THE LOCOMOTION OF THE COCKROACH PERIPLANETA AMERICANA

7/24/2019 THE LOCOMOTION OF THE COCKROACH PERIPLANETA AMERICANA

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J Exp

Biol.

(1971), 54. 443-452

With 6 text-figures

Printed in Great Britain

THE LOCOMOTION OF THE COCKROACH

PERIPLANETA AMERICANA

FRED DELCOMYN*

Department

of

Biology, University

of

Oregon

Received 8 September1970)

INTRODUCTION

Much attention

is

currently being directed toward

the

problem

of

control

and

co-ordination of leg movements during locomotion in insects (Wilson, 1965, 1966;

Runion Usherw ood, 1966, 1968; Pearson lies, 1970). Yet, a detailed, quanti-

tative description

of the leg

movements

of

insects during walking does

not

exist

for

the most common experimental animals. Wendler (1964) supplied suchadescription

for legmovementsin the stick insect, but this insect is little used in physiological

studies of locom otion. A description of locomotion in cockroaches

was

given by Hughes

(1952),

but itis in generalaqualitative one, and no longer provides the dep thofdetail

required by thephysiologist.

The present work w as undertaken

to

provide

a

firm foundation

of

behavioural data

on whichtobase hypotheses concerning the mechanismsofcontrol and co-ordination

of leg movements (Delcomyn, 1971).Themain finding has been that the gait used by

the cockroach, Periplaneta americana, the alternating tripod or alternating triangle

gait,

is

essentially the same over nearly the entire range

of

observed speeds

of

locomo-

tion. Only atvery lowspeedsisthere any significant deviation.

MATERIAL AND M E T H O D S

All animals used in this study were intact adult American cockroaches,

P.americana

L. Each subject was placedin anoblong Perspex boxforobservation. The bottomof

theboxwas lined with graph papertogivea reference grid formovements,and its

walls were coated with petroleum jelly to prevent the animal from escaping.The

cockroaches were photographed with a Hycam rotating-prism, high-speed motion

picture camera (Red Lake Labs, Santa Clara, California) at 200 or 500framesper

second as they moved freely along the lengthof thebox.Thecamera was arrangedso

that four to seven full stepsofeachlegcouldbecapturedon thefilm. Lighting was

provided by two Photoflood lights, one above each

end of

the box. These lights were

turned

off

periodically

for

brief periods during

the

photographic sessions

to

prevent

overheatingofthe animal.

The films were examined withthe aid of an analytical motion picture projector

(L-W Photo, Inc., Van Nuys, California). Analysis consisted

of

counting the num ber

of frames occupied by protraction and retraction (definitions below) during each

cycleofmovement, foreach leg.Theparametersof interest, protraction, retraction,

* Present address: Department of Zoology, University of Glasgow.


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444

FRED

DELCOMYN

cycle duration, protraction/retraction ratios, and relative phase positions were calcu-

lated from the frame data with the aid of a digital computer. G raphs of the p attern of

leg movements (e.g. Fig. 2) were drawn for each walking sequence and used as the

basis for editing the com puter output. Steps during which the animal abruptly changed

speed or direction were excluded, since the parameters under these conditions often

bore different relationships to frequency of leg movement than they did during steady

locomotion.

The terms used in describing the results are similar to those already established in

the literature (Hughes, 1952; Wilson, 1966), and are as follows:

Protraction:

the forward movement of a leg relative to the body and the ground.

Retraction:the backward movement ofaleg relative to the body. N o movement rela-

tive to the ground.

Lag:

the time from the beginning of protraction of one leg to the beginning of

protraction of another.

Phase:

the lag between two legs divided by the cycle duration of the leg which

moved first, i.e. the time relation between the movements of two legs.

RESULTS

Cockroaches do not generally run straight for long distances. However, the long

narrow structure of the running box and the petroleum jelly on the walls combined

to produce a large number of relatively straight runs through the field visible to the

camera. In add ition, the lighting was arranged so that the ends of the box were not as

well lit as the centre, which tended to increase the probability that the negatively

phototactic cockroach would continue through the well-lit centre rather than stop in

mid-run.

The cockroaches did not appear to be excessively disturbed by the lights, for after

10-15

m m m

the box some moved about quite slowly. In addition, they tended to carry

their bodies well off the floor of the box. Dragging the body is a mode of behaviour

characteristic of cockroaches in poor condition. The range of speeds observed was

about 2-80 cm/s (at a maximum temperature of

29

0

C ). The maximum speed observed

here is similar to that reported by others (Hughes, 1965).

In the present study the animals' rates of forward progression were measured

directly from the films in cm/s, and also estimated by measuring the frequency of leg

movement in Hertz (Hz). The latter measure has the dual advantage of allowing

cycle-by-cycle plotting of parameters, and of freeing the experimenter from the

necessity of measuring d irectly th e animal's rate of progression, a measurem ent which

is not possible under some experimental conditions. For these reasons, frequency of

leg movement was substituted for rate of forward progression as the independent

parameter in this study. The nearly linear relationship between average frequency of

leg movement and rate of forward progression (Fig. 1), shows that the substitution

is a straightforward one.

The movement of an animal's legs during locomotion can be visualised with the

aid of diagrams of stepping patterns, such as those shown in Figs. 2 and 3. These

diagrams illustrate typical sequences of leg movements at stepping frequencies from

1-5 t o 23 Hz, and show qualitatively the behaviour of both th e individual step


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The locomotion of the cockroach 445

parameters, protraction and retraction, and the inter-leg timing parameter, phase.

The behaviour of each of these parameters as a function of the frequency of leg move-

ments is described in detail in the following sections.

90

r

70

S. 50

< 30

10

10 20

Average frequency of leg movement Hz)

30

Fig. 1. The average speed of locomotion as a function of the average frequency of leg move-

ment. Each point represents a single continuous run. All data are for intact, unrestrained

animals.

Individual leg movem ents

The durations of both protraction and retraction decrease as the cockroach moves

at progressively higher speeds, but they do so at different rates. This may be seen in

the diagrams of stepping patterns (Figs. 2 and 3), and in Fig. 4. Retraction is nearly

three times longer than protraction at the lowest frequency of leg movement, but it

falls more rapidly than protraction as frequency of leg movement increases, until at

the highest observed stepping frequencies it is often shorter than the latter.

This differential rate of decrease is also reflected in the protraction/retraction

p/r)

ratio (Fig. 5), which increases linearly with increases in frequency of leg movement.

The relationship betweenp/r and frequency is nearly the same for each of the legs.

The parameters of the regression lines and other statistics for the data for each leg are

shown in Table 1. There is no significant difference between the slopes of any of the

distributions, i.e. the rate at which p/r increases as stepping frequency increases is

essentially the same for each of the legs.


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FRED DELCOMYN

However, the mean

p/r

ratios of each of the legs do not show such uniform ity, those

of the middle legs (R.2 and L2) being lower than those

of

the remaining four legs

(Table1).This difference betweenthemeanpjrof R 2 and L2and each of the remaining

R3

R2

R

L 3 -

L2f-

L1

m - - - -

- -

i-

m

-

1-

L

mi m

1 H

- - - -

1 H

Ms

B

L 3

-

m

m m m m

L2- - - - - - - - - - - - i

0-2s

Fig. 2. Stepping patterns

of

rapidly moving intact animals. Th e co nventions established by

Wilson (1966) have been followed. Th e legs on the r ight (R) and left (L) sides of the body are

numbered from front torear. Each row represents the movementsofthe indicated leg, the

solid bars representing protraction, dotted lines retraction. The diagram reads from leftto

right. N otice the simultaneous movements of the tw o sets of three legs, R3 , R i , L2 and L3 ,

L i , R2, each of which form a triangle. A . Frequen cy of leg movement about 22 H z. B. F re-

quency of leg movement about 9 Hz.

Table 1.

Correlation

and

regression parameters of

the

p / r ratio distributionfor each

leg

Leg

R i

R 2

R 3

L i

L 2

L 3

n

66

64

6 2

58

65

63

r

0-6922

0-8113

07031

07239

c-7457

0-7901

bs.e.

0-026510-0035

0-0358 + 0-0033

00344 00045

00308 0-0039

0-0279 0-003 1

00336 0-0033

y int.

0456

0 1 9 9

0-386

O-344

0-301

0 3 3 0

Mean

Plr

0-825

0-713

0889

0788

0-704

o-8n

(,no.ofob servations;r, correlation coefficient; 6s.E., regression coefficient (slope)its standard

error;

y

int., ordinate intercept

of

regression line. Each m ean

pjr

corresponds to

a

frequency of leg

movementof about 14-5 Hz (except R i , 139).)


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The locomotion of the cockroach

legs is significant statistically to at least the 97-5 % level of confidence in each case.

The re is no significant difference between the mean ratios of legs R.2 and L 2 , nor

between those of any of the remaining four legs. Graphically, therefore, the regression

lines for R2 and L2 are depressed vertically compared to those from the remaining

legs (Fig. 5). Since all the slopes are the same, the p/rratio at any given frequency of

leg movement is lower for legs L 2 and R2 than for legs R i , L i , R3 or L 3 . This

means that the middle legs are off the ground for shorter periods at any given speed

R3 -1

R2 -

R1

L3

L2

L1

0-2Ss

0-5s

Fig. 3. Stepping patterns of slowly moving intact animals. Conventions are as in Fig. 2.

A. The alternating movements of the two triangles of legs are still maintained at this low

frequency of leg movem ent (4 Hz ). Protraction duratio ns have now become significantly

shorter than retraction, resulting in periods during which all six legs are on the ground at

once.

B. The alternating triangle pattern has begun to break down at this frequency of leg

movement (1-5 Hz), and might be termed 'uncoupled' alternating triangle.

of locomotion than are any of the four other legs. Although there is, in fact, a great

deal of variation in thepjr ratio at any speed, thus necessitating the statistical treatm ent,

this phenomenon may be seen quite clearly in the R2 steps in Figs. 2B and

3

A.

Timing of leg movements

Except at the very lowest speeds of locomotion (stepping frequencies less than about

3 Hz),

Periplaneta

always uses the alternating tripod gait. This may be seen qualita-

tively in the stepping patterns shown in F igs. 2 and 3. Clearly, the leg movements are

rarely synchronous; that is, the three legs comprising one tripod do not usually beg in

protraction at exactly the same instant. Nevertheless, the overall consistency of the

stepping pattern is also clear.


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448

FRED DELCOMYN

This consistency isreflected in thedistributions ofphase values. Exc ept at the ex-

treme low end

of

the range

of

walking speeds, there

is n o

significant change

in

phase

as afunction of the frequency ofleg mo ve me nt Fig . 6). Statistical tests su pp or t this

statement Table

2),

since

in no

case

is

there

a

significant correlation between phase

and frequency

of

leg mo vem ent when phase values corresponding

to

frequencies less

than 5 Hz are omitted. Th is is not surprising, of course, since phase is simply a

600

520

440

360

280

U 200

120

40

s

o

fP

Ofl,

8 J

6 10 14 18 22

Frequency

of leg

movement

(Hz)

26

Fig. 4. T he du ration of the two comp onents of each step , protraction filled circles) and retra c-

tion open circles), as a function of the frequen cy of leg movem ent of leg L 3) . W hile both

components occupy less time at higher frequencies of leg movement than at lower ones, the

rate of change is different for the two.

leasure of the timing relationships between th e

legs,

which in tu rn determine the gait

mployed during walking. The fact that the average phase of L1 on L3 and of R1 on

13 is0 954 indicates that each of the front legs generally begins protraction slightly

arlier than the corresponding rear legs, rather than at exactly the same time, as

rould be demanded for a rigid alternating triangle gait. At very low walking speeds,

t stepping frequencies of about 3-4 Hz, the protraction of each front and middle leg

egins earlier than usual relative to the ipsilateral rear legs, as shown in Fig.

B,

so

le corresponding phase values are reduced Fig. 6A). Th is change in phase at low

talking speeds occurs only in ipsilateral legs. The phases of contralateral leg pairs,

lat

is,

legs in a single body segment, do not show any reduction at low walking speeds.


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The

locomotion

ofthe

cockroach

449

T a b le

2.

Correlation and

regression

parameters ofthe phase distribution of

leg

pairs.

r ri)

Mean

Leg pair >5 Hzonly) r )

b

s.E. int. phase

R2,R

3

R i , R

3

L3.R3

R i,

R2

L2,Rz

L i ,

R I

L2 , L

3

L i , L

3

L i , L

2

0.1172

53)

0-2586

47)

-0-1293 53)

0-2207 52)

0-1045 52)

O-222I 56)

O-O3O8

50)

- 0 0 8 8 4

48)

- 0 - 1 6 3 8 54)

O-II28

62)

O-4953 55)

- 0 0 6 6 8 62)

0-3446 64)

0-0141

64)

- 0 1 8 2 8 6 6 )

0-2862

61)

0-1467

57)

- 0 - 0 5 4 3 63)

(Symbols

as

0-00079 0-00090

0-00500 + 0-00121

0-00042 + 00 008 1

0-00294 + 0-00101

0-00010 + 0-00091

000148+000099

0-00212 + 0-00092

0-00142 + 0-00129

0-00036 + 0-00102

in Table1.)

0-471

0882

0499

0425

0-508

0520

0-469

O-934

0-464

0-482

954

O-493

0 4 6 7

0510

0-500

0-499

O-954

-

459

1-8

r

1-2

0-8

0-4

1-8

r

1-4

1-2

0-8

0-4

15

2 3

Frequencyofleg movement Hz)

15 21

Fig. 5.Thep/r ratio of legs R3 (A) and R 2 (B) as a function of the frequency of leg movement,

with best-fit regression lines shown. There

is no

significant difference between

the

slopes

of

the distributions, butthere isbetween thevertical displacements, indicating that R 2 (and

L 2 , not shown) protractions

are

generally shorter at

any

given speed oflocomotion than

those

of

the remaining legs.See also Table 1 andtext.

Th is finding suggests the possibility that the m echanism(s) responsible for th e phasing

of leg movements may

be

different

for

contralateral leg pairs tha n

for

ipsilateral legs.

Descriptionofthe behaviourofanother parameterofthe timingofleg movements,

lag,

isimplicitinthe descriptionofphase given above. Phaseissimply lag dividedby

cycle duration. Since phaseisconstant over nearly

the

entire range oflocomotor

speeds, lag must bear a constant relationship to cycle duration, which issimplya

reciprocal function offrequency ofleg m ovement.

DIS C US S ION

While early work on insect locomotion had been concerned primarily withthe

correct description oflegmovement (e.g.Carlet, 1879;Morgan, 1886;Demoor,

1890),

current attention has turned

to

investigations

of

mechanisms by which patte rns


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45

FRED DELCOMYN

1-2

1 0

0-8

0-6

0-4

n.1

i.

I

o

__

A

oo

o

.

_ l

e

o

O

I

o

o

I

o

oo

c

a

o

I I I

12 15 18 21 24 27

0-7 r

0-5

0-3

0-7

0-5

0-3 U

I

L

I I I

I

0 3 6 9 12 15 18 21 24 27

Frequency of leg movement Hz)

Fig . 6. Pha se as a function of th e frequency of leg mov eme nt during walking. A. Op en circles,

phase of L i on L 3 ; filled circles, phase of L 2 on L 3 . Th ere is an apparent tendency for the

phase to fall at leg movements below about 3 Hz, reflecting the breakdown of the alternating

triangle gait below this speed. B. Open circles, phase of L i on R i ; filled c ircles, phase of

L3 on R3. There is no fall in phase at low speeds with these contralateral leg pairs. (The

horizontal lines in the graphs are i-o and 0-5 reference lines only.)

of leg movem ents might be generated (e.g. Hughes,

1957;

Wilson, 1965, 1966; Pearson

& lies, 1970; Delcomyn, 1971). The present work is especially relevant to some of

these . Pearson & lies (1970) have shown tha t alternating bursts of flexor and extensor

motoneurone activity can be obtained in partially de-afferented preparations of

Periplaneta,

suggesting that the production of these bursts may be under the control

of

a

central programm e generator. T heir results show an increase in both extensor and

flexor burst durations as the burst period increases (i.e. as the frequency at which the

bursts occur decreases), although the latte r relationship is a weak

one.

Th eir findings

fit reasonably well with the behavioural observation that

as

leg-cycle time increases, the

duration of both protraction and retraction increase. (In the leg they examined, R3,

flexion causes protraction, extension retraction.) T he weak relationship between flexor

burst duration and burst period would be accounted for if few or none of the flexor

muscles were active during the entire period of protraction (cf. the lobster swimmeret

system, Davis, 1968), so that the duration of a burst of activity in any one flexor


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Thelocomotion of thecockroach

451

muscle would not accurately reflect the duration of protraction. In this case, the re-

lationship between flexor activity and burst period would not necessarily be similar

to that between protraction and leg-cycle time, and their results would be fully com-

patible with the behavioural data.

The data reported above are also relevant to Wilson's (1966) model of insect

Wilson pointed out that with three conditions fulfilled, an insect's gait would be

a direct function of its speed of locomotion, over the whole range of speeds. These

conditions were that as speed of walking increased: (1) protraction remained con-

stant, (2) lag between ipsilateral legs remained constant, resulting in increasing phase

between them, and (3) phase between contralateral leg pairs in each body segment

remained constant at 0-5. Conditions 1 and 2 clearly do not hold for

Periplaneta,

so

that the gait of this insect does not change over most walking speeds. Wilson has

suggested (personal communication) that Periplanetamight be considered a 'fast

wa lker', that is, an insect in which gait is affected by speed of walking only at very

low speeds, and stays constant at higher speeds. While the data are not complete for

low-speed walking, they do suggest a change of gait as the animal slows down, and thus

support this notion.

Wilson based his model primarily on the work of Wendler (1964, 1966) on the

stick insect,

arausius

morosus, and Hughes (1952, 1957) on the cockroach, Blatta

orientalis.

The locomotion of

arausius

differs from that of

Periplaneta

in several

respects. As in

Periplaneta

the

pjr

ratio increases and retraction decreases with in-

creasing speed of walking, but protraction is constant. The phase of leg pairs within

a single body segment (e.g. L2 and R2) is independent of speed, as in the cockroach,

but phases of ipsilateral leg pairs drift, increasing as speed of walking increases. Thus,

in this insect gait is a function of the speed of locomotion, over the whole range of

walking speeds.

The results of Hughes (1952) on

Blatta

have been interpreted similarly (Wilson,

1966;Wendler, 1966). However, examination of his results suggests thatBlatta walks

more like

Periplaneta

than

Carausius.

Hughes sta tes: ' Cockroaches use very nearly

the same rhythm

(R1,

L 2 , R 3 , etc.) at all speeds from

1

to 15 cm/s [about 1-8

H z ] . . . '

(p.

279), and:

The same basic rhythm of leg movements is found at all speeds of

cockroach movement, although at the very slowest ones different rhythms may be

observed. But these grade insensibly into the normal rhythm with an increase in

speed . . . (p .280).The basic rhyth m is the alternating triangle gait (cf. Fig.3 Aabove),

as shown in some of the graphs of leg movements appearing in his papers (Hughes,

1952,

1957). None of the phase values which can be calculated from his data are su b-

stantially different from those forPeriplanetashown in Figs. 4 and 5 above. Thu s, in

Blatta,gait is independent of the speed of walking at medium and fast speeds, and is

a continuous function of speed during very slow locomotion.

Mechanisms of locomotion in stick insects and cockroaches need not be as different

as the above descriptions of their patterns of locomotion might suggest. In

Periplaneta

the data suggest that at stepping frequencies below 3 -4 Hz , gait is a direct function of

velocity. The data of Hughes (1952, 1957) suggest that non-alternating tripod gaits

inBlattaalso appear only below this stepping frequency (equivalent to about 5 -7 cm /s,

see Fig. 1).

arausius

is a mu ch more slowly moving animal, and while the alternating

triangle gait is used only at the highest walking speeds, the speed at which it appears

29 EXB 54


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THE LOCOMOTION OF THE COCKROACH PERIPLANETA AMERICANA

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