Cleaning behaviour in Drosophila melanogaster

Antm. Behav., 1969, 17, 641-651

CLEANING BEHAu

IN DROSOPHILA MELANOGASTER

BY ANDREW L. SZEBENYI, S.J. Biology Department, Le Moyne College, Syracuse, New York 13214 as soon as dust particles stick to them' (p. 85). From the author's own observations the following general statements can be made. Cleaning behaviour is performed with the legs by two different basic movements: the sweeping movements of the legs over the body surface, and the rubbing motion of the legs along the tarsal joints. It has been observed in D. melanogaster on several occasions that removal of macroscopic particles was actually achieved by these movements. A small piece of yeast particle adhering to the body surface has been seen to be picked up by the sweeping movements, while the rubbing that followed caused the particle to travel along the tarsal joints and to drop off at the end. The direction of the movement of the particle seemed to be determined by the direction of bristles on the legs where they all point away from the body. It is not at all certain, however, that removal of larger particles is the only result of this behaviour. It is quite possible that microscopic particles adhering to sensory receptors, Or the need for even distribution of wax-coating on the body surface play some role in eliciting the movements. Further investigation is needed to determine the causes and the effects of this behaviour. The behaviour presents a rich source of material for study, and many aspects of it may become important not only as a mere behaviour study but also as a new source for behaviourgenetic analysis. To investigate these aspects and possibilities of this widespread and probably highly adaptive behaviour complex, a survey has been initiated. What was sought, first of all, was some means of obtaining records which would make it possible to analyse and compare the cleaning performance in different individuals and populations in appropriate qualitative and quantitative terms. The progressive phases of these preliminary investigations were the following: (1) analysis of cleaning behaviour into recurrent components and the construction of ethograms based on the performance of D. melanogaster wild type flies; (2) discovery of the structural organization of the behaviour based on the ethograms and on continued direct observations. (Thes~ two

The objective of this paper is to give a descriptive account of a behaviour pattern complex in Drosophila melanogaster, generally known as grooming or cleaning behaviour, and to present methods which make the descriptive and comparative study of this behaviour complex possible. Very little is known about grooming or cleaning behaviour in Diptera, Apart from the fact that cleaning movements do occur, most other aspects of this behaviour, such as the nature of the eliciting stimulus, spontaneity of movements, stereotypy of patterns, the importance of sensory feedback during performance, and to a large extent even the biological significance of the behaviour remained hitherto obscure. Recently, Connolly (1968) described social facilitation of preening behaviour in D. melanogaster and showed that facilitation is probably induced through vision, and it is unaffected by physical contact between flies, or by the amount of dirt on the body. Another published work on cleaning behaviour in Diptera is that of Heinz (1949) describing the cleaning movements in terms of a number of components, and investigating some of the conditions which may be responsible for releasing or strengthening cleaning activity. In the same article, Heinz also reported his observations on cleaning behaviour in twenty-eight Drosophila mutants, and found the movements to be identical with those of the wild type. It should be noted, however, that the system of components used by Heinz was rather limited and did not extend to more precise quantitative aspects of the behaviour which may account for this statement. Apart from these two studies, there are only a few sporadic references in the literature to cleaning behaviour in Diptera. Lorenz (1956) remarked in a conference on instinct: 'in Drosophila wingless mutants are still in full possession of the normal movements of cleaning wings' (p. 55). Tinbergen (1965) referred to this observation as a possible example of spontaneous behaviour, cautioning however, that the apparent absence of external stimuli is n o t in itself a positive proof of spontaneity. He also maintained th.at 'flies will always preen their wings 641

642

ANIMAL

BEHAVIOUR,

phases of the investigation furnished the material for the present paper.) (3) Meanwhile a dissection of the behaviour into relevant quantitative aspects has been undertaken, and a method for quick and accurate determination of cleaning behaviour in terms of quantitative parameters of populations has been developed. This third phase of the investigation is now being tested, and the results will be brought to light in the near future. All these phases are primarily descriptive but they lay the foundation for meaningful experimental and comparative study of the behaviour. The present account is based on studies of D. melanogaster wild-type flies which were obtained at Syracuse University from a population cage in Dr Marvin Druger's laboratory. The cage contains mixed strains derived from single females caught at various localities in Syracuse in October 1964. The cage was started with 15 males and 15 females of each of 15 strains in 23 December 1964. The flies used for observation and record in this account were maintained in culture bottles since November 1967. They were raised on agar molasses media at a temperature of 23~ and at 62 per cent humidity in a constant temperature and humidity room. Observations were carried out in the same room. For observation the flies were either transferred into clean glass vials or were transferred into food vials, and a 5-min 'settling down' period was allowed before each observation or recording.

Ethograms: The Descriptive Method Looking at unetherized flies, one is immediately struck by the high frequency of occurrence, and by the complexity and great variety of movements of cleaning behaviour. In most instances, the movements are rapid, and they follow each other in quick succession which renders detailed observation an exacting task, and also limits the precision of direct visual observation. The alternative to direct visual observation is to make use of motion pictures. This latter method, although excellent for analysis of movements, is not the best to give routine permanent record because it does not render the quantitative characteristics of the performance immediately comparable. This can be achieved better by permanent written records or ethograms. Fortunately, there is a simple and inexpensive way to obtain such ethograms. The following is recommended: cleaning behaviour is observed l~n[il one b~om~s familiar with the general

17, 4

characteristics of the movements. Next, the performance is analysed into components, and each of these components is given a verbal symbol. The symbols should be sufficiently simple and short since they are to be pronounced as fast as the movements occur. The next step is to carry out systematic observations during which the verbal symbols are recorded on tape. At this point, one has to be completely familiar with both the movements and their corresponding symbols to avoid lag or confusion during the recording. If the movements flow into each other, it is sufficient to mark the end of a component by the beginning of the next, and to say 'stop' at the end of a series of movements. No recorded symbol after the word 'stop' means no observable movement. The next step is to play back the tape and to write down the symbols. This gives a written record of patterns. For more elaborate ethograms the duration of each component is to be measured from the tape with the aid of a timer. The ethogram obtained in this manner gives most of the essential parameters of the behavionr (patterns, duration, frequency) in a form which is easily and directly comparable. It is found that one can carry out visual observation at different levels of complexity, and that the study of some aspects of cleaning behaviour does not require a specially detailed record. It is, therefore, practical to work out a number of systems of symbols of different complexity. The selection of the appropriate system will depend on the nature of the problem at hand. For instance, the study of front versus back cleaning preference, that is, a type of cleaning which is performed with the first pair of legs, while the second pair is moved forward for cleaning, versus a type of cleaning which is performed with the third pair of legs while the second pair is moved back for cleaning can be described quite adequately by a very simple system of symbols (system I). It should be remarked here that the choice of symbols is entirely subjective. The symbols are simply useful in converting fly movements into generalizations for human understanding of the fly's behaviour, and in making a written record possible. System I Cleaning behaviour is performed with the legs, and may refer to various body parts and to the legs themselves. Thus, the components can be described by giving a number to the legs involved in cleaning (first, second; and third

SZEBENYI: CLEANING BEHAVIOUR IN DROSOPHILA MELANOGASTER pair), and by giving a letter symbol to the main body parts cleaned (H = head, T = thorax, A : a b d o m e n , and W--= wings). No more than three legs may be involved in cleaning activity at the same time because the fly requires at least three legs for support. It can often be predicted which leg is going to be used for cleaning by observing the preparatory movements of the supporti~g legs shifting the centre of gravity of the body to the required position. The system of symbols is the following.

Body cleaning movements (sweeping motions). 1H, any cleaning movement directed toward any part of the head. The movements are performed with the first pair of legs. 2H, same as above but the movements are performed with the second pair of legs (a rare component). 1T and 2T, any cleaning movement directed towards the thorax and performed with the first or second pair of legs respectively. 3A, any cleaning moveanent directed toward any part of the abdomen and performed with the third pair of legs. 3W, wing cleaning movements performed with the third pair of legs. 3TW, a symbol representing the sweeping movement of one of the third pair of legs over the dorsal side of thorax and wings. 3HTW, same as above except that the movement also includes the head. 3T, the initial phase of 3TW; the wings are, however, not touched. The component may appear in itself without going into the 3TW movement.

Leg cleaning movements (rubbing motions). 1, the rubbing motion of the first pair of legs. No other legs are involved in this component. 12, the movements include both first legs and one member of the second pair. The legs approach each other on one side. 21, the movements include one of the first and one of the second pair of legs on one side. 2112, the above two components flow into each other. The 21 part is often very short. 32, the movements include both third legs and one member of the second pair which is moved back for cleaning. The performance is slightly to one side. The legs cleaning usually touch the ground and form additional support for the body. 3, rubbing movements performed with the third pair of legs. No other legs are involved in this component. 1C, performed with one of the first legs cleaning the coxal region of the other member of the first pair. The component is associated with the rigid extension of the leg cleaned. While the leg cleaning movements l~ormally mean ~h~ rubbin~ motio~ of the le~s

643

along the tarsal joints, this component is an exception. Experience in the use of symbols shows that recording from direct visual observation cannot go far beyond system I. The following systems are more suitable for analysis of motion pictures.

System H The description of components is extended to finer subdivisions of body parts. The leg cleaning components are the same as in the previous system. For sake of simplicity, the body cleaning components are not all prefixed by the number of legs involved in the activity but most of them have their own letter symbol. Head cleaning movements. F, all cleaning movements directed towards the front part of the head, antennae, front part of the eyes, ocelli (while head is bent down), and proboscis. The proboscis is not extended while the region is being cleaned. I, all cleaning movements directed towards the lateral sides of the head and eyes. The head is not turned during these movements. H, a characteristic head cleaning component. The movements clean the dorsal and ventral sides of the head at the same time while the head is rotated to various degrees to the right or to the left. P, proboscis cleaning component. The proboscis is extended for cleaning. All these components are performed with the first pair of legs. 2H, a rare component (see system I). Thorax cleaning movements. 1V, the ventral side of the thorax is cleaned with the first pair of legs. The fly usually takes up a posture at an angle to the horizontal and balances on four legs forming three supporting points, one of the second legs being extended parallel with one of the third legs on the same side. 2T, any cleaning movement directed towards the thorax and performed with the second pair of legs. One may distinguish between 2TD, 2TS, and 2TV depending on whether the dorsal, lateral, or ventral sides of the thorax are being cleaned. 3T, the dorsal side of the thorax is cleaned with one of the third pair of legs. The component is identical with the initial phase of TW movements.

Abdomen cleaning movements. D, S, V, and G. These symbols refer to dorsal, lateral, and ventral sides of the abdomen, and to genital and anal regions ((3) cleaned with the third pair of legs. The anal plates and the reproductive organs may or may not be ~xLen0r during cleaning.

644

ANIMAL

BEHAVIOUR,

Wing cleaning movements. B, the wing base is cleaned with one of the third pair of legs which is inserted at the inside angle of the wing. The movements are usually slow and protracted and are accompanied by slight opening and raising of the wing. K, a rather rapid movement which consists of a sharp kick against the underside of the wing. The wing is lifted by the movement. VS, SS, DS. The symbols represent the sweeping movements of the third pair of legs over the wing surfaces. The ventral sweep (VS) is often not distinguishable from movements cleaning the dorsal side of the abdomen (D). The dorsal sweep (DS) is similar to TW but the movement does not include the thorax. The lateral or side sweep (SS) refers to the movement along the outer edges of the wings in a parallel fashion. TW, and HTW, the same components as 3TW and 3HTW in system I. W, the most characteristic wing cleaning component. The wing is taken between the two third legs which move in a see-saw fashion along its dorsal and ventral surfaces. Several phases can be distinguished in this component. At an early phase, the wing is still in a near horizontal position, at the end phase, the wing is vertical. All these wing cleaning components are performed with the third pair of legs. Various modifications of the W component can be observed clearly in D. melanogaster vestigial mutants, and in other wing mutants of this species, such as unfolded and pupal. This is probably the component referred to by Konrad Lorenz (1956, p. 55). System III In addition to systems of symbols used in the previous account, the problem of symmetry may be dealt with by using subscripts R, L, and P meaning right, left and parallel, depending on the symmetry of the movements. For instance, WR, DSP, and 12L would mean cleaning of the right wing according to the W component, sweeping movement along the dorsal surfaces of the wings performed on both sides simultaneously, and the performance of the one-two component on the left side. Figure 1 shows the most commonly occurring cleaning behaviour components in D. melanogaster wild-type flies. The drawings, obtained by tracing single frames of motion pictures, are schematic, and in them several structural details were omitted to place emphasis on postures and movements. For the same reason, the wings are shown only in outline. The addition of v~n~tion on the wings would have. obsc_ur~d

17, 4

some of the legs. Each drawing is accompanied by the symbol of the component it represents according to system II. Figure 2 is an example of ethograms of cleaning behaviour in the D. melanogaster wild-type studied. The ethogram was obtained by analysis of motion pictures, using the described method. The movie was taken at 24 frames per sec, and was played back at 6 frames per sec. The duration of each component was measured at the low speed, and the true durations were calculated for the ethogram. The symbols follow system II. The ethogram is a sample observation of 280 sec duration of which 4.9 sec were spent in locomotion, 140.9 sec in cleaning, and 134.2 sec in motionless state. The performance is presented at three levels: the top level shows locomotion, the middle level cleaning, and the bottom level the rest periods during which no observable movement has occurred. The Problem of Error In preparing an ethogram, the final written record is based on a series of transformations. In case of direct visual observation, the event is first seen, and what is seen is expressed and recorded on tape by verbal symbols. Playing back the tape, what is heard is timed and written down. At each step in this series of transformations from the actual event to the written record there are a number of sources of error due partly to the observer and partly to the instruments used by the observer, in this case the tape recorder and the timer. If the visual observation is indirect, that is, if one makes use of motion pictures, additional sources of error are introduced by the movie camera and the projection equipment. Thus, the written record is rather far removed from the actual event it is supposed to represent. In order to see how closely the written record approximates the event, it is necessary to form some ideas about the magnitude and the direction of errors introduced by the transformations. It is customary to distinguish between systematic and random errors where the former refers to the accuracy, the latter to the precision of the results. It seems that systematic errors inherent in the equipment are of no real significance because the comparison of records requires no more than relative accuracy, and because it was found that random fluctuations in the recording and timing instruments were in practice negligible. The major cause for concern is the error introduced by the observer at the point of tra nfforrnatior~ of visual impressions into verbal

9ZEBENYI: C L E A N I N G B E H A V i O U R i N DROSOPHILA MELANOGASTER

I

12

-21

IC

f

64~J

52

i

~

.

\

3

G

I

H

P

B

IV TOP VIEW

3T

% IV SIDE VIEW

o

f

<

"l K

SS

iJ

VS

W EARLY AND LATE PHASES

Fig. I. The most commonly occurring cleaning behaviour components in D. melanogaster wild type flies. For the definition of symbols see system II in text,

L.

~46

ANIMAL

BEHAVIOUR,

17, 4

I_

,.oO

i

oo

12

~

I I

II

r

o

E Z

0

~

~

O--Z

~Zo UW

o-0

No

o

SZEBENYI: CLEANING BEHAViOUR iN DROSOPHILA MELANOGAST~ER symbols, and at the point of timing the duration of components from the tape. Each of these transformations had to be tested for the magnitude and direction of error, and for any cumulative effect. First, the precision of timing was tested. A randomly selected portion of the tape was played back ten times, and each time the duration of behaviour components was measured with an electric timer which reads in sec and tenths of sec. To aid the precision of measurements, the sequence of the components was first written down. In this way each component could be anticipated. To aid accuracy, the bar switch of the timer was eliminated and a sensitive microswitch was installed in its place getting rid of most of the lag associated with pressing down on the bar switch. The portion of the tape contained twenty behaviour components of a total duration of approximately 118.5 sec. of cleaning. The components were measured in a cumulative fashion, that is, the timer was not reset to zero after each measurement but only after all the twenty components had been timed. From these cumulative data the actual duration of each component was computed by subtraction. The ten measurements of each component were then processed for sample average, standard deviation, and relative percentage error expressed 2a as = • 100 where N is the average of the ten x measurements of the same component. The relative percentage error was calculated to show the relationship between duration of component and error of measurement. The results were rather encouraging. The range of relative percentage error was between 1 per cent and 20 per cent with an average value close to 8 per cent. The error is clearly related to duration of component and not to any cumulative effect of successive measurements. Table I gives the results of these computations. The next step was to see the precision of transformation of visual observation to verbal symbols. This was obtained in the following manner. Cleaning behaviour was recorded on film which was then replayed ten times, and each time the components were recorded on tape with the aid of verbal symbols. Each independent recording was then measured for duration of components, and the measurements were subjected to the same statistical analysis as in the previous case. To aid the precision of recording, a number of preruns were made with the film to become familiar with the sequence of

d4~

Table I. Sequence of 20 Sampleaverage components of 10 measurements of the same components (sec)

cr

2or - - x 100

1

0-9

0'06

13-3

2

4"8

0.08

3-3

3

1'8

0.06

6.7

4

1.6

0"07

8.8

5

1"2

0'07

11-7

6

1"8

0"10

11'1

7

0"6

0"04

13"3

8

7-5

0'06

1"6

9

1"5

0"11

14'7

10

3.7

0'06

3"2

11

8"6

0"07

1-6

12

4"5

0"15

6'7

13

2'6

0"14

10'8

14

14"2

0"2

2'8

15

36'0

0"18

1"0

16

1"1

0'06

10"9

17

0"5

0'05

20'0

18

6"5

0'08

2"5

19

1"7

0'09

10'6

20

17"5

0"10

1"1

events. The portion of the film contained twentytwo behaviour components. The average relative percentage error was found to be close to 16 per cent, approximately twice as great as in the previous case. Thus, it may be concluded that the process of transformation from visual observation to verbal symbols, on the average, introduces approximately 8 per cent error. This random error was found to be relative to the duration of components, and was free of cumulative effects.

The Organization of Cleaning Behaviour At first sight, as illustrated by the ethogram, cleaning behaviour is not only a complex phenomenon but the observation of its performance gives the impression of a bewildering

648

ANIMAL

BEHAVIOUR,

variety of movements apparently without any definable system. The comparison of many ethograms and continued direct visual observation, however, begin to reveal some consistencies of performance, such as the regular sequence of the two basic types of movements (sweeping and rubbing) separating the behaviour into body and leg cleaning types; the characteristic shifts of the centre of gravity of the body prior to a given type of cleaning involving one, two or three legs; well-definable postures which often accompany some sets of cleaning movements; the relatively high frequency of occurrence of some components over others; the stereotyped nature of some movements and patterns; the repetitive character of components and of subdivisions of components. These are no more than scattered observations. Nevertheless, they indicate that cleaning behaviour in its complexity does have organization. The behaviour is found to be built up of simple movements and of the repetition of these movements forming complexes which are recognized as behaviour components, while the components themselves are repeated forming major structural elements of the behaviour. One of the most fundamental features of this behaviour is its repetitive character. During the course of a longer period of time, such as during the course of a day, cleaning behaviour is being repeatedly performed. Each cleaning bout may be regarded as a complete unit on the behaviour level. It is not known whether these bouts are spread out in time evenly, having approximately the same duration and the same length of intermission periods between them, or whether there exists some variation of behaviour density in time, and if so, whether such variation is in any way correlated with particular times of the day. The random variation of behaviour density cannot be a priori excluded either. In any case, at this higher level of organization, the behaviour consists of the repetitive performance of cleaning bouts. There is some difficulty about the unambiguous definition of cleaning bouts in time. The sources of uncertainty are partly the indefinite end of the bout, and partly the fact that other behaviour types, namely, walking, feeding, mating, motionless state, and so on, often intrude during the performance of a cleaning bout. It is more realistic to speak of the dominance of a given behaviour type over others at any given period of time in the range of the bouts. The situation is similar to a woven meshwork

i?,

4

of cotoured fabric where at any area in the range of patterns a certain colour dominates others. In spite of these ambiguities, there are some well-definable features of the cleaning bout. Its beginning is often clear cut. The fly may be engaged in various kinds of activities when suddenly cleaning begins with an eruption of movements. During the cleaning performance, other behaviour types may intrude, most commonly walking and motionless state. If care is taken not to disturb the flies, the motionless state becomes more and more predominant over cleaning, and finally cleaning disappears altogether. Then cleaning may start again, or some other behaviour type takes over. Because of the intrusion of other behaviours each cleaning bout may be subdivided into smaller activity units on the behaviour level. As it has been mentioned earlier, cleaning behaviour is performed by two basic types of movements, the sweeping and the rubbing movements. Based on this distinction, each cleaning activity unit may be broken up into the repeated alternations of the two movement types, that is, into a series of alternating body and leg cleaning complexes. This subdivision of the behaviour is probably artificial. It is suggested that one set of body cleaning movements is followed by one set of leg cleaning movements, and they together represent the natural unit cycle of cleaning activity. The concept of unit cycle is consistent with the view that the primary function of the behaviour may be the removal of foreign material from the body surfaces, and thus the two movement types are part of the same natural unit of cleaning activity. That this may be so is indicated by the ethogram in the 53, 56, 69, 73, 152, 169, 171, 188 and 225 sec regions. The ethogram was selected to show some of the exceptions to this interpretation. Front cleaning activity--that is cleaning performed with the first pair of l e g s - i s often preceded by an initial set of rubbing movements, as can be seen in the ethogram in the 0 to 33, 108, 135, 148 and 187 sec regions. In addition, the H, W, and VS components often terminate the cleaning activity without being followed by the rubbing movements of the legs, as in the 16, 33, 103 and 205 sec regions. Each unit cycle may be subdivided into behaviour components depending on the leg or legs involved in the cleaning activity, or in the body part toward which the behaviour is directed. In this paper seven leg-cleaning and twenty body cleaning components have been described.

SZEBENYI: CLEANING BEHAVIOUR IN DROSOPHILA MEZANOGASTER A given behaviour component may occur several times within the same unit cycle, and there may be several different components in each activity type. The components are made of repeated sets of movements. The leg cleaning components, for instance, are built up of a number of repeated rubbing movements. The individual rubbing movements are similar and they represent the lowest level of organization of leg cleaning behaviour. Since the rubbing motions are mostly along a straight line, they may be regarded as one dimensional motor units. The organization of the body cleaning components is more complex because of the bilateral symmetry of the body surfaces, and because the sweeping of surfaces requires two dimensional movements. The repetitive character of the behaviour is extended to both of these aspects. The most characteristic wing cleaning component (W) may serve as an example. The wing on the right or on the left side is taken between the third pair of legs near the wing base. It is held at a slight angle to the horizontal. The legs then perform one sweeping movement from base to tip of the wing and at the same time many small sweeping movements over the wing surfaces between the inner and outer edges. The motor units are thus two dimensional. Toward the end of the component, the wing is bent and is nearly vertical. This set of movements is then often repeated on the same wing several times, and then on the other wing, or on alternate wings. Thus the repetition of similar elements within the same component occurs at a number of different levels of organization: bilateral repetitions of the entire component, unilateral repetitions of sets of movements, and finally the repetitions of two dimensional simple movements (Fig. 3). Not all body cleaning components have the same complexity of organization. For instance, the dorsal sweep (DS), another wing cleaning component, has three aspects of repetitive symmetry: the bilateral alternating, the bilateral parallel and the unilateral repetitive performances. It lacks the two-dimensional motor units, there being only repeated, smooth, onedimensional sweeps over the dorsal surfaces of the wings (Fig. 3). The side sweep (SS), another wing cleaning component, is even simpler. It consists of a few times repeated, uninterrupted sweeps along the outer edges of both wings at the same time. Thus the repetitive symmetry of the component is

649

reduced to the parallel state, :while the motor units are one dimensional (Fig. 3). The bilateral character of the components may also appear as movements to the right or to the left of the body part cleaned, as in the most typical head cleaning component (H). Here the head is rotated to the right or to the left while the first pair of legs carry out two dimensional sweeping movements over the dorsal and ventral surfaces of the head (Fig. 3). Thus it is found that cleaning behaviour in D. melanogaster wild-type flies is not a random aggregate of a great variety of movements, but the behaviour is organized into a hierarchy of repetitive complexes. The dgily cycles of the behaviour(?) are composed of cleaning bouts which are broken up by the intrusion of other behaviour types into activity units. Each activity unit is composed of sets of body and leg cleaning movements (unit types) which together probably form the natural units of cleaning on the behaviour level, the unit cycles. Each unit type consists of sets of behaviour components. Because of the repetitive nature of the behaviour, the movement complexes associated with the components may be classified according to three aspects of repetitive symmetry: bilateral alternating, bilateral parallel, and unilateral performances. Each of these complexes is built up of repetitions of simple movements along one or both coordinates of a Cartesian space, forming two- or one-dimensional motor units, the fundamental building blocks of the behaviour. Summary A descriptive account of cleaning behaviour in D. rnelanogaster wild-type is given. The behaviour complex is analysed into seven leg cleaning and twenty body cleaning components. A method of obtaining ethograms is presented. The method consists of a series of transformations from event to written record with the aid of verbal symbols recorded on tape. Three systems of symbols of increasing degree of complexity are proposed, and their usefulness is illustrated by an actual ethogram. The problem of error introduced by the series of transformations is discussed. It is found that ethograms may be constructed by the method with reasonable degree of precision. The overall average relative percentage error is found to be approximately 16 per cent, one half of which is caused by the transformation from event to verbal record, the other half by the process of timing the duration of components from the tape. The

ANIMAL

650

BEHAVIOUR,

17,

4

A

[3

W

IL ,,~,

--r

[3

I

c

/

i [35

C

.

$9 A

H

1

[3 Fig. 3. Diagrammatic representation of the repetitive organization of four cleaning behaviour components in D. melanogaster wild type flies. The components are in sequence W, DS, SS, and H. (For the definition of these symbols see text.) The movement complexes associated with these components may be classified according to bilateral repetitive symmetry (A), unilateral repetitive symmetry (B), and bilateral parallel symmetry (C). The components are built up of repetition of simple movements performed along the two axes of a Cartesian space (two-dimensional motor units), or along a single line (one-dimensional motor units). The vertical arrows re. present the direction of the main movement, while the double-headed arrows indicate the direction of small movements superimposed upon the main movement. The broken arrows show the direction of movement of body parts cleaned, as in the case of the H component.

SZEBENYI: CLEANING BEHAVIOUR IN DROSOPHILA MELANOGASTER magnitude of this error is dependent on the duration of components, and is free of cumulative effects. The organization of Cleaning behaviour is discussed. The behaviour is not a random aggregate of a great variety of movements, but it is organized into a hierarchy of repetitive complexes from the daily cycles down to the smallest building blocks of the behaviour, the m o t o r units. One of the most fundamental features of this behaviour is its repetitive character.

Acknowledgments The author would like to express his sincere gratitude to D r M. Druger and to G. Smith for their professional assistance and to the Society

651

of the Sigma Xi for a generous research grant which made this work possible.

REFERENCES Connolly, K. (1968). The social facilitation of preening behaviour in Drosophila melanogaster. Anita. Behav., 16, 385-391. Heinz, I-I-J. (1949). Vergleichende Beobachtungen fiber die Putzhandlungen bei Dil3teren im allgemeinen und bei Sarcophaga carnaria L. im besonderen. Z. TierpsychoL, 6, 330-371. Lorenz, K. (1956). The objectivistic~theory of instinct. In L'instinct clans le comportement des animaux et de l'homme (ed. P. P. Grassr). Paris: Masson et Cie. Tinbergen, N. (1965). Animal Behavior, pp 85-86. New York: Life Nature Library, Time Inc. (Received 3 July 1968; revised 2 February 1969; Ms. number: A724)