Entomology 3rd edition - C.Gillott - Chapter 14 ppt

Muscles Essentially, the structure and contractile mechanism of insect muscles are comparable to those of vertebrate skeletal cross-striated muscle; that is, there are no muscles in inse

in a variety of ways or run on the water surface.

In their locomotory movements, insects conform to normal dynamic and mechanicalprinciples However, their generally small size and light weight have led to the development

of some unique structural, physiological, and biochemical features in their locomotorysystems

2 Muscles

Essentially, the structure and contractile mechanism of insect muscles are comparable

to those of vertebrate skeletal (cross-striated) muscle; that is, there are no muscles in insects

of the smooth (non-striated) type Within muscle cells, the contractile elements actin andmyosin have been identified, and Huxley’s sliding filament theory of muscle contractionapplies Though insect muscles are always cross-striated, there is considerable variation intheir structure, biochemistry, and neural control, in accord with specific functions

Because of their small size and the variable composition of the hemolymph of insects,the neuromuscular system has some unique features (Hoyle, 1974) Being small, an insecthas a limited space for muscles which are, accordingly, reduced in size Though this isachieved to some extent by a decrease in the size of individual cells (fibers), the principalchange has been a decline in the number of fibers per muscle such that some insect musclescomprise only one or two cells Thus, to achieve a graded muscle contraction, each fiber must

be capable of a variable response, in contrast to the vertebrate situation where graded muscleresponses result in part from stimulation of a varied number of fibers Similarly, the volume

of nervous tissue is limited, so that there are few motor neurons for the control of muscle

437

CHAPTER 14

contraction The hemolymph surrounding muscles may contain high concentrations of ions(especially divalent ions such as Mg2+) (Chapter 17, Section 4.1.1) that could interfere withimpulse transmission at synapses and neuromuscular junctions That this does not occur isthe result of the evolution of a myelin sheath that covers ganglia, nerves, and neuromuscularjunctions

2.1 Structure

Insect muscles can be arranged in two categories: (1) skeletal muscles whose function

is to move one part of the skeleton in relation to another, the two parts being separated by ajoint of some kind, and (2) visceral muscles, which form layers of tissue enveloping internalorgans such as the heart, gut, and reproductive tract

Attachment of a muscle to the integument must take into account the fact that ically the remains of the old cuticle are shed; therefore, an insertion must be able to breakand re-form easily As Figure 14.1 indicates, a muscle terminates at the basal lamina lyingbeneath the epidermis The muscle cells and epidermal cells interdigitate, increasing thesurface area for attachment by about 10 times, and desmosomes occur at intervals, replac-ing the basal lamina Attachment of a muscle cell to the rigid cuticle is achieved throughlarge numbers of parallel microtubules (called “tonofibrillae” by earlier authors) Distally,the epidermal cell membrane is invaginated, forming numbers of conical hemidesmosomes

period-on which the microtubules terminate Running distad from each hemidesmosome is period-one,rarely two, muscle attachment fibers (= tonofibrils) Each fiber passes along a pore canal

FIGURE 14.1. Muscle insertion [After A C Neville,

1975, Biology of the Arthropod Cuticle By permission

of Springer-Verlag, New York.]

439 MUSCLES AND LOCOMOTION

to the cuticulin envelope of the epicuticle to which they are attached by a special cement

As the cuticulin layer is the first one formed during production of a new cuticle (Chapter

11, Section 3.1), attachment of newly formed fibers can readily occur Until the actual molt,

however, these are continuous with the old fibers and, therefore, normal muscle contraction

is possible (Neville, 1975)

Muscles comprise a varied number of elongate, multinucleated cells (fibers) (not to

be confused with the muscle attachment fibers mentioned above) that may extend along

the length of a muscle A muscle is arranged usually in units of 10–20 fibers, each unit

being separated from the others by a tracheolated membrane Each unit has a separate nerve

supply The cytoplasm (sarcoplasm) of each fiber contains a varied number of mitochondria

(sarcosomes) Even at the light microscope level, the transversely striated nature of muscles

is visible Higher magnification reveals that each fiber contains a large number of myofibrils

(= fibrillae = sarcostyles) lying parallel in the sarcoplasm and extending the length of the

cell Each myofibril comprises the contractile filaments, made up primarily of two proteins,

actin and myosin The thicker myosin filaments are surrounded by the thinner but more

numerous actin filaments Filaments of each myofibril within a cell tend to be aligned, and

it is this that creates the striated appearance (alternating light and dark bands) of the cell The

dark bands (A bands) correspond to regions where the actin and myosin overlap, whereas

the lighter bands indicate regions where there is only actin (I bands) or myosin (H bands)

(Figure 14.2) Electron microscopy has revealed in addition to these bands a number of thin

transverse structures in the muscle fiber Each of these Z lines (discs) runs across the fiber

in the center of the I bands, separating individual contractile segments called sarcomeres

Attached to each side of the Z line are the actin filaments, which in contracted muscle are

FIGURE 14.2. Details of a muscle fiber [After R F Chapman, 1971, The Insects: Structure and Function By

permission of Elsevier/North-Holland, Inc., and the author.]

CHAPTER 14

connected to the myosin filaments by a means of cross bridges present at each end of themyosin Periodically, the plasma membrane (sarcolemma) of the muscle fiber is deeplyinvaginated and forms the so-called T system (transverse system) In most insect musclesthe T system occurs midway between the Z line and H band; in fibrillar muscles, however,there is no regular pattern for the position of the invaginations

Though the above description is applicable to all insect muscles, different types ofmuscles can be distinguished, primarily on the basis of the arrangement of myofibrils,mitochondria, and nuclei; the degree of separation of the myofibrils; the degree of devel-opment of the sarcoplasmic reticulum; and the number of actins surrounding each myosin(Figure 14.3) These include tubular (lamellar), close-packed, and fibrillar muscles, all ofwhich are skeletal, and visceral muscles

Leg and segmental muscles of many adult insects and the flight muscles of primitivefliers, such as Odonata and Dictyoptera, are of the tubular type, in which the flattened(lamellate) myofibrils are arranged radially around the central sarcoplasm The nuclei aredistributed within the core of sarcoplasm and the slablike mitochondria are interspersed

FIGURE 14.3. Transverse sections of insect skeletal muscles (A) Tubular leg muscle of Vespa (Hymenoptera); (B) tubular flight muscle of Enallagma (Odonata); (C) close-packed flight muscle of a butterfly; and (D) fibrillar flight muscle of Tenebrio (Coleoptera) (Not to same scale.) [A, after H E Jordan, 1920, Studies on striped muscle

structure VI, Am J Anat 27:1–66 By permission of Wistar Press B, C, redrawn from electron micrographs

in D S Smith, 1965, The flight muscles of insects, Scientific American, June 1965, W H Freeman and Co By

permission of the author D, redrawn from an electron micrograph in D S Smith, 1961, The structure of insect

fibrillar muscles A study made with special reference to the membrane systems of the fiber, J Biophys Biochem.

Cytol 10:123–158 By permission of the Rockefeller Institute Press and the author.]

441 MUSCLES AND LOCOMOTION

between the myofibrils The body musculature of apterygotes and some larval pterygotes, the

leg muscles of some adult pterygotes, and the flight muscles of Orthoptera and Lepidoptera

are of the close-packed type Here the myofibrils and mitochondria are concentrated in the

center of the fiber and the nuclei are arranged peripherally In close-packed flight muscles,

the fibers are considerably larger than those of tubular flight muscles In addition, tracheoles

deeply indent the fiber, whereas in tubular muscles tracheoles simply lie alongside each

fiber It should be appreciated that the tracheoles do not actually penetrate the muscle

cell membrane, that is, they are extracellular In most insects the indirect muscles, which

provide the power for flight, are nearly always fibrillar, so-called because individual fibrils

are characteristically very large and, together with the massive mitochondria, occupy almost

all of the volume of the fiber Very little sarcoplasm is present, and the nuclei are squeezed

randomly between the fibrils Because of their size, there are often only a few fibrils per

cell, and these are frequently quite isolated from each other by the massively indented and

intertwining system of tracheoles The presence of large quantities of cytochromes in the

mitochondria gives these muscles a characteristic pink or yellow color It should be apparent

even from this brief description that fibrillar muscles are designed to facilitate a high rate

of aerobic respiration in connection with the energetics of flight

Visceral muscles differ from skeletal muscles in several ways The cells comprising

them are uninucleate, may branch, and are joined to adjacent cells by septate desmosomes

Their contractile elements are not arranged in fibrils and contain a larger proportion of actin

to myosin Nevertheless, the visceral muscles are striated (sometimes only weakly), and

their method of contraction is apparently identical to that of skeletal muscles

All skeletal muscles and many visceral muscles are innervated The skeletal muscles

always receive nerves from the central nervous system, whereas the visceral muscles are

innervated from either the stomatogastric or the central nervous system Within a particular

muscle unit, each fiber may be innervated by one, two, or three functionally distinct axons

One of these is always excitatory; where two occur (the commonest arrangement), they

are usually both excitatory (“fast” and “slow” axons), but may be a “slow” excitatory axon

plus an inhibitory axon; in some cases all three types of axon occur This arrangement,

known as polyneuronal innervation, facilitates a variable response on the part of a muscle

(Section 2.2) Each axon, regardless of its function, is much branched and, in contrast to

the situation in vertebrate muscle, there are several motor neuron endings from each axon

on each muscle fiber (multiterminal innervation) (Figure 14.4)

2.2 Physiology

Like those of vertebrates, insect muscles contract according to the sliding filament

theory The arrival of an excitatory nerve impulse at a neuromuscular junction causes

depo-larization of the adjacent sarcolemma A wave of depodepo-larization spreads over the fiber and

into the interior of the cell via the T system Depolarization of the T system membranes

induces a momentary increase in the permeability of the adjacent sarcoplasmic reticulum,

so that calcium ions, stored in vesicles of the reticulum, are released into the sarcoplasm

surrounding the myofibrils The calcium ions activate cross-bridge formation between the

actin and myosin, enabling the filaments to slide over each other so that the distance between

adjacent Z lines is decreased The net effect is for the muscle to contract Energy derived

from the hydrolysis of adenosine triphosphate (ATP) is required for contraction, though

its precise function is unknown It may be used in breaking the cross-bridges, or for the

active transport of the calcium ions back into the vesicles, or for both of these processes In

CHAPTER 14

FIGURE 14.4. Polyneuronal and nal innervation of an insect muscle [After G Hoyle, 1974, Neural control of skeletal mus-

multitermi-cle, in: The Physiology of Insecta, 2nd ed., Vol.

IV (M Rockstein, ed.) By permission of demic Press, Inc., and the author.]

Aca-addition to sliding over each other, both the actin and the myosin filaments may shorten (bycoiling), and in some myofibrils the Z lines disintegrate to allow the A bands of adjacentsarcomeres to overlap each other, thus enabling an even greater degree of contraction tooccur

Extension (relaxation) of a muscle may result simply from the opposing elasticity ofthe cuticle to which the muscle is attached More commonly, muscles occur in pairs, eachmember of the pair working antagonistically to the other; that is, as one muscle is stimulated

to contract, its partner (unstimulated) is stretched Normally, the previously unstimulatedmuscle is stimulated to begin contraction while active contraction of the partner is stilloccurring (cocontraction) This is thought to bring about dampening of contraction, perhapsthereby preventing damage to a vigorously contracting muscle Also, in slow movements,

it provides an insect with a means of precisely controlling such movements (Hoyle, 1974).Muscle antagonism is achieved by central inhibition, that is, at the level of interneuronswithin the central nervous system (Chapter 13, Section 2.3) Thus, for a given stimulus,the passage of impulses along an axon to one muscle of the pair will be permitted, andhence that muscle will contract However, passage of impulses to the partner is inhibitedand the muscle will be passively stretched It should be emphasized that in this arrangementthe axon to each muscle is excitatory In slow walking movements, for example, alternatingstimulation of each muscle is quite distinct At higher speeds this reciprocal inhibitionbreaks down, and one of the muscles remains permanently in a mildly contracted state,serving as an “elastic restoring element” (Hoyle, 1974) The other muscle continues to bealternately stimulated and thus provides the driving power for the activity

As noted earlier, commonly muscles receive two excitatory axons, one “slow,” the other

“fast.” These terms are somewhat misleading for they do not indicate the speed at whichimpulses travel along the axons, but rather the speed at which a significant contraction can

be observed in the muscle Thus, an impulse traveling along a fast axon induces a strong

443 MUSCLES AND LOCOMOTION

contraction of the “all or nothing” type; that is, a further contraction cannot be initiated until

the original ionic conditions have been restored In contrast, a single impulse from a slow

axon causes only a weak contraction in the muscle However, additional impulses arriving

in quick succession are additive in their effect (summation) so that, with the slow axon

arrangement a graded response is possible for a particular muscle, despite the relatively

few fibers it may contain Muscles with dual innervation use only the slow axon for most

requirements; the fast axon functions only when immediate and/or massive contraction is

necessary For example, the extensor tibia muscle of the hindleg of a grasshopper is ordinarily

controlled solely via the slow axon For jumping, however, the fast axon is brought into

play

The function of inhibitory axons remains questionable Electrophysiological work has

shown that in normal activity the inhibitory axon is electrically silent, that is, shows no

electrical activity, and is clearly being inhibited from within the central nervous system

During periods of great activity, impulses can sometimes be observed passing along the axon,

perhaps to accelerate muscle relaxation, though normally the use of antagonistic muscles

and central inhibition is adequate Hoyle (1974) suggested that peripheral inhibition may

be necessary at certain stages in the life cycle, such as molting, when central inhibition may

not be possible

3 Locomotion

3.1 Movement on or Through a Substrate

3.1.1 Walking

Insects can walk at almost imperceptibly slow speed (watch a mantis stalking its prey)

or run at seemingly very high rates (try to catch a cockroach) The latter is, however, a

wrong impression created by the smallness of the organism, the rate at which its legs move,

and the rate at which it can change direction Ants scurrying about on a hot summer day

are traveling only about 1.5 km/hr, and the elusive cockroach has a top speed of just under

5 km/hr (Hughes and Mill, 1974)

Nevertheless, an insect leg is structurally well adapted for locomotion Like the limbs of

other actively moving animals, it tapers toward the distal end, which is light and easily lifted

Its tarsal segments are equipped with claws or pulvilli that provide the necessary friction

between the limb and the substrate A leg comprises four main segments (Chapter 3, Section

4.3.1), which articulate with each other and with the body The coxa articulates proximally

with the thorax, usually by means of a dicondylic joint and distally, with the fused trochanter

and femur, also via a dicondylic joint Dicondylic joints permit movement in a single plane

However, the two joints are set at right angles to each other and, therefore, the tip of a leg

can move in three dimensions

The muscles that move a leg are both extrinsic (having one end inserted on the wall

of the thorax) and intrinsic (having both ends inserted within the leg) (Figure 14.5) The

majority of extrinsic muscles move the coxa, rarely the fused trochantofemoral segment,

whereas the paired intrinsic muscles move leg segments in relation to each other Some

of the extrinsic muscles have a dual function, serving to bring about both leg and wing

movements Typically, the leg muscles include (1) the coxal promotor and its antagonist, the

coxal remotor, which run from the tergum to the anterior and posterior edges, respectively,

CHAPTER 14

FIGURE 14.5. (A) Musculature of coxa; (B) segmental musculature of leg; and (C) musculature of hindleg of

grasshopper [A, C, from R E Snodgrass, Principles of Insect Morphology Copyright 1935 by McGraw-Hill,

Inc Used with permission of McGraw-Hill Book Company B, reproduced by permission of the Smithsonian

Institution Press from Smithsonian Miscellaneous Collections, Volume 80, Morphology and mechanism of theV insect thorax, Number 1, June 25, 1927, 108 pages, by R E Snodgrass: Figure 39, page 89 Washington, D.C.,

1928, Smithsonian Institution.]

of the coxa; contraction of the coxal promotor causes the coxa to twist forward, therebyeffecting protraction (a forward swing) of the entire leg; (2) the coxal adductor and abductor(attached to the sternum and pleuron, respectively), which move the coxa toward or awayfrom the body; (3) anterior and posterior coxal rotators, which arise on the sternum andassist in raising and moving the leg forward or backward; and (4) an extensor (levator)and flexor (depressor) muscle in each leg segment, which serve to increase and decrease,respectively, the angle between adjacent segments It should be noted that the muscles thatmove a particular leg segment are actually located in the next more proximal segment Forexample, the tibial extensor and flexor muscles, which alter the angle between the femurand tibia, are located within the femur and are attached by short tendons inserted at the head

of the tibia

It is the coordinated actions of the extrinsic and intrinsic muscles that move a legand propel an insect forward In considering how propulsion is achieved, it must also beremembered that another important function of a leg is to support the body, that is, to keep

445 MUSCLES AND LOCOMOTION

FIGURE 14.6. Magnitude of the longitudinal and lateral forces resulting from the strut effect for each leg in its

extreme position [After G M Hughes, 1952, The coordination of insect movements I The walking movements

of insects, J Exp Biol 29:267–284 By permission of Cambridge University Press, London.]

it off the ground In the latter situation, a leg may be considered as a single-segmented

structure—a rigid strut If the strut is vertical, the force along its length (axial force) will be

solely supporting and will have no propulsive component If the strut is inclined, the axial

force can be resolved into two components, a vertical supportive force and a horizontal

propulsive force Because the leg protrudes laterally from the body, the horizontal force can

be further resolved into a transverse force pushing the insect sideways and a longitudinal

force that causes backward or forward motion The relative sizes of these horizontal forces

depend on (1) which leg is being considered and (2) the position of that leg Figure 14.6

indicates the size of these forces for each leg at its two extreme positions It will be apparent

that in almost all of its positions the foreleg will inhibit forward movement, whereas the

mid- and hindlegs always promote forward movement In equilibrium, that is, when an

insect is standing still, the forces will be equal and opposite Movement of an insect’s body

will occur only if the center of gravity of the body falls This occurs when the forces become

imbalanced, for example, by changing the position of a foreleg so that its retarding effect

is no longer equal to the promoting effect of the other legs, whereupon the insect topples

forward (Hughes and Mill, 1974)

Also important from the point of view of locomotion is the leg’s ability to function as

a lever, that is, a solid bar that rotates about a fulcrum and on which work can be done

The fulcrum is the coxothoracic joint and the work is done by the large, extrinsic muscles

CHAPTER 14

Because of the large angle through which it can rotate and because of its angle to the body,the foreleg is most important as a lever In contrast, the mid- and hindlegs, which eachrotate through only a small angle, exert only a slight lever effect and serve primarily asstruts (in the fully extended, rigid position) For the foreleg in its fully protracted position,contraction of the retractor muscle (i.e., the lever effect) will be sufficient to overcome theopposing retarding (strut) effect and, provided that the frictional forces between the groundand tarsi are sufficient, the body will be moved forward

However, the largest component of the propulsive force is derived as a result of theleg’s ability to flex and extend by virtue of their jointed nature Flexure (a decrease in theangle between adjacent leg segments) will raise the leg off the ground so that it can bemoved forward without the need to overcome frictional forces between it and the ground

In the case of the foreleg, flexure first will remove, by lifting the leg from the ground, theretarding effect as a result of its action as a strut and, second, when the leg is replaced onthe substrate, will cause the body to be pulled forward Flexure of the foreleg continuesuntil the leg is perpendicular to the body, at which point extension begins so that now thebody is pushed forward For the mid- and hindlegs, flexure serves to bring the legs into anew forward position Extension, as in the case of the foreleg, will push the body forward.Because the hindleg is usually the largest of the three, it exerts the greatest propulsive force

As noted above, the horizontal axial force along each leg has a transverse as well as

a longitudinal component Thus, as an insect moves, its body zigzags slightly from side toside, the transverse forces exerted by the fore- and hindlegs of one side being balanced by

an opposite force exerted by the middle leg of the opposite side in the normal rhythm of legmovements

Rhythms of Leg Movements. Most insects use all six legs during normal walking.Other species habitually employ only the two anterior or the two posterior pairs of legs butmay use all legs at higher speeds In all instances, however, the legs are lifted in an orderlysequence (though this may vary with the speed of the insect), and there are always at leastthree points of contact with the substrate forming a “triangle of support” for the body (Insome species that employ two pairs of legs, the tip of the abdomen may serve as a point ofsupport.) Two other generalizations that may be made are (1) no leg is lifted until the legbehind has taken up a supporting position and (2) the legs of a segment alternate in theirmovements

In the typical hexapodal gait at low speed, only one leg at a time is raised off the ground,

so that the stepping sequence is R3, R2, Rl, L3, L2, Ll (where R and L are right and leftlegs, respectively, and 1, 2, and 3 indicate the fore-, mid-, and hindlegs, respectively) Withincrease in speed, overlap occurs between both sides so that the sequence first becomes R3

Ll, R2, Rl L3, L2, etc., and, then, R3 Rl L2, R2 L3 Ll, etc., that is, a true alternating tripodalgait

The orthopteran Rhipipteryx has a quadrupedal gait, using only the anterior two pairs

of legs and using the tip of the abdomen as a support Its stepping sequence is Rl L2, R2 LI.,etc Mantids are likewise quadrupedal at low speed, using the posterior two pairs of legs(sequence R3 L2, R2 L3, etc.) At high speed, the forelegs are brought into action thoughthe insects remain effectively quadrupedal (sequence Ll R3, L3 R2, L2 R1, etc.)

A variety of methods for turning have been observed, often in the same species Theyinclude increasing the length of the stride on the outside of the turn, increasing the frequency

of stepping on the outside of the turn, fixing one or more of the “inside” legs as pivots, andmoving the legs on the inside of the turn backward

Coordination of the movements both among segments of the same leg and amongdifferent legs requires a high level of neural activity, both sensory and motor Like other

447 MUSCLES AND LOCOMOTION

rhythmic activities, the walking rhythm is centrally generated; that is, the endogenous

activity of a network of neurons within each thoracic ganglion regulates the alternating

contraction of the leg flexor and extensor muscles, hence the flexion and extension of the

limb Intersegmental coordination of leg movements is achieved principally by “central

coupling,” that is, by signals traveling within the central nervous system from one network

to another Starting and stopping, turning, and change of speed are controlled by the brain

and subesophageal ganglion, via so-called “command neurons,” though how these centers

exert their control is unclear Superimposed on this central control is the input from the

insect’s sense organs, especially proprioceptors on the legs themselves, which permits the

insect to adjust its walking rhythm to compensate for changing environmental conditions

(See Chapter 13, Section 2.3)

3.1.2 Jumping

Jumping is especially well developed in grasshoppers, fleas, flea beetles, click beetles,

and Collembola In the first three mentioned groups, jumping involves the hindlegs, which,

like those of other jumping animals, are elongate and capable of great extension Their

length ensures that the limbs are in contact with the substrate for a long time during takeoff

Extension is achieved as the initially acute angle between the femur and tibia is increased

to more than 90◦by the time the tarsi leave the substrate The length and extension together

enable sufficient thrust to be developed that the insect can jump heights and distances many

times its body length For example, a fifth-instar locust (length about 4 cm) may “high

jump” 30 cm and, concurrently, “long jump” 70 cm

In Orthoptera the power for jumping is developed by the large extensor tibiae muscle

in the femur (Figure 14.5C) The muscle is arranged in two masses of tissue that arise on the

femur wall and are inserted obliquely on a long flat apodeme attached to the upper end of

the tibia The resultant herringbone arrangement increases the effective cross-sectional area

of muscle attached to the apodeme, thereby increasing the power that the muscle develops

As the extensor tibiae contracts, all activity ceases in the motoneurons running to its

antagonist, the flexor tibiae muscle, thus permitting all of the power developed to be used in

extending the tibia This inhibition results from the activity of a single, branched inhibitory

interneuron Because the apodeme is attached to the upper end of the tibia, slight contraction

of the extensor muscle will cause a relatively enormous movement at the tarsus (ratio of

movements 60:1 when the tibiofemoral joint is tightly flexed)

It has been calculated that for the locust to achieve the maximum thrust for takeoff,

the body must be accelerated at about 1.5× 104cm/sec2over a time span of 20 msec The

force exerted by each extensor muscle is about 5 ×105 dynes (= 500 g wt) for an insect

weighing 3 g (Alexander, 1968, cited from Hughes and Mill, 1974) To withstand this force,

the apodeme must have a strength close to that of moderate steel The extremely short time

period over which this acceleration is developed makes it unlikely that jumping occurs as a

direct result of muscle contraction Indeed, Heitler (1974) showed that the initial energy of

muscle contraction is stored as elastic energy using a cuticular locking device that holds the

flexor tendon in opposition to the force developed within the extensor muscle At a critical

level, the tendon is released, allowing the tibia to rotate rapidly backward

Likewise, in fleas, the energy of muscle contraction is first stored as elastic energy

Prior to jumping, the flea contracts various extrinsic muscles of the metathorax, which are

inserted via a tendon on the fused trochantofemoral segment This serves to draw the leg

closer to the body, compressing a pad of resilin and causing the pleural and coxal walls

to bend At a certain point of contraction, the thoracic catches (pegs of cuticle) slip into

CHAPTER 14

notches on the sternum, thereby “cocking the system.” The jump is initiated when otherlaterally inserted muscles contract to pull the catches out of the notches, thus allowing the

stored energy to be rapidly released (Rothschild et al., 1972).

Once airborne, an insect may or may not stabilize itself in preparation for landing or

flight For example, the flea beetle Chalcoides aurata sometimes jumps “out of control,” its

body rotating continuously till it hits the ground However, it can, when necessary, controlits jump by extending the wings so that a “feet-first” landing occurs (Brackenbury andWang, 1995) Larger species such as Orthoptera use their hindlegs as rudders during thejump, facilitating an upright landing or takeoff for flight (Burrows and Morris, 2003)

3.1.3 Crawling and Burrowing

Many endopterygote larvae employ the thoracic legs for locomotion in the manner ical of adult insects; that is, they step with the legs in a specified sequence, the legs of a givensegment alternating with each other Usually, however, changes in body shape, achieved

typ-by synchronized contraction/relaxation of specific body muscles, are used for locomotion

in soft-bodied larvae In this method the legs, together with various accessory locomotoryappendages, for example, the abdominal prolegs of caterpillars, are used solely as frictionpoints between the body and substrate Apodous larvae depend solely on peristalsis of thebody wall for locomotion

Where changes in body shape are used for locomotion the body fluids act as a hydrostaticskeleton In other words, the insect employs the principle of incompressibility of liquids,

so that contraction of muscles in one part of the body, leading to a decrease in volume, willrequire a relaxation of muscles and a concomitant increase in volume in another region ofthe body Special muscles keep the body turgid, enabling the locomotor muscles to effectthese volume changes

Crawling in lepidopteran caterpillars is probably the best studied method of locomotion

in endopterygote larvae and comprises anteriorly directed waves of contraction of the gitudinal muscles, each wave causing the body to be pushed upward and forward (Hughesand Mill, 1974; Brackenbury, 1999) Three main phases can be recognized in each wave ofcontraction (Figure 14.7) First, contraction of the dorsal longitudinal muscles and trans-verse muscles causes a segment to shorten dorsally and its posterior end to be raised so thatthe segment behind is lifted from the substrate The dorsoventral muscles and leg retractormuscles then contract, lifting both feet of the segment from the substrate Finally, contrac-tion of the ventral longitudinal muscles, combined with the relaxation of the dorsoventraland leg retractor muscles, moves the segment forward and down to the substrate Compared

lon-to walking, crawling and burrowing are relatively slow means of forward progression, withspeeds of about 1 cm/sec for typical caterpillars To take evasive action, for example, from

a predator, caterpillars may walk backward by simply reversing the direction of peristalsis.Under extreme provocation, the caterpillar may coil up into a wheel and simply roll back-ward, achieving speeds up to 40 times greater than normal walking (Brackenbury, 1999).Little work has been done on the neural coordination of crawling, though it seems probablethat endogenous activity within the central nervous system is responsible However, pro-prioceptive stimuli undoubtedly influence the process

Crawling or burrowing in apodous larvae is comparable to peristaltic locomotory ments found in other invertebrates, for example, mollusks and annelids Larvae that crawlover the surface of the substrate grip the substrate with, for example, protrusible prolegs

move-or creeping welts (transversely arranged thickenings equipped with stiff hairs) situated at

449 MUSCLES AND LOCOMOTION

FIGURE 14.7. Phases in the passage of a peristaltic wave along the body of a caterpillar [After G M Hughes,

1965, Locomotion: Terrestrial, in: The Physiology of Insecta, 1st ed., Vol II (M Rockstein, ed.) By permission

of Academic Press, Inc., and the author.]

the posterior end of the body A peristaltic wave of contraction then moves anteriorly,

lengthening and narrowing the body The anterior end is attached to the substrate while the

posterior is released and pulled forward as the anterior longitudinal muscles contract In

many burrowing forms peristalsis proceeds in the opposite direction to movement, so that

the narrowing and elongation begins at the anterior end and runs posteriorly As the anterior

end relaxes behind the peristlatic wave, it expands This expansion serves both to anchor

the anterior end and to enlarge the diameter of the burrow (Hughes and Mill, 1974; Berrigan

and Pepin, 1995)

3.2 Movement on or Through Water

Progression on or through water presents very different problems to movement on a

solid substrate For small organisms, such as insects that live on the water surface, surface

tension is a hindrance in production of propulsive leg movements For submerged insects,

the liquid medium offers considerable resistance to movement, especially for actively

swim-ming forms

Insects that move slowly over the surface of the water, for example, Hydrometra

(Hemiptera), or crawl along the bottom, for example, larval Odonata and Trichoptera,

normally employ the hexapodal gait described above for terrestrial species More rapidly

moving species typically operate the legs in a rowing motion; that is, both legs of the segment

move synchronously Some species do not use legs but have evolved special mechanisms

to facilitate rapid locomotion

3.2.1 Surface Running

The ability to move rapidly over the surface of water has been developed by most

Gerroidea (Hemiptera), whose common names include pondskaters and waterstriders To

stay on the surface, that is, to avoid becoming waterlogged, these insects have developed

various waterproofing features, especially hydrophobic (waxy) secretions, on the distal parts

CHAPTER 14

of the legs However, these features considerably reduce the frictional force between thelegs and water surface which is necessary for locomotion This problem is overcome inmany species by having certain parts of the tarsus, particularly the claws, penetrate thesurface film and/or by having special structures, for example, an expandable fan that openswhen the leg is pushed backward In the Gerridae, however, the backward push of the legs

is sufficiently strong that a wave of water is produced that acts as a “starting block” againstwhich the tarsi can push (Nachtigall, 1974)

The functional morphology and mechanics of movement have been examined in detail

in Gerris (Brinkhurst, 1959; Darnhofer-Demar, 1969) This insect has greatly elongated

middle legs through which most of the power for movement is supplied Some power isderived from the hindlegs, though these function primarily as direction stabilizers Thearticulation of the coxa with the pleuron is such that the power derived from contraction ofthe large trochanteral retractor muscles is used exclusively to move the legs in the horizontalplane, that is, to effect the rowing motion Equally, the coxal muscles serve only to lift thelegs from the water surface during protraction At the beginning of a stroke, the forelegs arelifted off the surface The middle legs are rapidly retracted so that a wave of water formsbehind the tarsi As the legs are accelerated backward, the tarsi then push against this wave,causing the insect to move forward After each acceleration stroke, the insect glides overthe surface for distances up to 15 cm The power developed in each leg of a segment isidentical and the insect glides, therefore, in a straight line Turning can occur only betweenstrokes and is achieved by the independent backward or forward movement of the middlelegs over the water surface

Waterstriders of the genus Velia and the staphylinid beetle Stenus use an ingenious

means of skimming across the water surface They release a surface tension-reducing cretion behind themselves and are thus pulled rapidly forward, reaching speeds of 45–70

se-cm/sec (Stenus).

3.2.2 Swimming by Means of Legs

Both larval and adult aquatic Coleoptera (Dytiscidae, Hydrophilidae, Gyrinidae, plidae) and Hemiptera (Corixidae, Belostomatidae, Nepidae, Notonectidae) swim by means

Hali-of their legs Normally, only the hindlegs or the mid- and hindlegs are used and these arevariously modified so that their surface area can be increased during the propulsive strokeand reduced when the limbs are moving anteriorly Modifications include (1) an increase

in the relative length and a flattening of the tarsus; (2) arrangement of the leg tion, so that during the active stroke the flattened surface is presented perpendicularly tothe direction of the movement, whereas during recovery the limb is pulled with the flat-tened surface parallel to the direction of movement; the leg is also flexed and drawn backclose to the body during recovery; (3) development of articulated hairs on the tarsus andtibia that spread perpendicularly to the direction of movement during the power stroke,yet lie flat against the leg during recovery; such hairs may increase the effective area by

articula-up to five times; and (4) in Gyrinus, development of swimming blades on the tibia and

tarsus (Figure 3.24A) These are articulated plates that normally lie flattened against eachother During the power stroke, the water resistance causes them to rotate so that theiredges overlap and their flattened surface is perpendicular to the direction of movement ofthe leg

In addition to the surface area presented, the speed at which the leg moves is proportional

to the force developed Thus, it is important for the propulsive stroke to be rapid, whereas

451 MUSCLES AND LOCOMOTION

the recovery stroke is relatively slow Accordingly, the retractor muscles are well developed

compared with the protractor muscles

In the best swimmers other important structural changes can be seen, such as

stream-lining of the body and restriction of movement and/or change in position of the coxa In

adult Dytiscus, for example, which may reach speeds of 100 cm/sec when pursuing prey,

the coxa is inserted more posteriorly than in terrestrial beetles and is fused to the thorax

Thus, the fulcrum for the rowing action is the dicondylic coxotrochanteral joint which

operates like a hinge so that the leg moves only in one plane Because of this

arrange-ment, all of the muscle power can be used to effect motion in this plane (Ribera et al.,

1997)

Several variations are found in the rhythms of leg movements Where a single pair of

legs is used in swimming, both legs retract together When both the midlegs and hindlegs

are used, both members of the same body segment usually move simultaneously, but are in

opposite phase with the legs of the other segment; that is, when one pair is being retracted,

the other pair is being protracted In adult Haliplidae and Hydrophilidae and many larval

beetles all three pairs of legs are used, in a manner comparable with the tripodal gait of

terrestrial insects

Steering in the horizontal plane (control of yawing) is achieved by varying the power

exerted by the legs on each side For vertical steering (movement up or down) the

non-propulsive legs become involved These may be held out from the body in the manner of

a rudder or may act as weakly beating oars By varying the angle to the body at which

the legs are placed the insect will either dive, surface, or move horizontally through the

water Most aquatic insects are quite stable in the rolling and pitching planes because of

their dorsoventrally flattened body (See Figure 14.14 for explanation of the terms yawing,

pitching, and rolling.)

3.2.3 Swimming by Other Means

A variety of other methods for moving through water can be found in insects, including

body curling and somersaulting found in many larval and pupal Diptera, body undulation

(larval Ephemeroptera and Zygoptera), jet propulsion (larval Anisoptera), and flying (a few

adult Lepidoptera and Hymenoptera) (Nachtigall, 1974)

Many midge and mosquito larvae rapidly coil the body sideways, first in one

direc-tion, then the other, to achieve a relatively inefficient form of locomotion Chironomids,

for example, lose 92% of the energy expended in the power stroke during recovery

Conse-quently, a 5.5-mm larva oscillating its body 10 times per second moves at only 1.7 mm/sec

through the water Mosquito larvae possess flattened groups of hairs (swimming fans) or

solid “paddles” at the tip of the abdomen and are consequently more efficient and more

active swimmers than chironomids

Pupae of midges and mosquitoes somersault through the water, especially when

at-tempting to escape predators Interestingly, the surface-dwelling pupa of the mosquito Culex

pipiens somersaults at a greater frequency (hence swims faster) than the bottom-dwelling

pupa of the midge Chironomus plumosus, perhaps because there is greater predator pressure

for a surface-dweller (Brackenbury, 2000)

Larvae of Zygoptera and some Ephemeroptera undulate the abdomen, which is

equipped at its tip with three flattened lamellae (Zygoptera, Figure 6.11) or swimming

fans (Ephemeroptera, Figure 6.4) Some ephemeropteran larvae supplement the action of

the fans by rapidly folding their abdominal gills against the body

CHAPTER 14

Dragonfly larvae (Anisoptera) normally take in and expel water from the rectum duringgas exchange (Chapter 15, Section 4.1) In emergencies this arrangement can be convertedinto a jet propulsion system for moving an insect forward at high speed (up to 50 cm/sec).Rapid contraction of longitudinal muscles causes the abdomen to shorten by up to 10%.Simultaneous contraction of the dorsoventral muscles leads to an increase in hemolymphpressure which forces water out of the rectum via the narrow anus at speeds approaching

250 cm/sec

Female Hydrocampa nympheata (Lepidoptera) and adult Dacunsa (Hymenoptera) use their wings in addition to legs for swimming underwater Other Hymenoptera (Polynema and Limnodites) swim solely by the use of their wings.

3.3 Flight

As noted in Chapter 2, Section 3.1, wing precursors originally had functions quiteunrelated to flight Subsequent evolution led to enlargement and perhaps articulation ofthese structures as they took on a new function, propulsion of an insect through the air,partly as a result of which insects were able to move into new environments to become thediverse group we know today Despite this diversity, there is sufficient similarity of skeletaland neuromuscular structure and function to suggest that wings had a monophyletic origin(Pringle, 1974)

Examination of the form and mode of operation of the pterothorax reveals certaintrends, all of which lead to an improvement in flying ability Primitively, the power for wingmovement was derived from various “direct” muscles, that is, those directly connected withthe wing articulations These muscles serve also to determine the nature of the wing beat.Even today, the direct muscles remain important power suppliers in the Odonata, Orthoptera,Dictyoptera (Blattodea), and Coleoptera In other insect groups, efficiency is increased byseparating the control of wing beat (by the direct muscles) from power production, whichbecomes the job of large “indirect” muscles located in the thorax

There are important differences in the fine structure and neuromuscular physiology ofthe direct and indirect flight muscles Generally, in insects that flap their wings relativelyslowly (up to 100 beats/sec), each beat of the wings is initiated by a burst of impulses to thepower-producing muscles, which are of the tubular or close-packed type (Figure 14.3B, C).This applies to all users of direct muscles for powering flight, plus Lepidoptera in which theindirect muscles are used In contrast, in fliers that use indirect muscles and whose wing-beatfrequency is high (up to 1000 beats/sec), muscle contraction is not in synchrony with thearrival of nerve impulses at the neuromuscular junction Rather, the rhythm of contraction isgenerated within the muscles themselves, which are fibrillar (Figure 14.3D) Accordingly,the two forms of rhythm are described as synchronous (neurogenic) and asynchronous(myogenic), respectively The use of asynchronous muscles to power flight has evolvedseveral times within the Insecta Its significance appears to be the facilitation of high wing-beat frequencies, thereby moving more air, so that even insects with small wings relative totheir body size are efficient fliers

3.3.1 Structural Basis

Each wing-bearing segment is essentially an elastic box whose shape can be changed

by contractions of the muscles within, the changes in shape causing the wings to move

up and down The skeletal components of a generalized wing-bearing segment are shown