Behavioral development of the cockroach (Periplaneta americana)

J. Insect Physiol., 1977, Vol. 23, pp. 213 to 220. Pergumon Press. Printed in Great Britain.

BEHAVIORAL DEVELOPMENT OF THE COCKROACH (PERIPLANETA PMERICANA) ROBERT R. PROVINE Department

of Psychology, University of Maryland Baltimore County, Baltimore, Maryland 21228, U.S.A. (Received 9 June 1976; revised 20 August 1976)

Abstract-The 12 to 16 cockroach pharate first instar larvae (Periplaneta americana) which inhabit a single ootheca simultaneously eclose and hatch after 30 days of incubation at 29°C. Descriptions of behavior development were obtained by observing larvae which were removed from the oijtheca after 16 to 18 days and incubated individually in organ culture dishes. The first movements were localized muscle twitches and depressions of the soft cuticle which first appeared at approximately 16 days. Coordinated multisegmental flattening movements of the abdomen and wave movements which rippled through the entire body appeared by 20 to 22 days. The frequency of larval movements increased up to 26 to 27 days and then decreased until hatching around day 30. Up to 28 days, most larval movements were localized twitches. The proportion of coordinated multisegmental movements increased from 18 through 29 days when they became the most frequent type. Larvae were largely quiescent on days 29 to 30 when eclosion and hatching movements were spontaneously initiated. Eclosion and hatching are performed concurrently using the same caudal to rostra1 peristaltic wave movements. All of the 12 to 16 larvae occupying a given oijtheca eclosed and hatched simultaneously. Ligation of various body regions indicated that neither the head nor thorax were necessary for the performance of the rhythmic eclosion-hatching movements of the abdomen once they are initiated. Also, larvae with mid-abdominal ligations maintained asynchronous eclosion waves on both sides of the ligation, indicating that a given abdominal ganglion is capable of organizing the patterned motor output within its own segment and that any abdominal ganglion is capable of triggering eclosion movements in the adjacent rostra1 segment. The eclosion-hatching movements of the pharate first instar larvae are immediately terminated when the cuticle is removed. The first instar larvae which emerge are miniatures of the adult and perform the typical adult locomotor gait.

1976a; SIKES and WIGGLESWORTH,1931; TRUMAN and SOKOLOVE,1972). Instead of focussing upon a specific UNTIL recently, little attention has been directed action pattern, as have many previous studies, the toward the ontogeny of movement and its neural present work takes a broader perspective and anabasis in insects and other invertebrates (BENTLEYand lyzes the development of the pharate first instar HOY, 1970; BERG, 1972; BERRILL, 1973; DAVIS, 1968, larva* of Periplanetu americnna, tracing motility from 1973; DAVIS and DAVIS, 1973; KUTSCH, 1971; PRO- its inception at about half-way through incubation VINE, 1976a, b; PROVINE et al., 1976; TRUMAN, 1971; in the ootheca, up to and including its culmination WIGGLESWORTH, 1972; WITT et al., 1972; YOUNG, in eclosion and hatching when adult-type locomotor 1973). This contrasts with the relatively sizeable literaactivity appears. Ligation and nerve cord sectioning ture concerning the neuro- and behavioral embryoexperiments were performed in an attempt to locate logy of vertebrates which has accumulated over the the neural mechanisms involved in eclosion and past hundred years (GOTTLIEB, 1973; HAMJXJRGER, hatching movements. 1973; OPPENHEIM, 1973; PROVINE, 1973, 1976b). Only a few invertebrate behaviors have been examined MATERIAL AND METHODS from a developmental perspective, with eclosion and hatching being among the most popular topics (BEROiithecae were collected daily from the cage floor RILL, 1971; DAVIS, 1968; OPPENHEIM, 1973; PROV~NE, of a laboratory colony of Periplaneta americana. The oothecae were placed in Petri dishes which were kept humid with wet cotton and incubated in the dark at 29°C. After 16 to 18 days incubation, individual *The uharate frrst instar larvae described in this and larvae were removed from the oiitheca and placed other work by the author (Provine, 1976a) were previously in organ culture dishes. Details of this procedure are called ‘embrvos’ , the first _ (PROVINEet al.. 1973, 1974. 1976): described in Paovr~~ (1976a). The culture dishes were instar larvae which emerge after ecdysis and hatching are identical to the first instar ‘nymphs’ referred to in earlier kept in a darkened incubator which was maintained reports. at 29°C between observation sessions. 213 INTRODUCTION

ROBERT R. PROVINE

214

Larval movements were observed with a dissecting microscope at 25 x or in rare cases at 50 x . Larvae were viewed through the tops of the clear plastic culture dishes in which they were incubated. Low level illumination from the microscope light source provided both illumination and heat adequate to maintain the temperature within the dish at the incubation level, 29°C. The experimenter responded to visually observed larval twitches by activating one of two oscillograph event markers. One channel was used to register isolated segmental movements or twitches. A second channel registered m&segmental movements, which were primarily peristaltic waves or dorsal-ventral abdominal flattening movements. Weak pulsations of the circulatory system were not recorded. The standard observation period was 30min. Larvae were observed daily between 2 to 8 p.m. If a larva died during incubation, records obtained from that larva were discarded.

RESULTS I. 06theca

and larval morphology

The oiitheca resembles a small bean with a notched ridge on one side. Within the oijtheca, 12 to 16 translucent white pharate first instar larvae are grouped in two opposed rows of 6 to 8, with the larvae in each row lined up side-by-side. The larvae of both rows face inward toward each other and the center of the ootheca. Each of the larvae is ensheathed in an individual chorionic membrane. The heads of all larvae are oriented toward the notched edge of the ootheca through which the larvae respire (WIGGLESWORTH and BEAMENT, 1950, 1960). During hatching, the larvae pry open the clam-like ootheca along a seam which runs along the mid-line of the notched edge and emerge. Few major changes in body proportions occur during the second half of incubation, the period of concern in the present study. The body segments are clearly defmed and the legs, antennae and cerci are differentiated and lie folded against the ventral part of the body (Fig. 1). After about 16 days, the eyespots darken and enlarge. Body bristles appear at about 26 to 27 days. The bristles are pinned beneath the transparent cuticle until the time of eclosion and hatching, when they are freed. The first instar larva which emerges after hatching and eclosion has the general appearance of a miniature adult, with the exception that it has no wings.

A behaviorally significant anatomical consideration is that the body surface of the first instar larva is soft and flexible; tanning and hardening of the cuticle do not take place until after eclosion and hatching. Because the larval cuticle is soft, the legs and other body parts are capable of little movement. Muscle contractions result in a twitch or depression in the cuticular surface against which the muscles are anchored. II. Larval behavior development A. Qualitative aspects. The earliest observed movements were infrequent, weak, slow depressions in the cuticle (dimpling), which most often appeared in the upper leg region of the prothoracic segments of 16to 17-day first instar larvae.* A single dimpling movement may last from approximately one to many seconds. By 18 days, dimpling was observed in the upper portion of all legs as well as in the lateral wall of the thorax. Less frequently observed was dimpling of the lateral regions of the mid-abdominal segments and head. There seems to be no intersegmental organization of movement beyond a possible weak coupling which may be reflected in a tendency of different parts to be coactive during a given interval. Movements of the cardiovascular apparatus were not considered. At later stages, there was an increase in the variety, frequency, and amplitude of movements in addition to an increase in the number of motile body parts and segments. At the 20-day stage, infrequent, weak, coordinated multisegmental movements were observed in about half of the larvae in addition to the more frequent isolated dimples and twitches. The multisegmental movements were synchronous dorsalventral Jlattenings of the abdomen which were similar to the ventilation movements observed in posthatching cockroaches (MILLER, 1966). By day 22, the majority of larvae showed at least one such flattening movement during a 30-min observation period. The flattenings usually occur in series, with regular intervals between the movements of a given series. The 22-day stage also marks the onset in a few larvae of another form of multi-segmental activity, the wave.

Imm Cd)

* The first movements may appear a day or more earlier but these infrequent movements are not a primary concern at this report. Because larvae younger than about 16 days are like yolk-filled bags with weak body walls, they tend to spread out when removed from the chorion. This spreading increases the pressure on the body walls and probably restricts movement.

Fig. 1. Sketch of a single pharate first instar larva which has been removed from the ootheca and stripped of its chorion. The general body proportions of this larva are typical of those examined during the interval of study. The eyespot appears and darkens during the last half of incubation and hairs and bristles (not shown) appear beneath the cuticle after approximately 26 days.

Cockroach

behavior

These are ripples of muscle contractions which pass smoothly from segment to segment throughout part or all of the body. At 24 days, more flattening movements are observed and, for the first time, a majority of larvae perform multisegmental waves. The waves may begin iti either the thorax or abdomen and sweep either rostrally or caudally or occur in midbody regions and propagate in both directions. Occasionally, waves will be simultaneously initiated in different body parts and collide in intermediate regions. Following these wave collisions, the larva is often racked by a series of twitches. Another behavior pattern making its appearance at 24 days is the shudder. These are vigorous tremors which occur simultaneously in all body segments. A notable change in behavior between 24 and 29 days involves an increase in the proportion of multisegmental, relative to local, movements, particularly after 26 days. The multisegmental movements of older larvae are also stronger and more clearly organized than thdse observed earlier. For example, the indistinct waves or ripples characteristic of early stages are transformed into vigorous peristaltic movements with precise and regularly timed sequences of segmental contractions. The ripples of early stages are more suggestive of a general wave of excitation spreading through the body than of a coordinated intersegmental behavior pattern. At later stages, there are more frequent and longer episodes of flattening movements and occasional dorsal and ventral bowing movements of the entire body. The 29th and 30th days are characterized by very low levels of activity and the appearance of eclosion mouements. These movements consist of series of vigorous caudal-to-rostra1 peristaltic waves and ventral thoracic flexures which occur at regular intervals of 5 to 6 set (see below). B. Frequency of movement. Two clearly discriminated general types of behavior were counted: segmental and multisegmental movements. Segmental movements are local, isolated twitches or dimples appearing in a given body segment, or concurrently occurring but otherwise disorganized movements in different body segments. Multisegmental movements include synchronous, in-phase contractions of several body segments, such as the dorsal-ventral flattening or wave-like activity which moves through the body of the larva. The frequency of all segemental and multisegmental movements are summed at each developmental stage to yield a third category, total movements. The number of larvae observed at each stage

Table Age in days N * Number

I.?. 23/2-u

of oijtheca

development

215

of incubation and the number of oothecae from which they were taken are given in Table 1. The frequency of larval movement observed during a 30-min observation interval at different stages of development is presented in Fig. 2. The number of total body movements increased up to a peak at 26 to 27 days and then declined until the time of eclosion and hatching at approximately 30 days. However, segmental and multisegmental activity show different developmental trends. The number of segmental movements increased from a low level on day 18 up to a peak at about 26 days and then sharply declined. In contrast, multisegmental movements, which consist primarily of abdominal dorsal-ventral flattenings, increased in frequency from their time of appearance on about day 20 up to day 26, after which their frequency doubled in a single day. The increased 400 Movements: H Local n--oMuitisegmental w

5

Tota

I

u-/q

E 300

\ /I

k?

Fig. 2. Frequency of spontaneous movement of 1% to 3@-day pharate first instar larvae during a 30-min observation period. Observations were of larvae stripped of their chorions and incubated singly in organ culture dishes. Local (segmental) movements are isolated muscle contractions within a single segment. Multisegmental movements are coordinated contractions involving several segments. These include simultaneous dorsal-ventral abdominal flattening movements and peristaltic waves. Total movements are the summed local and multisegmental movements at a given stage. Local movements increase in frequency up to a peak on day 26 and then decline until hatching-eclosion behavior starts on day 30. Data from eclosing embryos are not included in the figure. Multisegmental activity, which primarily consists of flattening type movements, increases up to 26 to 29 days and then declines. Flattening is the most common movement on day 29.

1. Number

of larvae

18

20

22

24

26

27

28

29

30

14(5*)

8(3)

13(4)

16(4)

B(5)

lO(3)

lO(4)

8(3)

15(6)

from which

larvae

were taken

given in parentheses.

216

ROBERT R. PROVINE

number of flattening movements which is observed as a function of increasing larval age is largely due to the occurrence of more frequent and longer-lasting episodes of flattening movements. On days 29 and 30, multi-segmental movements were the most commonly observed behavior. The multi-segmental movements are usually over a second in duration, while the segmental twitches may last only a small fraction of a second. Therefore, if the total time spent in motility were computed, the multisegmental movements could make a relatively larger contribution than would segmental activity. C. Periodicity of movement. The most common periodically recurring behavior is the multi-segmental dorsal-ventral flattening movement. This movement is usually executed in clusters with regular intermovement intervals of approximately 5 to 6 set between the movements of a cluster. The intermovement interval histograms of flattening movements sampled from within movement clusters of five 22-day and five 29-day larvae are shown in Fig. 3. The mean intermovement intervals for both larval stages are similar. The peristaltic eclosion movements which appear at the terminal stages of incubation also occur at regular intervals of 5 to 6 set (Fig. 4, see below). Among segmental movements, dimpling within a given segment most often shows a regular periodicity (1 to several set). However, regular periodicity is not typical of segmental movements. Visual examination of entire 30-min event marker records of summed movements (segmental plus multisegmental) from each embryo observed from 18 to 30 days detected no evidence of clear cut cyclic phenomena with a longer period than the 5 to 6 set described for flattening and eclosion. Thus, while larvae show intervals of generalized activity and inactivity, most behavior is better described as intermittent than periodic. III. Eclosion A. General considerations. Eclosion refers to a series of coordinated, stereotyped caudal-to-rostra1 peristaltic waves and ventral body flexures occurring at regular intervals of 5 to 6sec which enable the larva to shed its cuticle (PROVINE, 1976a). Initially, eclosion movements will be described for single larvae raised in culture dishes. The role of the eclosion movements in hatching will be discussed later. During the 29th day of incubation, few movements of any kind are observed (Fig. 2), with many larvae remaining completely immobile during an entire 30-min observation period. Late on the 29th or on the 30th day, vigorous, smooth, caudal-to-rostral peristaltic waves of contractions pass through the abdomens of the larvae. When the wave reaches the thorax, it is propagated as a segment-to-segment ventral flexure. Dorsal thoracic flexures and rotational movements of the abdomen are occasionally interspersed with these behaviors. A few larvae performed a series of eclosion movements and temporarily halted while others started and continued until eclo-

sion was complete. If the eclosion movements were sustained, they OCCUTTCd at a mean intermovement interval of 5.46 $1 + 2.38 set (S.D.), as shown in Fig. 4). Air swallowing is performed concurrently with eclosion movements. The swallowed air bubbles may be seen inside the translucent bodies of the larvae. After the beginning of the eclosion movements, the previously sleek cuticle becomes slack and wrinkled, which is due, at least in part, to the combined effects of the stretching by the body movements and the increase in body volume which is brought about by air swallowing. The first tear in the cuticle appears along the dorsal surface of the thorax. The thin cuticle is then passed over the head and moved caudally along the remainder of the body. Removal of the cuticle transforms the soft, delicate immature-looking pharate first instar larva into a larva which has the general body proportions of the adult. Eclosion frees the body bristles and cuticular plates, which were previously pinned beneath the cuticle. Also, the antennae, cerci and legs, which lay passively against the ventral surface of the larva during incubation, assume their mature positions after eclo6022 days x =6.4lsec

50-

;D:

40-

1.5; set

N'=5

3020ln 0 IO> z + .c 0 Z',sOh 550z 40-

29doys X =5.32sec ;D;F)tiFsec N1=5

30-. 2010rt 0

2

4

I I ,I 6 6

Intermovement

I I I L I I 0; IO 12 14 16 intervals,

set

Fig. 3. Intermovement interval histograms of abdominal dorsal-ventral flattening movements of 22 and 29 day pharate first instar larvae. One hundred intervals (NJ were sampled from five larvae (N) at each stage. (Twenty ititervals from each larva). The mean intermovement interval observed at 22 days issimilar to that observed at 29 days, the day before hatching-eclosion.

Cockroach behavior development

217

50-

=5.46 SDr2.38

40-

Y

30.

N =I50

0

2

4

6

8

IO

12

14

16

16

20

22

24

26

28

Intermovement intervals,set

Fig. 4. Intermovement interval histograms of peristaltic eclosion movements in the abdomens of intact and decapitated pharate first instar larvae and isolated abdomens. The eclosion movements were present in all conditions but intermovement intervals were longer and more variable in the headless larvae and isolated abdomens than in intact larvae.

sion and the cuticle hardens and gradually darkens to a reddish brown color. During eclosion, larvae show no response to tactile stimulation. Even pinching the cerci with forceps had no apparent effect on ongoing eclosion movements. A radical change in behavior occurs once the cuticle is removed and the eclosion movements cease (PROVINE, 1976a). The newly emerged larva runs about using the adult locomotor gait. It also shows an escape reaction to air puffs and tactile stimulation. These mature patterns of behavior were never observed during eclosion or at earlier pre-eclosion larval stages. B. Neural origin of eclosion behavior. The participation of various parts of the CiVS in the production of the eclosion pattern was evaluated by ligating or sectioning different parts of the pharate first instar larva and observing the effect on the resulting behavior. Eclosion movements were usually initiated by tactile stimulation of 30&y larvae (PROVINE, 1976a). A loop of human hair was manipulated into position between the desired body segments of the larva. The loop was then tightened, dividing the larva into two parts. In many cases, the portion of the body on one side of the ligature was severed in order to insure that all neural connectives between the two body parts were disrupted. (1) Behavior of decapitated larvae. The effect of decapitation on edosion behavior was evaluated by ligating the neck of the first instar larva and severing the head rostra1 to the ligation. In all cases, typical

vigorous caudal-to-rostra1 peristaltic waves remained after the elimination of the head, which contains both the cerebral structures and the subesophageal ganglion (Fig. Sb). However, the mean frequency of the eclosion movements of the decapitated larvae (X = 8.05 set, S.D. = 2.92, Fig. 4) was significantly lower than the control value (% = 5.46, S.D. = 2.38, Fig. 4) which was obtained from intact larvae (t = 8.63, df = 298, P < 0.001). Therefore, head structures are not necessary for the performance of eclosion movements but they may have an influence upon their frequency. (2) Behavior of isolated abdomens. Abdomens were isolated by placing a ligation between the metathoracic and first abdominal segments. Eclosion movements were maintained in the abdomens of all experimental larvae (Fig. 5~). However, the mean intermovement interval (X = 9.13 set, SD. = 4.55) was significantly longer than that obtained from intact controls (K = 5.46 set, t = 8.95, df = 298, P < 0.001) and decapitated larvae (X = 8.05 set, t = 2.51, df = 298, P < 0.01). There was also a much greater variability in the distribution of intermovement intervals in the isolated abdomens (Fig. 4) than was observed in either control (Fig. 4) or decapitated larvae (Fig. 4). The amplitude of the eclosion waves in the abdomens was also often lower than that observed in either control or headless preparations. Despite these deviations from normality, the results indicate that eclosion movements may be organized within the abdominal ganglia in the absence of rostra1 input.

ROBERTR PROVINE

218

IV. Hatching

(a)

Cd)

Fig. 5. Effects of various abdominal ligations on eclosion movements. (a) The arrow shows the direction of propagation of the peristaltic eclosion movements in intact control larvae. When the wave reaches the thoracic segments, they are propagated as ventral flexures. (b) Decapitated larvae show caudal to rostra1 waves typical of intact control larvae. (c) Larvae with ligations between the last thoracic and first abdominal segments show independent movements on both sides of ligation. Eclosion waves are maintained in the abdomen. The question mark indicates uncertainty about the relation to -eclosion of post-ligation movements in the thorax. (d) Larvae with mid-abdominal ligations show independent (asynchronous) caudal to rostra1 eclosion-type movements on both sides of the ligation.

The behavior of the head and thorax which were isolated from the abdomen was difficult to evaluate (Fig. 5~). Although these body parts participate in eclosion movements in intact larvae by flexing ventrally, they were isolated from the abdominal waves which were the principal cues to the occurrence of an eclusion movement. (3) Behavior of larvae with mid-abdominal ligations. The capacity of various abdominal ganglia to maintain eclosion behavior was evaluated by ligating the abdomen at various mid-abdominal sites (usually between abdominal segments two and three or three and four) and observing the effect on ongoing eclosion movements both rostra1 and caudal to the ligation. The typical result is shown in Fig. 5d. The rhythmic eclosion waves remained in the abdominal segments caudal to the ligation, regardless of where the ligation was made. Typical caudal-to-rostra1 waves were also present in the body parts rostra1 to the ligation as long as 1 to 2 abdominal segments were attached to the thorax. The waves present on both sides of the ligation were always asynchronous.

Hatching is the act of escaping from the oiitheca. Cockroach hatching is a communal behavior because all 12 to 16 larvae occupying a given oiitheca emerge synchronously. Hatching and eclosion occur simultaneously and involve similar movements. Hatching was induced immediately after 29 to 30 days of incubation in 18 of the 24 oiithecase observed by breaking off the dorsal ridge of the o theta with forceps. This procedure may involve a tactile triggering mechanism reported previously (PROVINE, 1976a) or may weaken the ootheca and thus increase the effectiveness of already ongoing hatching movements. The first sign of hatching is a slight periodic opening and closing of the mouth of the oiitheca. The glistening, translucent white heads of all the larvae soon appear. The hatching movements consist of air swallowing and caudal to rostral peristaltic waves combined with thoracic ventral or dorsal flexures and occasional abdominal rotations which resemble those described for eclosion. The larvae undergo eclosion as they rhythmically surge headfirst out of the oiitheta. The shed cuticles are left in the mount of the oiitheca which closes immediately after the larvae have hatched.

DISCUSSION Motility begins early in the developmental history of the cockroach larvae, making its appearance at about halfway through incubation in ovo. Until the time of hatching, larval behavior results in essentially no body displacement in space. For this reason, it is difficult to compare larval movements with those which are observed after hatching. However, the larval ‘flattening’ movements are probably equivalent to post-hatch ventillatory behavior and the peristaltic wave movements of eclosion and hatching appear to be identical to those periodically used in eclosion throughout the remainder of larval development. Most pharate first instar larval movements have not yet been shown to have neurogenic origins, therefore we can only speculate concerning possible parallels between behavior patterns and underlying neural events. At present, we know only that the immature nervous system is bioelectrically active because ganglia of 16-day first instar larvae generate spike discharges at least as early as 1 to 2 weeks after being placed in tissue culture (PROVINE et al., 1973, 1974: PROVINE, 1976b). A neurogenic basis for the flattening and eclosion movements is probable because counterparts for both have been identified at post-hatching stages and in the case of eclosion, a neural correlate has been identified in the immature of another species (TRUMAN and SOKOLOVE, 1972). However, one must be cautious in making inferences about neural development on the basis of behavior events alone even if a given movement is known to be neurogenic. Observed behavior changes may be the product of

Cockroach behavior development hormonal modulation of neuronal motor circuitry and may only indirectly reflect neurogenetic events (TRUMAN and SOKOLOVE,1972). Few studies of behavior development have been conducted with invertebrates, so the present data are difficult to place in a comparative perspective. However, the few reports which do exist for a scattering of species (BERG, 1972; BERRILL, 1973) indicate that motility at very early developmental stages is not unique to the cockroach or to the vertebrate forms in which it is well documented (GOTTLIEB,1973; PROVINE, 1976b). More comprehensive data from a variety of invertebrate species may help to reveal properties common to all developing neuromuscular systems. For example, an interesting finding of the present study was that the amount of cockroach larval motility increased up to a point after which it declined until eclosion-hatching. This is a pattern typical of the embryos of many avian species (HAMBURGER, 1973; PROVINE, 1976b). Caudal-to-rostra1 peristaltic wave movements such as those described in this report are instrumental in eclosion (SIKES and WIGGLESWORTH, 1931; TRUMAN, 1971; WIGGLESWORTH,1972) and hatching (SIKES and WIGGLESWORTH,1931; WIGGLESWORTH1972) in some but not all species. SIKES and WIGGLESWORTH(1931) report that Cimex simultaneously hatches and ecloses, leaving the spent cuticle in the mouth of the egg in the manner of Periplaneta. The behavioral strategies which have evolved in hatching are as varied as the hatching tasks and specialized body morphologies which are present in the invertebrate world (WIGGLESWORTH, 1972; for a comparative review, see OPPENHEIM, 1973). In the present study, ligation experiments indicated that the neuronal circuitry present within isolated chains of abdominal ganglia is sufficient to maintain eclosion behavior once initiated. That the central motor program for eclosion is located in abdominal ganglia has already been demonstrated for silkmoths by TRUMAN and SOKOLOVE(1972). Since each eclosion wave is propagated in a caudal-to-rostra1 sequence, it is probable that the caudal-most abdominal ganglion in the chain triggers the activity in its more rostral neighbors. Ligation experiments at various midabdominal sites suggest further that any abdominal ganglion is capable of initiating (directly or indirectly) the eclosion activity in the next adjacent rostral ganglion. The present experiments do not permit the evaluation of the relative importance of peripheral input (GROBSTEIN, 1973) or interneuronal coordinating systems (STEIN, 1971) in the phase-coupling of movement in adjacent body segments. However, a sensory feedback loop involving the cuticle plays an important role in regulating the termination and thus the duration of the eclosion sequence in the cockroach. A previous investigation (PROVINE, 1976a) indicated that once a larva initiates eclosion, the premature removal of the cuticle by the experimenter caused an immediate cessation of the ongoing eclosion

219

rhythm. Conversely, the gluing of the cuticle to the body of the larva prolonged eclosion behavior. Thus, while eclosion behavior may involve an hormonally triggered central program (cf. TRUMAN and SOKOLOVE, 1972), the termination and thus the duration of the program readout must in this case be cuticle controlled. It was also shown that tactile stimulation will trigger eclosion movements during the last day of incubation. Therefore, it is possible that the mutual tactile stimulation of the 12 to 16 larvae occupying the oiitheca may act to simultaneously trigger and thereby synchronize the eclosion-hatching movements of all of the larvae. When the cuticle is shed on day 30, the eclosionhatching behavior abruptly ceases and the newly hatched first instar larvae walk away using the adult locomotor gait. This walking behavior is apparently performed perfectly at the first opportunity even though no ‘rehearsal’ was possible in OOO. Parallels have been found in the ‘precocial’ development of butterfly flight (PETERSON et al., 1956), in the flight and stridulation patterns of nymphal crickets (BENTLEY and HOY, 1970) and in the development of the swimmerette motor pattern in lobster larvae (DAVIS and DAVIS, 1973). These findings concur with a growing body of evidence from vertebrate research which suggests that CNS circuits for the generation of motor patterns are capable of developing in the absence of sensory input (BEKOFF et al., 1975; BERMAN and BERMAN, 1973; HAMBURGER, 1973; HAMBURGER et al., 1966; NARAYANAN and HAMBURGER, 1971; PROVINE, 1976b). Acknowledgements-I thank Drs. V. HAMBURGER, R. W. OPPENHEIM,A. C. CATANIAand P. G. SOKOLOVE for commenting on early drafts of this manuscript. DEBBIE AMDUR and JILL H-R typed the manuscript. Part of the research was conducted in the laboratory of Dr. RITA LEVIMONTALCINI, Department of Biology, Washington University, St. Louis, Missouri, and was supported by NIH Grant NS-03777 and NSF Grants GB-16330X and GB-37142. The author was also supported by research funds provided by the University of Maryland Baltimore County.

REFERENCES BEKOFF A.. STEIN P., and HAMBURGER V. (1975) Coordinated motor output in the hindlimb of the 7-day chick embryo. Proc. nat. Acad. Sci., U.S.A. 72, 1245-1248. BENTLEY D. R. and HOY R. R. (1970) Postembryonic development of adult motor patterns in crickets: a neural analysis. Science, Wash. 170, 1409-1411. BERG C. J. (1972) Ontogeny of the behavior of Strombus maculatus. Am. 2001. 12, 427443. BERMAN A. M. and BERMAN D. (1973) Fetal deafferentation: the ontogenesis of movement in the absence of sensory feedback. Exp. Neural. 38, 17@176. BERILL M. (1973) The embryonic behavior of certain crustaceans. In Behavioral Embryology (Ed. by GOTTLIEB G.) pp. 141-158. Academic Press, New York.

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