs, which are drawn forwards together towards its tip. Mosquitoes have a comb,