Louis M. Roth and Barbara Stay.
A Comparative Study of Oöcyte Development in False Ovoviviparous Cockroaches.
Psyche 69:165-208, 1962.

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PSYCHE
Vol. 69 DECEMBER, 1962 No. 4
A COMPARATIVE STUDY OF
OOCYTE DEVELOPMENT IN FALSE
OVOVIVIPAROUS COCKROACHES*
BY LOUIS M. ROTH AND BARBARA STAY^
Pioneering Research Laboratories
Quartermaster Research and Engineering Center Natick, Massachusetts
Recently Engeln~ann (1960) compared various internal and exter- nal factors which affect the activity of the corpora allata in Leuco- $ham maderae (Fabricius) and Diplotera punctata (Eschscholtz) . In these two species the stimuli resulting from mating, food intake, gesta- tion, and parturition differed in the degree to which they influenced production of gonadotropic hormone.
In this paper we report our experiments on control of oocyte devel- opment in several species of cockroaches that incubate their eggs internally in a brood sac or uterus. We classify these species as false ovoviviparous forms because the uterine eggs increase in water content only (Roth and Willis, I 955 ) as opposed to false viviparous species, like Diplofitera, in which the embryos take up both water and solids from the mother (Roth and Willis, 1955a). In both groups the oviposition behavior is similar. The eggs do not pass directly from the ovaries into the uterus but are first extruded to the outside of the body and then retracted into the brood sac (Roth and Willis, 1954, 1958). Cockroaches that incubate their eggs internally have two birth products, the egg and nymph (Roth and Willis, 1958). Ovulation and oviposition refer to the eggs being released from the ovaries, oriented by the ovipositor, and covered by the ootheca. After the eggs are in the uterus the females are pregnant (gestation) for a certain period of time and give birth (parturition) to nymphs, MATERIALS AND METHODS
Except for one series of experiments on Nauphoeta (see page I 74)) all insects were reared on dog chow checkers and maintained at 24' *Manuscript received by the editor August 1,1962. 'Present address: Department of Zoology, University of Pennsylvania, Philadelphia, Pennsylvania.
165




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I 66 Psyche [December
to 2s0 C. and 50 to 70% relative humidity. Engelmann (1957, 1959) showed that yolk deposition and growth of the oocytes are correlated with and dependent upon activity of the corpora allata in Leucophaea and Diploptera and we have used oocyte development as an indicator of endocrine activity. Measurements were made, with an ocular mic- rometer, of oocytes that were dissected from ovaries in Ringer's solu- tion. Our measurements of the oocytes of Leucophaea are larger than those reported by Engelmann ( 1960). This discrepancy is probably due to the fact that he measured the oocytes after fixation (Engel- mann, 195 7). We measured one large oocyte per female; in establish- ing the normal ovarian cycle or the sizes of the oocytes at a specific period a number of females were usually dissected to give some indica- tion of the extent of variation. Various operations (allatectomy, nerve cord severance, etc.) were performed on insects kept under carbon dioxide anesthesia.
The species reported on in this paper are Pycnoscelus surinamensis (Linnaeus) , Byrsotria fumigata (Gukrin) , Blaberus craniifer Bur- meister, Blaberus giganteus (Linnaeus) , Nauphoeta cinerea (Olivier ), and Leucophaea maderae. There are two strains of Pycnoscelus suri- namensis which differ physiologically. The bisexual strain cannot reproduce parthenogenetically and the parthenogenetic strain females when mated to males of the bisexual form show a reduction in fertility and the resulting offspring are all females which reproduce partheno- genetically (Roth and Willis, 1961).
Practically all of the experi-
ments on Pycnoscelus were done on the parthenogenetic strain but a few were performed o,n the bisexual form. A similar study on control of oocyte development in Diploptera and two species of BlatteZla has been reported elsewhere (Roth and Stay, 1961, 1962). RESULTS AND DISCUSSION
Oocyte development in virgin and mated females Py cnoscelus surinamensis: Biological data for the two strains are given in table I. The basal oocytes of the ovarioles of females less than a day old are large and may already contain yolk. In fact yolk may be present in the oocytes of some newly-emerged adults indicating that gonadotropic hormone had already been released in the nymphal stage.
The ovarian cycle from emergence to the formation of the second ootheca in the parthenogenetic strain is shown in figure I. During gestation the oocytes remain small and increase only slight- ly in length during the development of the eggs in the uterus. Yolk deposition occurs after parturition and the oGcytes increase rapidly in size.




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Table I - Biological Data For Two Strains of Pycnosccl~[s surinamensis BIOLOGICAL OBSERVATION
Length (mm.) of oocytes
less than 1 day after
emergence of adult
Length (mm.) of mature
oocytes at oviposition3
Length (mm.) of new
basal oocyte at
time of oviposition
'S.E.=standard error, here and in all following tables. %=number of insects, here and in all following tables. "Data from Roth and Willis (1961).
PARTHENOGENETIC STRAIN
Min.
Max. Mean å S.E.l N'
0.86
0.99 0.91 & 0.03 5
day after parturition
Age (days) at first
ovulation
Virgins
Mated
Gestation (days)3
Virgins
Mated
Number days to
ovulation following
parturition3
u
BISEXUAL STRAIN
Min. Max. Mean 31 S.E. N
0.73 0.94
0.85 k 0.02 10
2.97
3.36 3.21 k 0.04 10
0.50
0.57 0.53 k0.01 6
2.69 3.36 2.99 iz 0.04
l5 b o
Ìö-+
0.50 0.74 0.60 5 0.02 16
a
ft^
Length (mm.) of basal 0.79 0.74k 0.01 10 oocvtes less than 1
10 20 12.8 2 0.1 244
- -
- -
-
5 3 5 8 55.450.3 20
- - - - -
14 17 15.5 k 0.3 11
0.69 0.79 0.745 0.01
F
5 - I
1
0
^t-
8 25 13.6å 0.2 138 2
9 22 11.920.1
-
59 g
a-
"a t->
- - - - -
50 5 6 52.8 * 0.2 37
10 16 14.2 k 0.7 8




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I 68 Psy c lz e [December
In the parthenogenetic strain the first ovulation occurs when the female is about 13 days old whereas the second ovulation takes place about 16 days after birth of young. This 3 day difference is explained by the difference in size of the oocytes in the newly-emerged female and in the female at parturition; the oocytes are smaller after the female gives birth and it takes about 3 days to attain the same degree of development as they are at adult emergence. In Diploptera the reverse is true and the second preovulation period is 3 days shorter than the first although, as in Pycnoscelus the growth rate of the oocytes is about the same during the first and second preovulation periods. In Diplofitera the oocytes at parturition are about the size of those of a 3-day-old mated female which explains the shorter period required for ovulation after parturition (Engelmann, 1959). Pycnoscelus surinomensis
3 fi!- OVIPOSITION
OVIPOSITION
GESTATION ->
Fig. 1. Ovarian cycle of Pycnoscelus surinamensis (parthenogenetic strain). Each point on the curve for oocyte development from 0 to 13 days is the mean of 6 to 13 measurements (NÌÔ134) Each point for the gestation period from 13 to 68 days represents individual measurements (NÌÔ99 when 2 or more points were similar for a particular age only one is indicated). The part of the curve representing the growth of the oocytes after parturition (birth) is based on 1 to 3 individuals (NÌÔ24 for each point. Vertical bars -
-standard errors of mean values.
In the parthenogenetic strain of Pycnoscelus it is obvious that mat- ing is unnecessary for development of the oocytes. The initial develop- ment of the oocytes in the bisexual strain is similar to that found in the parthenogenetic form but differs in that mating slightly stimulates the growth rate and also is necessary for normal retraction of the ootheca into the uterus. Mating a parthenogenetic strain female with a male



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19621 Roth and Stay - Cockroaches 169
of the bisexual strain has no stimulating effect on growth of the oocytes as indicated by age of the female at ovulation (Roth and Willis, I 961 ) .
Six parthenogenetic strain females, allatecto~nized when I - 2 days old, did not oviposit within a month after the operations. Five of these females had 2 pairs of corpora allata implanted at 29 to 30 days aftei- allatectomy. Four produced oothecae in less than 35 days and one died after 44 days. At I I I days after allatectomy one female that still had not ovulated received corpora allata implants and oviposited in less than 21 days. This strain normally oviposits about 13 days after emergence (table I). The delay in oviposition after implanting cor- pora allata may have been due to the presence of degenerating oocytes in the ovaries since the oocytes already have yolk one to two days after emergence (the age at which allatectomy was performed). In Leuco- phaea, oocytes in resorption inhibit the corpora allata (Engelmann, 1957).
Table 2 - Effect of mating on oocyte development and oviposition in Byrsotria fumigata
OBSERVATION
Total number observed
Number oviposited
Ootheca retracted normally
Ootheca incompletely retracted
Ootheca dropped
Number failed to oviposit
Oocytes large, well developed
or matured but degenerating
and being resorbed
Oocytes small, abnormal in
shape, being resorbed
Oocytes small, normal in
appearance but only
slightly or not at all developed
MATED
VIRGIN
'Three of the 4 females had sperm in their spermathecae; one lacked sperm.
*These females were 35 to 60 days old when dissected. had sperm in their spermathecae.
twenty-one of these females were 32 to 60 days old. The other 14 were 11 to 24 days of age but since their oocytes were small and abnormal they would not have oviposited.



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Psyche
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AGE OF FEMALE (DAYS)
&sotria fumigate!
o = Oocytes,virgin females
= Oocytes, mated females
'
8 = Degenerating oocytes, virgin females Fig. 2. Growth of oocytes in virgin and mated females of Byrsotria ft gata. Each point represents one female.
Females were mated when 1 tc
days old.




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19621 Roth and Stay - Cockroaches I7 *
Byrsotria fumigata: The effects of mating on oocyte development and oviposition in Byrsotria are shown in table 2 and figure 2. About 50 percent of the virgin females failed to oviposit but of these I 11 females 61 % had large well-developed oocytes that were degenerating or were being resorbed (fig. 14E). It is evident from figure 2 that after the thirty-fifth day of age the oocytes of many virgins degenerate although most of them may reach a length of 5 mm. or more. About 16% of the virgins and about 10% of the mated females had small abnormally-shaped oocytes that were being resorbed. It is unlikely that lack of hormone is responsible for this type of abnormality since Barth (personal communication) has dissected pheromone-producing Byrsotria females which had small degenerating oocytes but accessory glands filled with secretion.
In those females that mate, copulation has little, if any, effect on the growth rate of the oocytes (fig. 2). Mated females oviposited at 26 to 41 days of age (Z=32.4å±0. days; N=53) ; virgin females oviposited 26 to 44 days after emergence (?=34.3å±0. days; N= 121). That there is little effect on the rate of growth resulting from mating is further borne out by the fact that the females oviposit at about the same age regardless of their age when mated. In our series the females were with males continuously until they mated; copula- tion occurred from 4 to 25 days after female emergence. The oocytes may vary considerably in size in females between these age limits (fig. 2). A female with large oocytes mated when 25 days old may ovulate 10 days later whereas one with small oocytes mated at 4 days of age may take 30 days to ovulate (fig. 3). This is quite different from the effect of mating in Leucophaea (Engelmann, 1960) where the average interval between mating and oviposition is about the same regardless of the age of the female when mated (fig. 3) because the females tend to mate more readily when their oocytes reach a certain size (see below) . Barth ( 1961 ) found that Byrsotria females begin to produce sex pheromone 10 to 30 days after the imaginal molt; however, recently (1962) he has found that some females may mate as early as 4 days after adult emergence. It seems that in Byrsotria mating (perhaps the presence of sperm in the spermathecae) serves
as a stimulus to oviposition.
This is
indicated by the fact that the oocytes in many virgin females apparent- ly mature yet ovulation does not occur. The oocytes in virgin females at ovulation vary in length from 5.90 to 7.60 mm. (2=6.79å±0.0 ; N=7). Although the mean ages at ovulation of mated and virgin females are very similar a breakdown of the data (fig. 4) shows that



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Psyche [December
Fig. 3.. Relationship between age at mating and ovulation (as indicated by oviposition) in 4 species of cockroaches. Each point represents one female. (N = 3 56 for Leucophaea) .
38% of the virgins oviposited after the thirty-fifth day as compared to I 3% of mated females.
Fifteen virgin females allatectomized when I to 2 days old did not produce oothecae within more than 50 days. At 52 to 210 days after allatectomy, corpora allata were implanted; 9 females ovulated in less than 82 days and one oviposited in 128 days; 3 died without oviposit- ng and two dissected after 150 days had small undeveloped oocytes. One allatectomized female that oviposited after receiving corpora allata implants had well developed oocytes although the ootheca was in the uterus (fig. 14D). Of 25 sham operated females 16 oviposited in less than 56 days. We don't know how to account for the delay in ovulation after implantation of corpora allata into allatectomized females. Four pregnant females (i.e. with an ootheca in the brood sac) had corpora allata implanted and were dissected at 35 to 41 days of pregnancy. Their oocytes measured 4.90 to 6.81 mm. in length



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19621 Roth and Stay -- Cockroaches I73
indicating renewed growth of the ovarian eggs as a result of the implants.
Nauphoeta cinerea: The oocytes of virgins develop but unless mating occurs the oocytes in many females may degenerate before they reach ovulation size (fig. 5). Virgin females that ovulate do so in 31 to 47 days (x=35.8zk1.2 days; N=17). Mating results in stimu- Blaberus craniifer
AGE OF FEMALE (DAYS)
Fig. 4. Effect of mating on oviposition. Solid circlesÌÔvirgi females. Open circlesÌÔmate females. The curves for Byrsotria are based on 53 mated and 121 virgin females. The curves for Blaberus are based on 18 mated and 36 virgin females.




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Psyche
[December
lation of the corpora allata so that the oocytes develop rapidly (fig. 5) and oviposition occurs in 18 to 21 days (2=18.9dz0.40; - N=8). Copulation is completed in 17 to 30 minutes (x=20.4å±0.8 min. ; N=17). Of 22 females kept with males continuously, 19 mated 5 days after emergence; the other 3 mated after 6, 8, and 10 days respec- tively.
4.4
-
4.0 -
3.6 -
3.2
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2.8-
I
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& 16)
0
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-
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o = Oocytes, virgin females
= Oocytes, mated females
i = Degenerating oocytes, virgin females Fig. 5.
Growth of oocytes in mated and virgin females of Nauphoeta cinerea. Each point represents one female. Except for 2 individuals mated at 8 and 10 days of age, all others were mated when 5 days old. In a series of experiments performed at Harvard University, tem- perature was uncontrolled but usually higher than 24O to 25' C.; the insects were maintained on Purina Laboratory Chow. Both virgin and mated females oviposited earlier than in the above experiment but virgin females still oviposited later (24 to 35 days) than mated indi-



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Roth and Stay - Cockroaches
AGE OF FEMALE (DAYS)
Fig. 6. Effect of mating, starvation, and combined starvation and mating on oocyte development in Nauphoeta cinerea. The points are mean values; fed virgins, N1707; starved virgins, NX133 ; fed mated, NY58 ; starved mated, N=21. Females were mated when 4 to 6 days old, Vertical bars are one standard error (only positive halves of standard errors are indicated wherever errors overlapped) ; no vertical bars indicate standard errors of 2 0.02 mm. or less,




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176 Psyche [December