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 DOI: 10.1177/027836498400300209

1984 3: 101The International Journal of Robotics ResearchK.G. Pearson and R. Franklin

TerrainCharacteristics of Leg Movements and Patterns of Coordination in Locusts Walking on Rough

  

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Characteristics of LegMovements andPatterns ofCoordination inLocusts Walking onRough Terrain

K. G. PearsonDepartment of PhysiologyUniversity of AlbertaEdmonton, Alberta, Canada

R. FranklinDepartment of BiologyUniversity of OregonEugene, Oregon 97403

R. Franklin’s present address is Environmental Research Institute of

Michigan, P.O. Box 8618, Ann Arbor, Michigan 48107.

Abstract

A cinematographic analysis was made of locusts walking ona variety of terrains to determine the tactics used by singlelegs to find a site for support and the patterns of leg coordina-tion when walking on rough terrain. Three tactics were usedby individual legs for finding a support site: (1)rhythmicsearching movements initiated when the leg failed to contactthe substrate at the end of the swing phase, (2) a tactile reflexto lift the leg above an object contacted during swing phase,and (3) local searching movements once the leg had contacteda potential supporting surface. Animals did not adopt rigidgaits when walking on rough terrains. The wide range ofstepping patterns was due mainly to variation in the timingof stepping in opposite legs of the same segment. However,there was a tendency for the stepping movements of oppositelegs to be either 180° out of phase or exactly in phase. In-phase stepping of the middle legs was observed frequentlywhen animals walked over a ditch or up onto an elevated ob-ject. Once the forelegs had found support on either the farside of the ditch or on the elevated object, both middle legsstepped simultaneously and were then used together to movethe animal over the ditch or up onto the object.

1. Introduction

A major problem facing those building walking ma-chines is to establish algorithms to control individuallegs and coordinate movements of different legs (Rai-bert and Sutherland 1983). Since a number of ma-chines now under development are hexapods (Raibertand Sutherland 1983; McGhee, forthcoming), there issome interest in the strategies used by insects whenthey walk on rough terrain and when they execute suchmaneuvers as turning, climbing over objects, and tra-versing ditches. Knowledge of the mechanisms respon-sible for the remarkable dexterity of insects walkingover rough terrain could be of use in the developmentof control algorithms for hexapod machines.From studies of insects walking on smooth horizon-

tal surfaces, the following rules have been formulated(Delcomyn 1981 ):

1: Stepping movements occur in a metachronalsequence from rear to front.

2. Legs on opposite sides of a single segment stepin antiphase.

3. No front or middle leg steps before the onebehind it finishes its forward movement.

4. The duration of the protraction (swing) phaseremains constant as walking speed changes.

With the additional assumption of a constant delaybetween the placement of one leg and the lifting of theleg in front of it, Wilson (1966) showed that many ofthe common gaits observed in insects could be gener-ated by changes in just one variable, namely the timeof retraction (stance). In particular, Wilson accountedfor the smooth transition between a metachronal gait

This project was supported by the Defense Advanced ResearchProjects Agency under Subcontract RF714250-01 from The OhioState University.

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(wave gait) at low walking speeds and an alternatingtripod gait at high speeds. These rules do not accountfor all the empirical data, however. In some casesslight modification of one or more rules is required,such as a weak dependence of protraction time onspeed ( a modification of rule 4), while in other cases arule is clearly violated, such as simultaneous steppingof opposite legs (a violation of rule 2) (DelcomynI 981 ). Nevertheless, these rules are adequate for de-scribing the qualitative features of leg coordination inmost insects when they walk on smooth horizontalsurfaces.Of more interest to those designing walking ma-

chines are the rules governing leg movements whenanimals walk in a varying environment. Unfortu-nately, there have been very few studies on how insectswalk on rough and complex terrain. This is somewhatsurprising considering the large number of investiga-tions on insects walking on even surfaces, but under-standable since the object of most research on insectwalking has been to determine the underlying neuralmechanisms. Because of this lack of interest in naturalbehavior there are, at present, no general concepts fordescribing how insects adapt their walking to roughterrain. In fact, there are not even any detailed de-scriptions of what insects actually do when they walkon rough terrain. There is, however, some informationon the body orientation of stick insects when theywalk up and down steps (Cruse 1976) and on theirstepping movements when they walk over ditches(Cruse 1976; 1979). The only clear phenomenonemerging from these studies on stick insects is a strongtendency for posterior legs to seek support sites closeto the support sites of the immediately anterior ipsi-lateral legs. If this &dquo;follow-the-leader&dquo; behavior oc-curred in adjacent legs in other insects, then it clearlywould be an important general strategy contributingto an insect’s ability to walk over rough terrain. Ob-viously it cannot be the only strategy, for at the veryleast there must be means by which the forelegs findsupport sites.With the aim of gaining more information about leg

movements and the patterns of stepping in differentsituations, we filmed locusts walking over a variety ofrough terrains. In particular, we wished to determine(1) the tactics used by single legs to find a site for sup-port, (2) any relationships between the pattern of coor-

dination and the terrain upon which the animal was

walking, and (3) the method used for stepping overditches and over elevated objects.

2. Materials and Methods

2.1. ANIMALS

All experiments were carried out on adult locusts (Lo-custa migratoria) obtained from a crowded colony atthe University of Alberta. Initially, each animal wasplaced repeatedly (about 20 times) on the terrain todecrease the probability of jumping. Filming was com-menced as soon as the animal began to walk withouthesitation. If it did not walk spontaneously, the abdo-men was lighty touched to initiate walking.

2.2. TERRAIN

Locusts were filmed while walking on (1) a flat surface,(2) a wire mesh, (3) an irregular surface of woodenblocks, (4) a surface comprised of hexagonal array offlat heads of nails, (5) a flat surface containing a ditch,(6) a flat surface containing an elevated step, and (7) avertical rod with projecting side branches.

2. 2.1. Wire Mesh

A 12 X 12 in sheet of square wire mesh (interwiredistance = 0.25 in) was arranged horizontally, and an-imals were filmed from above while walking over thismesh.

2.2.2. Wooden Blocks

This terrain consisted of a square array of 2,304 (48 X48) wooden blocks (dimensions 0.25 X 0.25 X 3.5 in)arranged lengthwise. Each block could be adjusted to adifferent height within a 12 X 12 in frame. The heightswere set to provide a rough terrain. The maximumdifference in height between adjacent blocks was 0.25 in.

2.2.3. Nail Heads

This terrain consisted of a 12 X 12 in hexagonal arrayof the heads of flat-head nails. The diameter of the

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Fig. 1. Experimental ar-rangement for ftlmtng (fromabove) animals walking overa ditch. The walking surface(cardboard sheet) containingthe ditch was placed in a12 X 12 in box mounted oncasters. The camera wasmounted directly above thisswface. As the animal

walked fronz an octagonalarena across the ditch it waskept within the field of viewby moving the box. Theditch (approximately 1 cmwide) was constructed with-out vertical walls to preventsupport when a leg was inthe ditch.

heads was 1 cm, and the distance between nails was1.5 cm. Thus the terrain consisted of only 40% solidsurface. Nails were used to create this surface becauseour initial observations showed that if rods were usedthe animals would find support sites on the verticalfaces of the rods. When walking on nails, animalswere forced to find support sites on the horizontal sur-faces of the nail heads.

2.2.4. Ditch

The ditch was arranged either around an octagonalarena (Fig. 1 A) or midway along an elevated runway.The width of the ditch was approximately 1 cm. Thisensured a reasonably high probability of a foreleg step-ping into it: the average length of a step of a forelegwas a little over 2 cm. The ditch was constructed with-

out vertical walls (the animal walked on thin card-board) to prevent the possibility of any support whenthe leg was in the ditch. With this arrangement, legswere forced to find support on the horizontal surfaceon either side of the ditch.

2.2.5. Elevated Step

The step was arranged either around an octagonalarena or midway along an elevated runway. The stepheight was 1.2 cm. The maximum elevation of theforelegs during walking on a smooth surface was about0.5 cm. Thus the forelegs had to be elevated higherthan normal to find support on all these steps.

2.2.6. Vertical Rod

This consisted of a vertical wooden rod 1 cm in diam-

eter, with short projections arranged regularly along itslength. Animals were induced to climb vertically upthe rod with their bodies orientated so that the projec-tions lay directly to one side. This terrain was used toinvestigate the movements of legs when they contactedthe projections, and to find out whether the use of aprojection for support influenced the movement of theadjacent posterior leg.

2.3. FILMING

Walking animals were filmed at 50, 64, or 100 frames/second with a Locam 51 camera. The magnificationwas usually such that the animal’s length was aboutone-half the frame width. Three camera arrangementswere used. When filming the animals from above, thecamera was fixed and the terrain was shifted to keepthe animal in view (Fig. 1 B). When filming from theside, both the camera and the terrain were fixed andthe field of view included either a ditch or an elevated

step. The camera was panned to track the animalwalking up the vertical rod.The majority of films were made using Kodak 7250

(400 ASA) color film. Otherwise Kodak TriX (160ASA) black and white film was used. The color filmwas not much more costly than black and white, andit had the advantage of requiring much lower lightintensities during filming.

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2.4. ANALYSIS

Films were analyzed frame by frame using a photo-optical data analyzer (Model 224A Mark VI, L-WInternational, Woodland Hills, California). Quantita-tive measurements of step trajectories, amplitudes,and lengths were made by projecting the image onto aground-glass screen and tracing successive images ontotransparent plastic sheets.

3. Results

3.1. TACTICS USED BY LEGS TO FINDSUPPORT SITES

We identified three distinct tactics used by single legsto find support sites on rough terrain:

1. Searching movements. These are rapid, rhyth-mic, up-and-down movements initiated when

’

the leg fails to find any support at the end of aswing phase.

2. Elevator reflex. This consists of a marked ele-vation of the leg when it contacts an objectduring the swing phase, and it usually resultsin the tarsus being placed on the object.

3. Local searching movements. These are small,rhythmic shifts of the tarsus on a potentialsupporting surface.

In the following sections, we describe each of thesetactics in more detail, but first, because of its impor-tance, we report a negative result; namely, the lack ofany strong evidence that anterior legs signal informa-tion about potential support sites to posterior legs.Since this phenomenon is very clear in the stick insect(Cruse 1979; Dean and Wendler 1983), we lookedcarefully for its occurrence in the locust under a varietyof conditions, for example, when locusts walked upthe vertical rod with projecting side pieces. On this ter-rain, a foreleg often found a support site on a projec-tion more laterally located than the preceding supportsite on the vertical rod. If foreleg placement does in-fluence placement of the ipsilateral middle leg, thenforeleg placement on a lateral projection should initi-ate lateral stepping movements of the ipsilateral mid-dle leg. This occurred very rarely. In fact, we observed

only one reasonably convincing example in over 50observations. In most cases, movements of the middle

legs were not significantly altered when the foreleg wasplaced on the lateral projection. Neither did observa-tions of animals walking on flat nail heads or over aditch reveal any follow-the-leader strategy. First, thesupport site of the middle legs in more than 50% of thesteps was on a different nail head than the ipsilateralforelegs; and second, the probability of a middle legnot finding a support site at the end of the swing phase,(i.e., stepping into the gaps between the nails or intothe ditch) was close to the probability of a foreleg notimmediately finding a support site. These probabilitieswere 0.25 for the foreleg versus 0.3 for the middle legwhen animals walked over the ditch. If a follow-the-leader strategy were being used, then we would expectthis probability to be much lower for the middle legs,as has been observed in stick insects (Cruse 1979).Because of one example of a middle leg following aforeleg in an animal walking up the vertical rod, we arereluctant to conclude that the follow-the-leader strat-

egy is never used by the locust.

3. 1. 1. Searching Movements of Single LegsThe most obvious tactic used by a leg to find a supportsite on rough terrain was to initiate rhythmic searchingmovements when it failed to contact an object at theend of the swing phase. Of course, these searchingmovements only occurred on terrain where there wasa possibility of failure in contacting the substrate atthe end of swing, such as on wire mesh, over a ditch,or over the heads of nails. The characteristics of the

searching movements were as follows:

1. Rapid elevation and depression movements ofthe leg at frequencies of up to 8 cycles/second,resulting in the exploration of a wide spacearound the point of articulation of the leg withthe body

2. Usually, marked extension at distal joints,effectively increasing the range of the searchrelative to the body

3. Continuation for many cycles (the most wehave observed is eight)

4. Termination when the animal stopped walkingor the leg struck and found support on an object

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Fig. 2. Elevator reflex of theleft foreleg, initiated whenremoving the leg from aditch. A. Stick diagram offoreleg walking on a flatsurface (moving from right toleft). B. Stick diagram offoreleg as it is removed fromthe ditch, striking the faredge of the ditch. The filled

circles above each diagramindicate the position of theipsilateral eye. Note that theelevator reflex evoked in Bresulted in the tarsus beingelevated higher than duringnormal walking. Diagramswere constructed from se-quential frames: film-speed = 50 frames/second.

Two other characteristics of searching movementsare noteworthy. The first is that they caused the animalto pause in walking and, when extensive, to stop walk-ing completely. The second is that they were oftenmade when the animal repositioned itself on the sub-strate. Thus, searching movements were seen in asso-ciation with postural adjustments and with walking.The speed of the searching movements during stand-ing, was considerably less than the speed during walk-ing (e.g., 1- 2 cycles/second compared to 6 - 8 cycles/second).

3.1.2. Elevator ReflexWhen walking on a rough and uneven terrain, there isa high probability that legs will strike objects duringthe swing phase. The legs of locusts have an effective

Fig. 3. Elevator reflex ofmiddle leg, initiated whenwalking over an elevatedstep (movement from right toleft). The filled and opencircles show the trajectoriesof the tarsus on two separatetrials, one when the tarsusstruck the step (filled circles)

and one when the tarsus

failed to strike the step (opencircles). Note the exagger-ated elevation orthe tarsuson the trial when it struck the

step. Each point is fromsequential frames: filmspeed = 50 frames/second.

reflex to deal with this occurrence; namely, a rapidelevation and extension of the leg to lift it above theobject (provided the object is not too high), followedby depression, which usually results in the object beingused as a site for support.The elevator reflex occurred in all three pairs of legs

but was seen most clearly in the forelegs and middlelegs. Because the hind legs trail behind the animal, itwas often difficult to distinguish between an elevatorreflex and a more-or-less passive pulling of the hindlegs up onto the object as the animal moved forward.Although we observed this reflex on all the rough ter-rain we studied, it was filmed most clearly when theanimals walked over a ditch or up onto an elevated

step (Figs. 2 and 3). These and other films showed thatthe elevator reflex could be initiated when either thetarsus or the tibia struck the object.The elevator reflex also occurred during searching

movements. This usually led to the termination of .

searching movements.

3.1.3. Local Searching

Once the leg had located a surface that might be asuitable support, either directly at the end of a normalswing phase or following searching movements and/oran elevator reflex, the tarsus was often moved quicklyfrom point to point on the surface. This we term localsearching, for its clear function was to find a local

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Fig. 4. Examples of localsearching of right forelegwalking up vertical rod withprojecting side pieces. Thediagram shows the sites(dots) on a projection wherethe tarsus was placed. Thenumbers indicate frarnenumbers (filjn speed = 50frames/second ). The tarsusfirst contacted the projectionat site O. It was then elevated

and placed sequentially at aseries of sites until finding afinal support site at .Z3 in Aand 17 in B. In A, the pro-jection was a smooth woodenrod and the final stcpport sitewas on tl2e upper surface. InB, the projection was a rodcovered with roughetaedplasticine and the final sup-port site was close to thevertical part of the projection.

region for a suitable support site. These movementsvaried in magnitude and number. The most we ob-served for a single placement was six cycles. With thisnumber of movements, local searching could cover abroad area of the potential support surface.

Local searching was most obvious when the poten-tial support surface was smooth and the leg actionrequired was to propel the animal forward. For exam-ple, when the projections from the vertical rod weremade hard and smooth, the forelegs very often madelocal searching movements on these projections butnever established the final support site on their slopedor vertical surfaces (Fig. 4A). If, however, the projec-tions were covered with soft roughened plasticine, theprobability of local searching was diminished and thefinal support site was often on the vertical surface ofthe projection (Fig. 4B). Thus the probability of localsearching is related to the smoothness of the surface,We have not determined what information is used tosignal a suitable support site and terminate the localsearch, but we hypothesize it is a signal related to theload carried by the leg. Thus we propose that if theload on the leg does not quickly increase after thetarsus touches the surface, then the tarsus is quicklylifted and replaced on the surface at another point.This process continues until the critical load is borne

by the leg. Presumably, if the surface is rough, there is

Fig. 5. Stepping patterns inan animal walking on ahorizontal surface. Filledbars indicate leg protraction(swing). A. 4ut-of phasecoordination (tripod gait). B.In-phase coordination atbeginning, followed by a

variable pattern. C. Variables

pattern of stepping: note thatthe frequency of stepping onthe two sides is diff’erent.L = left; R = right; F = fore-leg; M = middle leg;H = hind leg.

less chance of the tarsus slipping and an increasedchance that the load will increase enough to terminatesearching.

3.2. COORDINATION OF LEG MOVEMENTS

3.2.1. Coordination on Flat Horizontal SurfacesOur observations of animals walking on a flat surfacerevealed a mode of coordination not previously de-scribed (e.g., Bums 1973). Basically, this mode con-sisted of in-phase stepping of opposite legs of the samesegment. The stepping sequence was both hind legs,both middle legs, both forelegs, both hind legs, and soon (Fig. 5B). We refer to this sequence as in-phasecoordination. Sequences of in-phase coordination wereusually short and occurred most often at the start ofwalking. Moreover, a complete sequence (hind, mid-dle, fore) was quite rare (about 5% of trials), but com-ponents of the in-phase mode, for example, both mid-dle legs stepping together, occurred frequently. Theother basic mode of coordination was the familiar

tripod gait in which stepping in adjacent legs (acrossand along the animal) alternated (Fig. 5A). This werefer to as out-of-phase coordination.

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Fig. c5. Histogram of thephase relationship betweenthe stepping of the left middleleg and the cycle of the rightmiddle leg in an animalwalking on a flat horizontalsurface. Note the bimodalnature of the histograms,with peaks close to 0.5 (out

of phase) and 1. 0 (in phase).Note also that phases arebroadly distributed from 0 to1. This type of phase hi.sto-gram was not common.

Usually. there was a singlepeak at 0.5, as shown inFig. 9.

Another feature of coordination seen in animals

walking on a flat surface was considerable flexibility inthe pattern of stepping. Often, it was not possible todefine a particular gait. An example is shown in Fig.5C. Despite this flexibility, one fairly constant featureof gait could be seen: a posterior-to-anterior sequenceof stepping on each side of the animal (Figs. 5A and5B). Much variation in stepping patterns can be ac-counted for by changes in the relative timing of theposterior-to-anterior stepping sequence on the twosides of the body. If they begin at the same time, thereis in-phase coordination (Fig. 5B); if they begin inantiphase, there is out-of-phase coordination (Fig. 5A),and if they drift relative to each other, there is no fixedpattern (Fig. 5C).The large flexibility in the stepping patterns raises

the question of whether in-phase and out-of-phasemodes really are two distinct modes or simply ex-tremes in a continuum. Evidence for two distinctmodes comes from an analysis of the relative timing

Fig. 7. Examples of steppingpatterns on rotcgh terrain. A.Control: a smooth horizontal

suiface. B. Blocks. C. Wiremesh. Note the variability inthe patterns of stepping onrough terrain (B and C).Note also that on rough ter-

rain the hind-middle-forestepping sequence persists formost cycles and is similar tothat which occurred whenthe animal walked on thesmooth surface. Labels areas defined for Fig. 5.

of stepping of the two middle legs. The histogram ofthe phase of stepping of one middle leg in the cycle ofthe other middle leg often has two distinct peaks, oneclose to a phase of 1 (in-phase coordination) and oneclose to 0.5 (out-of-phase coordination) (Fig. 6). An-other indication that in-phase stepping is a distinctmode is that precise in-phase coordination of fore andmiddle legs was seen on all terrains (see Fig. 9).

3.2.2. Coordination on Rough Terrains

When the terrain became varied, it was often difficultto discern any clear pattern of coordination (Figs. 7Band C), although the posterior-to-anterior sequencewas usually preserved (Figs. 7 and 8). The most obvi-ous change in the pattern of coordination was themarked increase in the occurrence of in-phase steppingof the middle legs and forelegs (Figs. 9 and 10). Figures9 and 10 also show an overall loss of precision in thepattern of coordination as the terrain became more

complex.When walking over very rough terrain, such as the

heads of nails, progression was punctuated by periodswhen the animal made searching movements of theforelegs and the middle legs. The occurrence of thesesearching movements, as well as the lack of the smooth

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Fig. 8. Histograms showingthe distribution of intervals(in milliseconds) between thetime of placement of a mid-dle leg and the beginning ofprotraction of the ipsilateral

foreleg when animals werewalking on wooden blocks (Aand B, bottom) and on wiremesh (C, bottom). The upperhistograms in A, B, and Cwere obtained from the same

three animals walking on aflat horizontal surface. Notethat walking on rough ter-rain did not lead to a signifi-cant change in interval dis-tributions. Thus, the

coordination of adjacentforelegs and middle legs wasnot significantly alteredwhen animals walked on

rough terrain.

progression, prevented any repetitive pattern of step-ping movements. Nevertheless, two features notedearlier (in-phase stepping of the middle legs, and thetendency of the forelegs to step soon after the middlelegs found support) were observed. All these observa-tions suggest that when locusts walk on rough terrainthey do not adopt a strategy for coordination thatdiffers in principle from the one used on flat surfaces.Rather, each leg appears to act independently in find-ing a support site, and the basic modes of coordina-tion (in phase and out of phase) of opposite legs, andthe posterior-to-anterior sequence of stepping in ipsi-lateral legs, are preserved. It should be noted, however,that very occasionally we observed a phenomenonnever seen in animals walking on a flat surface: simul-

taneous stepping of adjacent ipsilateral legs. We havebeen unable to relate the occurrence of this phenome-non to terrain or to the speed of walking, but in mostcases (four out of five) it only occurred when the posi-tions of the supporting legs ensured stability. In thefifth case, the animal fell to the unsupported side.

3.3. STRATEGIES FOR WALKING OVER DITCHESAND ONTO A STEP

If ditches were not too wide and steps not too high,animals often walked over them with little change inspeed or coordination. They quickly compensated forany interference presented by the obstacle. For exam-

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Fig. 9. Phase histograms ofprotraction of the left middle(LM) leg in the cycle of theright middle (RM) leg whenanimals walked on woodenblocks (A, right) and on wiremesh (B, right). The histo-grams on the left in A and Bwere for the same two ani-mals walking on a flat hori-zontal surface. Protraction ofthe middle legs of both ani-mals approximately alter-

nated ( phase close to 0.5)when they walked on the flatsurface. By contrast, therelative timing of middle-legstepping became highlyvariable when the animalswalked on rough terrain(phase values distributedfrom 0 to 1 ). Note the peaksin the right histograms closeto 0, indicating in-phaseprotraction of the middle legs.

ple, if a leg stepped into the ditch, a single search cyclewas usually sufficient to find the far side; and if the legcontacted the step, the elevator reflex quickly lifted itto the top.More interesting situations arose with wide ditches

(> 1 cm) and high steps (> 1 cm), which can be re-garded as significant discontinuities in the terrain. Theanimals could not quickly and reliably compensate forthese obstacles and maintain walking speed and aregular pattern of coordination. To traverse obstaclesof this magnitude, animals very often adopted a fairlystereotyped strategy for both the ditch and the step(Figs. 11 and 12). Its basic elements were as follows:

1. The animal detected the obstacle either visually(judged by the fact that it ceased walking whenclose to the obstacle but before the antennae or

forelegs touched the obstacle) or, in the case ofthe ditch, by touching with the forelegs andthen stopping walking.

2. The animal then adjusted its posture by draw-ing the hind legs into a flexed position and

Fig. 10. Phase histograms ofprotraction of the left foreleg(LF) in the cycle of the rightforeleg (RF) when animalswalked on wooden blocks (A,right) and on wire mesh (B,right). The histograms on

the left in A and B were forthe same two animals walk-

ing on a flat horizontal sur-face. Note that the relativetiming of stepping in the tvvoforelegs became more vari-able on rough terrain.

taking small steps with the middle legs to yielda fairly symmetric arrangement of the hindand middle legs on either side of the body.

3. The forelegs then found support on the oppo-site side of the ditch (often following extensivesearch movements in the ditch and/or an ele-vator reflex) or on the top of the step (usuallyinvolving an elevator reflex).

4. Both middle legs then stepped simultaneouslyover the ditch or onto the step.

5. The animal then continued walking with pat-terns of coordination similar to those seen atthe start of walking on flat terrain.

This strategy occurred in 65% of trials on the ditchand 58% of trials on the step. An important character-istic of the strategy was the stable, tetrapod supportprovided by the hind legs and forelegs when both mid-dle legs were stepping. If this support was absent, due,say, to the failure of one or both hind legs to be drawninto flexion, the simultaneous stepping of both middlelegs usually did not occur.

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Fig. 11. In-phase protractionof middle legs of an animalclimbing onto a step 1.2 cmhigh. In A and C, all legswere on the substrate, whilein B both middle legs were

protracting (arrows) simulta-neously. These sketches weremade by tracing projectionfrom,fi/m. Film speed = 50frames/second. Frame num-bers : A = I , B = 6, C = 10.

3.4. USE OF VISION FOR CONTROLLING STEPPING

The final aspect of this study was to assess whether lo-custs use vision to control the stepping of individuallegs and, more generally, whether vision is used in theavoidance of objects and the detection of changes inthe terrain. Some simple observations clearly illustratethe use of vision in detecting changes in the terrain.For example, briskly walking animals often stoppedwalking just short of the ditch or the elevated step.Neither antennal nor tactile signals could have beenused to terminate walking in most of these cases. Ani-mals even stopped just short of a I.5-crn black linepainted on a flat white surface.When this occurred, theleg movements observed when the animal resumedwalking often (about 60% of trials) resembled thoseseen when animals crossed a ditch or moved up onto a

step, that is, in-phase stepping of the middle legs. Thus,vision often caused the animal to stop walking whenapproaching a change in the terrain, and this was fol-lowed by a strategy involving in-phase coordinationfor dealing with the change in terrain.

Locusts also use vision to avoid small objects lyingin their path. In one test, animals were placed in anarena partly encircled by an elevated step. Each animalwas placed so that it faced the middle of the elevatedstep, and the step extended about 45 ° to either side ofthe animal. Some, but not all, animals changed direc-tion just enough to avoid walking into the lateral edgeof the step. In the absence of the partly encircling step,these animals walked straight ahead.

Fig. 12. In-phase protractionof middle legs of an animalwalking over a ditch I cmwide. In A and C, all legswere on tlre substrate, while

in B both middle legs wereprotracting (arrows) simulta-neously. Film speed = 50frames/second. Frame num-bers : A = 1, B = 11, C = 20.

The use of vision to detect changes in terrain andchange direction to avoid objects is not particularlysurprising. Of greater interest is that under some cir-cumstances vision appeared to be used to change thestepping movements of the forelegs. This was observedin two situations, one in which an animal approachedan elevated step and one in which an animal climbeda vertical rod with side projections. Occasionally, ananimal elevated a foreleg abnormally high just beforeany part of its body touched the step. Presumably, thiswas an attempt by the animal to place the foreleg onthe step (which it succeeded in doing on some occa-sions). In the second situation involving the verticalrod with projecting side pieces, we observed on threeoccasions a stepping foreleg being directed laterallytoward the projection even though no part of the ani-mal had touched the projection. These observationsleft little doubt that vision can direct the movementsof the forelegs toward a potential support site. Locustsclearly do not always use this mechanism, however,even when it would be advantageous to do so. Forexample, when walking up the vertical rod, the forelegsalmost always located the lateral projections followingan elevator reflex. This was also true for the majorityof cases where the animal found support on an ele-vated step. When the animals walked on the heads of

nails, we saw no indication that vision was used todirect the forelegs toward a support site. In general, wefound little indication that vision is used often for

directing foreleg movements.The clearest evidence for visual guidance of foreleg

stepping movements comes from observations of ani-mals approaching an elevated step. It is not yet cer-

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tain, however, that vision is ever used to indicate aspecific support site. More likely, vision changes theanimal’s orientation toward or away from objects inthe environment, and modifies the foreleg movementsto direct them toward a potential support surface. Thelocation of the precise support site seems to depend onthe use of the tactics described in Section 1.

4. Discussion

The main findings from this study of walking locustswere ( 1 ) tactics by which a single leg finds a site forsupport, (2) a mode of coordination involving simulta-neous stepping of the two legs of the same segment,and (3) a strategy for walking over ditches and up ontoa step. These findings, together with some negativeresults, have given us some insight about how locustswalk on rough terrain.

4.1. FINDING SUPPORT SITES

Perhaps the most obvious feature of leg movements inwalking locusts is that individual legs have the capac-ity for finding support sites independently of the otherlegs and without input from the eyes and the anten-nae. Each leg can act as a single functional unit infinding a site for tarsal placement. Three tactics usedby each leg to find a support site are (1) rhythmicsearching movements, initiated when a leg fails tocontact the substrate at the end of the swing phase, (2)elevation of the leg and placement of the tarsus on anobject when the leg strikes the object during swing,and (3) rapid shifts of the tarsus from point to pointon an object to locate a suitable support site once theobject has been found. Of course, these tactics are notused in every step, for the leg may immediately find asupport site at the end of swing, as usually happenswhen the animal is walking on a smooth surface. On asmooth surface, the exact placement of the tarsus isnot critical. But as the complexity of the terrain in-creases, so do the chances that the leg will not locate asuitable site at the end of swing and that it will strikean object during swing. Thus, on rough terrain thethree basic tactics are used in varying combinations,depending on the local environment in which the leg is

moving and the nature of the surface on which it isseeking support.Other factors that might contribute to choosing sites

for support are vision and information from other

legs. For the types of terrain we examined, locusts usedvision only rarely, and then only to move a foreleg inthe general direction of a potential support site, not toset it down at a discrete postion. A possible explana-tion for this general absence of visual control is thatour animals were well adapted to the terrain (havingwalked on it many times on different trials) and con-sequently they were using a more autonomous modeof walking. It is noteworthy that high stepping move-ments of the forelegs as animals approached an ele-vated object were most often observed during initialtrials.Somewhat surprisingly we found no convincing

evidence that a leg used information from other legs tohelp establish a site for support. A mechanism ofinter-leg communication has been clearly demon-strated in the stick insect (Cruse 1979). Its evident ab-sence in locusts may be related to habitat. Stick insects

commonly walk on twigs and intricate branches,whereas locusts usually walk on less varied surfaces(leaves, blades of grass, etc.) and frequently jump tomove from one place to another. It might be expected,therefore, that stick insects have more elaborate mech-anisms for finding support sites.

Generally, our observations suggest that supportsites on rough terrain are primarily chosen by mecha-nisms intrinsic to individual legs.

4.2. COORDINATION OF LEG MOVEMENTS

One of the unexpected findings in this study was theextensive use of in-phase stepping of the two legs of asingle segment. This type of coordination was observedon all types of terrain, but occurred more frequentlyas the complexity of the terrain increased. Anothersituation where in-phase coordination is used fre-quently is during swimming (Franklin, Jander, andEle 1977). One very common strategy used on roughterrain was for the animal to support itself on a tetra-

pod composed of the forelegs and hind legs, and thento step simultaneously with both middle legs. Thefunctional advantage of using this strategy on rough

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terrain, particularly for tasks such as crossing ditchesand moving onto elevated surfaces, is not immediatelyobvious. It may permit greater movement of the body.In one animal, we observed a 35% increase in bodymovement during in-phase stepping of the middle legscompared to out-of-phase stepping of a single middleleg. If this is true, it resembles the transition in mam-mals from out-of-phase (walking, trotting) to in-phase(galloping) gaits.Although our data indicate two basic modes for

coordination of the two legs on the opposite side ofthe same segment (Figs. 6 and 9), the relative timingof stepping movements of opposite legs can be ex-tremely variable. This flexibility in coupling betweenopposite legs may result from varying sensory signalsfrom leg receptors modifying the out-of-phase mode.Because these sensory signals depend on complexinteraction among body orientation, leg position, posi-tion of other legs, and active forces generated by mus-cle contractions, it follows that there is no simple wayto predict the sequence of stepping movements asanimals move over rough terrain. (See the paper byPearson, Fourtner, and Wong [ 1973] for a discussionof this point in relation to stepping in the cockroach.)A far less variable aspect of the stepping patterns wasthe posterior-to-anterior sequence of stepping in legson one side. This feature can be seen even when thereis no obvious overall pattern of stepping (Figs. 5C and7B).Our analysis does not indicate that locusts adopt a

unique gait when walking on rough terrain. The majorfeatures of coordination observed on rough terrainwere also seen (although not necessarily with the samefrequency) in animals walking on smooth surfaces.The most noticeable features of coordination on roughterrain were the extensive use of in-phase coordinationof the middle legs and the lack of a stereotyped gait.These features presumably result from a large sensorycomponent in the control of leg movements.

5. Acknowledgments

We thank Dr. R. McGhee for suggesting this projectand for his support and encouragment throughout.Dr. F. Delcomyn kindly gave us valuable commentsfor improving the manuscript.

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Burns, M. D. 1973. The control of walking in orthoptera. I.Leg movements in normal walking. J. Exp. Biol. 58:45-58.

Cruse, H. 1976. The control of body position in the stickinsect (Carausius morosus), when walking over uneventerrain. Biol. Cybern. 24:25 - 33.

Cruse, H. 1979. The control of the anterior extreme positionof the hindleg of a walking insect, Carausius morosus.Physiol. Entomol. 4:121-124.

Dean, J., and Wendler, G. 1983. Stick insect locomotion ona walking wheel: interleg coordination of leg position. J.Exp. Biol. 103:73-94.

Delcomyn, F. 1981. Insect locomotion on land. Locomotionand excercise in arthropods, ed. C. F. Herreid andC. R. Fourtner. New York: Plenum.

Franklin, R., Jander, R., and Ele, K. 1977. The coordination,mechanics and evolution of swimming by a grasshopper,Malanoplus differentialis (Othoptera: Acrididea). J. KansasEnt. Soc. 50:189-199.

McGhee, R. B. Forthcoming. Vehicular legged locomotion.Advances in automation and robotics, ed. G. N. Saridis.Greenwich, Conn.: Jai Press.

Pearson, K. G., Fourtner, C. R., and Wong, R. K. 1973.Nervous control of walking in the cockroach. Control ofposture and locomotion, ed. R. B. Stein et al. New York:Plenum, pp. 495-514.

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Wilson, D. M. 1966. Insect walking. Ann. Rev. Entomol.11:103-122.

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