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Isolation of the abdomen releases oviposition behaviour in females of the cricket, Acheta domesticus
J. Insrcr Physiol.. Vol. 28, No. 5. pp. 401-404, Printed in Grrar Brifain.
1982
0022-1910/82/050401~04$03.00/0
Prrgmon
Pre.~ Lrd
ISOLATION OF THE ABDOMEN RELEASES OVIPOSITION BEHAVIOUR IN FEMALES OF THE CRICKET, ACHETA DOMESTICUS GRANT M. CARROW, RAFAELDE JESUSCABEZA and GLENN FLORES The Biological
Laboratories.
Harvard
(Rrcrired
University.
19 Srptemher
Cambridge.
MA 02138.
USA
198 I )
Abstract-Upon isolation, abdomens of adult female house crickets (Acltrtu domesricus) produced abdominal and ovipositor movements characteristic of normal oviposition. Oviposition behaviour was thus released even in reproductively mature or immature virgins where under normal conditions it was never observed. Decapitation was not sufficient to release oviposition behaviour but transection of the ventral nerve cord between the thorax and the abdomen of immobilized females evoked the response. These observations indicate that the motor programmes for certain components of the oviposition sequence reside in the abdominal ganglia. Moreover. the prerequisite circuitry for ovipositional posturing of the abdomen and ovipositor appears to be functional prior to sexual maturity and Insemination. primed by mating. and subject to inhibition by the thoracic ganglia. Key Word Index- Oviposition behaviour. motor programme. ventral nerve cord transection. descending inhibition. cricket, Acheru domesticus
INTRODUCTION SEVERALreproductive motor programmes encoded in the central nervous system of insects appear to be controlled by means of descending inhibition. Brain lesions release calling songs in male crickets (BENTLEY and HOY. 1970). Decapitation of males releases copulatory behaviour in mantids. cockroaches (ROEDER et al.. 1960) and mosquitoes (MCDANIEL and HORSFALL. 1957). In the mantids and cockroaches control was localized to the suboesophageal ganglion. Since inhibitory control is not limited to the brain, there is no a priori reason to expect such control to be limited to cerebral ganglia. Oviposition behaviour has been studied in isolated abdomens of moths (MCCRACKEN, 1907). wasps (GREANY and OATMAN. 1972) and locusts (VINCENT. 1975: THOMPSON, 1979); thus, the circuitry for the behaviour resides largely in the abdominal ganglia. In the studies of isolated abdomens of moths and wasps, specific stimuli were required to evoke oviposition. In the locusts. however. the appearance of oviposition posturing upon isolation of the abdomen suggested release from anterior inhibitory control. In the work cited here, the motor scores for oviposition and copulation were produced after severance of the ventral nerve cord of sexually mature adults. In no case was evidence provided that intact individuals failed to display the behaviour. Therefore, a causal relationship between nerve cord transection and behaviour cannot be unequivocally inferred. However. the experimental evocation of the callingsong neural pattern in nymphal crickets (BENTLEYand HOY, 1970) indicates that a motor programme not normally available for expression can be released by removal of anterior control centres. ln the present study, we used the house cricket. Achera domusricus. to determine whether oviposition
behaviour could be released prior to its normal period of expression by the interruption of descending inhibition. MATERIALS
AND
METHODS
Crickets were obtained from Fluker’s Cricket Farm. Baton Rouge, LA. They were maintained at 27-C in covered cardboard drums; food and water in the form of wheat germ and apple slices were provided ad lib. The drums contained neither soil nor any other substrate for oviposition; females treated in this manner were termed ‘nulliparous’ until provided with oviposition sites. In order to obtain virgin adult females, last-instar nymphs were isolated in a separate drum. Virgin female adults with undeveloped ovaries (termed ‘immature’) were utilized within 2 days after adult ecdysis. Virgin female adults with mature ovaries (termed ‘mature’) were used at least a week after adult ecdysis. Oviposition sites consisted of flat beds of moistened soil in uncovered plastic boxes. Soil was partially cleared from under the ovipositor in order to observe its downward deflection. Decapitation consisted of complete severance of the head from the thorax with scissors. Abdomens were isolated by cutting between the thorax and the first abdominal segment. In some individuals the ventral nerve cord was transected by a cut through the ventral cuticle between the thorax and the first abdominal segment. Sham operations were accomplished by cutting the cuticle and muscle between the thorax and the first abdominal segment on one side of the individual. leaving the ventral nerve cord intact. The wounds were left unsealed. Times are represented throughout as mean + S.E.M.
401
402
GRANT M. CARROW et ul.
RESULTS Control
observations
Intact nulliparous females were exposed to the oviposition substrate for up to 15 min. During that period. oviposition behaviour was observed in 88% of mated, mature females (n = 49) after an average of 2.3 f 0.3 min. Oviposition behaviour here denotes actual insertion of the ovipositor into the soil. This behaviour was accompanied by a series of motor acts, namely: downward deflection of the ovipositor, a ventrally oriented abdominal flexion, the alternate contraction and extension of the terminal abdominal segments, and deposition of eggs. Under similar circumstances, oviposition behaviour was never observed in intact, mature or immature, virgin females (n = 35). Operated frmalrs
All individuals were observed for 30 min after surgical intervention except for sham-operated females. The latter were observed for 15 min after sham operation; their ventral nerve cords were subsequently
(A)
transected and they were observed for an additional 15 min. Within a minute of isolating the abdomen, an adult female invariably deflected her ovipositor and cerci upward accompanied by scissoring of the cerci (Fig. 1B). This posturing could be elicited also by handling of intact individuals. Several minutes after the operation the majority of females displayed oviposition behaviour (Fig. 1C) consisting of the following components: alternate contraction and extension of the abdomen, downward deflection of the terminal abdomen segments and ovipositor. and digging or scooping movements of the ovipositor at the soil surface. Digging often included oscillation and upward bending of the tip of the ovipositor and. twice. egg deposition. The behavioural effects of each surgical procedure are summarized in Table 1. In each case we record the percentage of females showing oviposition behaviour as well as the mean elapsed time between the operation and the onset of the behaviour. Effects of abdominal
isolation
Isolated abdomens from adults (Groups I-III in Table 1) displayed oviposition behaviour in 70:,, of trials. Suprisingly enough, there was no difference among abdomens derived from mated and virgin females. even though intact virgins never displayed oviposition behaviour. The average delay to onset of the behaviour was similar among all groups of isolated abdomens. By contrast. isolated abdomens from last-instar females (Group IV) never exhibited the oviposition posture even though the majority (849,). like adults, deflected their abdominal tips upward. &ffects of decapitation
Decapitation of mature. mated females that were in the act of ovipositing failed to block further oviposition behaviour in 58”/,, of the individuals tested (n = 33). Resumption of digging with the ovipositor. which often included insertion of over half the ovipositor length into the soil. took place about a minute (1.3 f 0.4 min) after decapitation. By contrast. decapitation of nulliparous females was rarely followed by ovipositor movements (Groups V-VIII in Table 1). The average delay to onset of ovipositor digging movements in the few cases observed in these females was slightly greater than in the case of isolated abdomens. .?@cts of wntral
Fig. 1. Postures assumed by isolated abdomens of adult female Ackta donwsricus. drawn from photographs. A. normal posture before and just after isolation of abdomen: B. upward deflection of ovipositor and cereal scissoring a minute after isolation: C. oviposition posture.
nerw
cord transection
In otherwise intact females. oviposition behaviour was not observed after transection of the ventral nerve cord between the thorax and the abdomen. These preparations wandered persistently over the soil. dragging their abdomens behind them. It was possible to block this locomotion by decapitation just prior to nerve cord transection (Groups IX and X in Table 1). Although the jumping of these preparations often interrupted observations, more than half showed digging with the ovipositor. As indicated in Table 1. the delays to onset of the behaviour were essentially the same as in the case of isolated abdomens. Sham operation of the abdomen in decapitated females was not sufficient to elicit ovipositor movements (Groups VII and VIII). To demonstrate that
Release of Table
1. Oviposition
Group
behaviour
oviposition
in operated
403
adult and last-instar
Reproductive condition of females
Operation
behaviour female Ackeru dornesricl,.\
Oviposition behaviour
Mean delay to onset of behaviour
)I
(“A*
(min + S.E.M.)+
Mated. mature: Virgin. mature Virgin. immature Last instar
27 24 39 19
74 71 67 0
5.5 * I.3 4.6 f 1.2 4.1 f 0.7
6.0 k 2.9 18.0 f X.5
I II III IV
Isolation
V VI
Decapitation
Mated. Virgin.
mature mature
28 20
II I5
VII VIII
Decapitation and sham operation of abdomens
Mated. mature Virgin. mature
22 20
9 5
7.0 f 14.0
IX X
Decapitation and VNC transection
Mated.
mature
56 50
1.4
mature7
25 22
5.0 f
Virgin.
4.7 *
1.3
XI XII
VNC transection after decapitation and sham operation\’
20 I9
70 74
3.3 + 0.8 2.5 + 0.5
of abdomen
i
Mated. mature Virgin. mature
I.0
* Percentages were compared using Bonferroni chi square (DAYTON and SCHAFER. 1973). Groups l--Ill and IX-XII were not different from each other at the 99:,, confidence level. Groups IV VIII were not different from each other but were significantly different from all other groups. t Times were compared using analysis of variance. Only groups VI and VIII were different. due to the low number of responders. : One abdomen deposited 2 eggs after isolation. #Groups Xl and XII were the same animals as in Groups VII and VIII. See text for further explanation. The ventral nerve cord (VNC) was transected between the metathoracic and first abdominal ganglia. 1 One individual deposited I egg after nerve cord transection.
these individuals could still exhibit the proper behaviour. their ventral nerve cords were severed 15 min after initial decapitation and sham operation (Groups XI and XII). Locomotion could also be blocked without decapitation by removing the legs. Oviposition posturing was similarly elicited by nerve cord transection in 9 of these individuals (n = 10) after the usual delay (3.1 + 0.6 min). DISCUSSION We have demonstrated
that certain components of the motor score for oviposition are released in adult. nulliparous female crickets by isolating the abdomen or by transecting the ventral nerve cord between the metathoracic ganglion and the first abdominal ganglion. In this manner. oviposition behaviour was elicited even from virgins which under normal conditions never oviposited. The ovipositor digging and abdominal movements induced experimentally by these manoeuvers were nearly identical to those observed in intact females, or in females decapitated while in the act of ovipositing. On the other hand, the upward deflection of the ovipositor and cerci seen immediately after surgical intervention appears to be an artifact of cutting the ventral nerve cord, since similar posturing was elicited in most of the abdomens isolated from last-instar nymphs while oviposition posturing was not. Often, this type of posturing was observed upon handling of intact adult females. Onlv a few mature. nulliparous females displayed ovipoiitor movements after decapitation-a pro-
cedure which removes both the brain and the suboesophageal ganglion. While decapitation rarely released the oviposition programme. it generally failed to interrupt the latter once it was underway. These observations demonstrate that removal of the thorax specifically releases oviposition behaviour in female crickets. There seem to be one or more inhibitory centres in the thoracic ganglia which must be inactivated before oviposition can occur. Evidently. these centres are normally inactivated in mated adults by exposure to an appropriate oviposition site in the absence of competing stimuli. However, there may be a second level of control because exposure to soil is not sufficient to elicit oviposition behaviour in virgins. This failure to display oviposition behaviour is not due to a lack of functional development of the oviposition programme since abdominal isolation released oviposition behaviour in virgins. Rather, the readiness to oviposit may be primed by a ‘mating-factor’ from the spermatophore as proposed for Teleoyryllus (LOHER and EDSON. 1973) and suggested by earlier work on Achetu (MEIKLE. and MCFARLANE,
1965).
Acknowledyements-We express our appreciation to Prof. CARROLL M. WILLIAMS for his support of this research. for a critical reading of the manuscript, and for contributing the term ‘nulliparous’ to the entomological literature. We also thank Dr. EDMUNDARBAS and Profs.
RONALDCALABRESEand RONALDHOY for suggestions and criticisms. Mr. KENNETHCARLSONfor assistance with the statistical analysis. and Ms. CYNTHIA‘PHILLIPS for the drawings. The research was supported by funds from the Department of Biology and by a grant from the National Institutes of Health to Prof. WILLIAMS.
GRANT M. CARROWet al.
404 REFERENCES
BENTLEY D. R. and HOY R. R. (1970) Postembryonic development of adult motor patterns in crickets: A neural analysis. Science Wash. 170, 1409-1411. DAYTONC. M. and SCHAFERW. D. (1973) Extended tables of t and chi square for Bonferroni tests with unequal error allocation. J. Am. smrisr. Ass. 68, 78-83. GREANYP. D. and OATMANE. R. (1972) Oviposition by an isolated parasite abdomen. Ann. Em. Sot. Amer. 65, 991-992.
LOHERW. and EDSONK. (1973) The effect of mating on egg production and release in the cricket Teleoyryllus commodus. Enr. exp. and Appl.
16,483490.
MCCRACKENI. (1907) The egg-laying apparatus
in the
silkworm (Bombyx mori) as a reflex apparatus. J. corn;. Neural. Psycho/. 17, 262-285. MCDANIEL 1. N. and HORSFALLW. R. (1957) Induced copulation of aedine mosquitoes. Science Wash. 125,745. MEIKLEJ. E. S. and MCFARLANEJ. E. (1965) The role of lipid in the nutrition of the house cricket, Achero domesricus L. (0rthoptera:Gryllidae). Can J. Zoo/. 43, 87-98. ROEDERK. D., TOZIANL. and WEIANTE. A. (1960) Endogenous nerve activity and behaviour in the mantis and cockroach. J. fnsecr Physiol. 4, 45-62. THOMPSONK. J. (1979) Locust oviposition: A system for the study of motor pattern generation. Sot. Neurosci. Absrr. 5, 264.
VINCENTJ. F. V. 1975. How does the female locust dig her oviposition hole’! J. Enr. (A) 50, 175-181.
1982
0022-1910/82/050401~04$03.00/0
Prrgmon
Pre.~ Lrd
ISOLATION OF THE ABDOMEN RELEASES OVIPOSITION BEHAVIOUR IN FEMALES OF THE CRICKET, ACHETA DOMESTICUS GRANT M. CARROW, RAFAELDE JESUSCABEZA and GLENN FLORES The Biological
Laboratories.
Harvard
(Rrcrired
University.
19 Srptemher
Cambridge.
MA 02138.
USA
198 I )
Abstract-Upon isolation, abdomens of adult female house crickets (Acltrtu domesricus) produced abdominal and ovipositor movements characteristic of normal oviposition. Oviposition behaviour was thus released even in reproductively mature or immature virgins where under normal conditions it was never observed. Decapitation was not sufficient to release oviposition behaviour but transection of the ventral nerve cord between the thorax and the abdomen of immobilized females evoked the response. These observations indicate that the motor programmes for certain components of the oviposition sequence reside in the abdominal ganglia. Moreover. the prerequisite circuitry for ovipositional posturing of the abdomen and ovipositor appears to be functional prior to sexual maturity and Insemination. primed by mating. and subject to inhibition by the thoracic ganglia. Key Word Index- Oviposition behaviour. motor programme. ventral nerve cord transection. descending inhibition. cricket, Acheru domesticus
INTRODUCTION SEVERALreproductive motor programmes encoded in the central nervous system of insects appear to be controlled by means of descending inhibition. Brain lesions release calling songs in male crickets (BENTLEY and HOY. 1970). Decapitation of males releases copulatory behaviour in mantids. cockroaches (ROEDER et al.. 1960) and mosquitoes (MCDANIEL and HORSFALL. 1957). In the mantids and cockroaches control was localized to the suboesophageal ganglion. Since inhibitory control is not limited to the brain, there is no a priori reason to expect such control to be limited to cerebral ganglia. Oviposition behaviour has been studied in isolated abdomens of moths (MCCRACKEN, 1907). wasps (GREANY and OATMAN. 1972) and locusts (VINCENT. 1975: THOMPSON, 1979); thus, the circuitry for the behaviour resides largely in the abdominal ganglia. In the studies of isolated abdomens of moths and wasps, specific stimuli were required to evoke oviposition. In the locusts. however. the appearance of oviposition posturing upon isolation of the abdomen suggested release from anterior inhibitory control. In the work cited here, the motor scores for oviposition and copulation were produced after severance of the ventral nerve cord of sexually mature adults. In no case was evidence provided that intact individuals failed to display the behaviour. Therefore, a causal relationship between nerve cord transection and behaviour cannot be unequivocally inferred. However. the experimental evocation of the callingsong neural pattern in nymphal crickets (BENTLEYand HOY, 1970) indicates that a motor programme not normally available for expression can be released by removal of anterior control centres. ln the present study, we used the house cricket. Achera domusricus. to determine whether oviposition
behaviour could be released prior to its normal period of expression by the interruption of descending inhibition. MATERIALS
AND
METHODS
Crickets were obtained from Fluker’s Cricket Farm. Baton Rouge, LA. They were maintained at 27-C in covered cardboard drums; food and water in the form of wheat germ and apple slices were provided ad lib. The drums contained neither soil nor any other substrate for oviposition; females treated in this manner were termed ‘nulliparous’ until provided with oviposition sites. In order to obtain virgin adult females, last-instar nymphs were isolated in a separate drum. Virgin female adults with undeveloped ovaries (termed ‘immature’) were utilized within 2 days after adult ecdysis. Virgin female adults with mature ovaries (termed ‘mature’) were used at least a week after adult ecdysis. Oviposition sites consisted of flat beds of moistened soil in uncovered plastic boxes. Soil was partially cleared from under the ovipositor in order to observe its downward deflection. Decapitation consisted of complete severance of the head from the thorax with scissors. Abdomens were isolated by cutting between the thorax and the first abdominal segment. In some individuals the ventral nerve cord was transected by a cut through the ventral cuticle between the thorax and the first abdominal segment. Sham operations were accomplished by cutting the cuticle and muscle between the thorax and the first abdominal segment on one side of the individual. leaving the ventral nerve cord intact. The wounds were left unsealed. Times are represented throughout as mean + S.E.M.
401
402
GRANT M. CARROW et ul.
RESULTS Control
observations
Intact nulliparous females were exposed to the oviposition substrate for up to 15 min. During that period. oviposition behaviour was observed in 88% of mated, mature females (n = 49) after an average of 2.3 f 0.3 min. Oviposition behaviour here denotes actual insertion of the ovipositor into the soil. This behaviour was accompanied by a series of motor acts, namely: downward deflection of the ovipositor, a ventrally oriented abdominal flexion, the alternate contraction and extension of the terminal abdominal segments, and deposition of eggs. Under similar circumstances, oviposition behaviour was never observed in intact, mature or immature, virgin females (n = 35). Operated frmalrs
All individuals were observed for 30 min after surgical intervention except for sham-operated females. The latter were observed for 15 min after sham operation; their ventral nerve cords were subsequently
(A)
transected and they were observed for an additional 15 min. Within a minute of isolating the abdomen, an adult female invariably deflected her ovipositor and cerci upward accompanied by scissoring of the cerci (Fig. 1B). This posturing could be elicited also by handling of intact individuals. Several minutes after the operation the majority of females displayed oviposition behaviour (Fig. 1C) consisting of the following components: alternate contraction and extension of the abdomen, downward deflection of the terminal abdomen segments and ovipositor. and digging or scooping movements of the ovipositor at the soil surface. Digging often included oscillation and upward bending of the tip of the ovipositor and. twice. egg deposition. The behavioural effects of each surgical procedure are summarized in Table 1. In each case we record the percentage of females showing oviposition behaviour as well as the mean elapsed time between the operation and the onset of the behaviour. Effects of abdominal
isolation
Isolated abdomens from adults (Groups I-III in Table 1) displayed oviposition behaviour in 70:,, of trials. Suprisingly enough, there was no difference among abdomens derived from mated and virgin females. even though intact virgins never displayed oviposition behaviour. The average delay to onset of the behaviour was similar among all groups of isolated abdomens. By contrast. isolated abdomens from last-instar females (Group IV) never exhibited the oviposition posture even though the majority (849,). like adults, deflected their abdominal tips upward. &ffects of decapitation
Decapitation of mature. mated females that were in the act of ovipositing failed to block further oviposition behaviour in 58”/,, of the individuals tested (n = 33). Resumption of digging with the ovipositor. which often included insertion of over half the ovipositor length into the soil. took place about a minute (1.3 f 0.4 min) after decapitation. By contrast. decapitation of nulliparous females was rarely followed by ovipositor movements (Groups V-VIII in Table 1). The average delay to onset of ovipositor digging movements in the few cases observed in these females was slightly greater than in the case of isolated abdomens. .?@cts of wntral
Fig. 1. Postures assumed by isolated abdomens of adult female Ackta donwsricus. drawn from photographs. A. normal posture before and just after isolation of abdomen: B. upward deflection of ovipositor and cereal scissoring a minute after isolation: C. oviposition posture.
nerw
cord transection
In otherwise intact females. oviposition behaviour was not observed after transection of the ventral nerve cord between the thorax and the abdomen. These preparations wandered persistently over the soil. dragging their abdomens behind them. It was possible to block this locomotion by decapitation just prior to nerve cord transection (Groups IX and X in Table 1). Although the jumping of these preparations often interrupted observations, more than half showed digging with the ovipositor. As indicated in Table 1. the delays to onset of the behaviour were essentially the same as in the case of isolated abdomens. Sham operation of the abdomen in decapitated females was not sufficient to elicit ovipositor movements (Groups VII and VIII). To demonstrate that
Release of Table
1. Oviposition
Group
behaviour
oviposition
in operated
403
adult and last-instar
Reproductive condition of females
Operation
behaviour female Ackeru dornesricl,.\
Oviposition behaviour
Mean delay to onset of behaviour
)I
(“A*
(min + S.E.M.)+
Mated. mature: Virgin. mature Virgin. immature Last instar
27 24 39 19
74 71 67 0
5.5 * I.3 4.6 f 1.2 4.1 f 0.7
6.0 k 2.9 18.0 f X.5
I II III IV
Isolation
V VI
Decapitation
Mated. Virgin.
mature mature
28 20
II I5
VII VIII
Decapitation and sham operation of abdomens
Mated. mature Virgin. mature
22 20
9 5
7.0 f 14.0
IX X
Decapitation and VNC transection
Mated.
mature
56 50
1.4
mature7
25 22
5.0 f
Virgin.
4.7 *
1.3
XI XII
VNC transection after decapitation and sham operation\’
20 I9
70 74
3.3 + 0.8 2.5 + 0.5
of abdomen
i
Mated. mature Virgin. mature
I.0
* Percentages were compared using Bonferroni chi square (DAYTON and SCHAFER. 1973). Groups l--Ill and IX-XII were not different from each other at the 99:,, confidence level. Groups IV VIII were not different from each other but were significantly different from all other groups. t Times were compared using analysis of variance. Only groups VI and VIII were different. due to the low number of responders. : One abdomen deposited 2 eggs after isolation. #Groups Xl and XII were the same animals as in Groups VII and VIII. See text for further explanation. The ventral nerve cord (VNC) was transected between the metathoracic and first abdominal ganglia. 1 One individual deposited I egg after nerve cord transection.
these individuals could still exhibit the proper behaviour. their ventral nerve cords were severed 15 min after initial decapitation and sham operation (Groups XI and XII). Locomotion could also be blocked without decapitation by removing the legs. Oviposition posturing was similarly elicited by nerve cord transection in 9 of these individuals (n = 10) after the usual delay (3.1 + 0.6 min). DISCUSSION We have demonstrated
that certain components of the motor score for oviposition are released in adult. nulliparous female crickets by isolating the abdomen or by transecting the ventral nerve cord between the metathoracic ganglion and the first abdominal ganglion. In this manner. oviposition behaviour was elicited even from virgins which under normal conditions never oviposited. The ovipositor digging and abdominal movements induced experimentally by these manoeuvers were nearly identical to those observed in intact females, or in females decapitated while in the act of ovipositing. On the other hand, the upward deflection of the ovipositor and cerci seen immediately after surgical intervention appears to be an artifact of cutting the ventral nerve cord, since similar posturing was elicited in most of the abdomens isolated from last-instar nymphs while oviposition posturing was not. Often, this type of posturing was observed upon handling of intact adult females. Onlv a few mature. nulliparous females displayed ovipoiitor movements after decapitation-a pro-
cedure which removes both the brain and the suboesophageal ganglion. While decapitation rarely released the oviposition programme. it generally failed to interrupt the latter once it was underway. These observations demonstrate that removal of the thorax specifically releases oviposition behaviour in female crickets. There seem to be one or more inhibitory centres in the thoracic ganglia which must be inactivated before oviposition can occur. Evidently. these centres are normally inactivated in mated adults by exposure to an appropriate oviposition site in the absence of competing stimuli. However, there may be a second level of control because exposure to soil is not sufficient to elicit oviposition behaviour in virgins. This failure to display oviposition behaviour is not due to a lack of functional development of the oviposition programme since abdominal isolation released oviposition behaviour in virgins. Rather, the readiness to oviposit may be primed by a ‘mating-factor’ from the spermatophore as proposed for Teleoyryllus (LOHER and EDSON. 1973) and suggested by earlier work on Achetu (MEIKLE. and MCFARLANE,
1965).
Acknowledyements-We express our appreciation to Prof. CARROLL M. WILLIAMS for his support of this research. for a critical reading of the manuscript, and for contributing the term ‘nulliparous’ to the entomological literature. We also thank Dr. EDMUNDARBAS and Profs.
RONALDCALABRESEand RONALDHOY for suggestions and criticisms. Mr. KENNETHCARLSONfor assistance with the statistical analysis. and Ms. CYNTHIA‘PHILLIPS for the drawings. The research was supported by funds from the Department of Biology and by a grant from the National Institutes of Health to Prof. WILLIAMS.
GRANT M. CARROWet al.
404 REFERENCES
BENTLEY D. R. and HOY R. R. (1970) Postembryonic development of adult motor patterns in crickets: A neural analysis. Science Wash. 170, 1409-1411. DAYTONC. M. and SCHAFERW. D. (1973) Extended tables of t and chi square for Bonferroni tests with unequal error allocation. J. Am. smrisr. Ass. 68, 78-83. GREANYP. D. and OATMANE. R. (1972) Oviposition by an isolated parasite abdomen. Ann. Em. Sot. Amer. 65, 991-992.
LOHERW. and EDSONK. (1973) The effect of mating on egg production and release in the cricket Teleoyryllus commodus. Enr. exp. and Appl.
16,483490.
MCCRACKENI. (1907) The egg-laying apparatus
in the
silkworm (Bombyx mori) as a reflex apparatus. J. corn;. Neural. Psycho/. 17, 262-285. MCDANIEL 1. N. and HORSFALLW. R. (1957) Induced copulation of aedine mosquitoes. Science Wash. 125,745. MEIKLEJ. E. S. and MCFARLANEJ. E. (1965) The role of lipid in the nutrition of the house cricket, Achero domesricus L. (0rthoptera:Gryllidae). Can J. Zoo/. 43, 87-98. ROEDERK. D., TOZIANL. and WEIANTE. A. (1960) Endogenous nerve activity and behaviour in the mantis and cockroach. J. fnsecr Physiol. 4, 45-62. THOMPSONK. J. (1979) Locust oviposition: A system for the study of motor pattern generation. Sot. Neurosci. Absrr. 5, 264.
VINCENTJ. F. V. 1975. How does the female locust dig her oviposition hole’! J. Enr. (A) 50, 175-181.