L. M. Roth and E. R. Willis.
Intra-Uterine Nutrition of the "Beetle-Roach" Diploptera dyliscoides (Serv.) during Embryogenesis, with Notes on its Biology in the Laboratory (Blattaria: diplopteridae).
Psyche 62(2):55-68, 1955.

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INTRA-UTERINE NUTRITION OF
THE "BEETLE-ROACH" DIPLOPTERA DYTZSCOIDES (SERV.)l DURING EMBRYOGENEISIS, WITH NOTES ON I'TS BIOhOGY IN THE LABORATORY
(BLATTARIA : DIPLOPTERIDAE)
BY LOUIS M. ROTH and EDWIN R. WILLIS
Pioneering Researfch Division
U. S. Army Quartermaster Research
and Development Center
Natiak, Massachusetts
Diploptera dytiscoides is a common viviparous cockroach that injures the bark of several kinds of trees in Hawaii and other Pacific Islands (Fullaway and Krauss, 1945). Its embryology has been extensively studied by Hagan (1951) who indicated that the embryo increases over five times in size during development. This growth was not accompanied by a decrease in yolk, and Hagan suggested that the developing embryo acquired nutriment from an- other source. The embryos have greatly elongated pleuro- podia to which Hagan (1939, 1951) tentatively ascribed nutritional or respiratory functionsy or both. Because of the embryo's increase in size and its modified pleuropodia, Hagan (1951) cited D. dytiscoides as the one example of pseudoplacental viviparity among cockroaches. Although Hagan's suggestion is a logical hypothesis? the acquisition of nutriment by the embryo has never been examined experimentally.
The eggs of the false ovoviviparous cockroach, Nau- phoeta cinerea (Oliv.), also increase in size during em- bryogenesis; this increase is closely correlated with absorp- tion of water? whereas solids are slowly lost until hatching (Roth and Willis? 1955). In order to determine whether 'We are greatly indebted to the United States Department of Agri- culture for permission to import this species, and to Mr. Fred A. Bianchi of the Hawaiian Sugar Planters Association, who kindly sent us several hundred living specimens of Diploptera. The insects were cultured on Purina dog chow checkers.




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56 Psyche [June
absorption of water alone could account for the increase in the size of Diploptera eggs, we have studied the changes? with age? in wet weight and in dry matter and water con- tent of the developing eggs.
Female Diploptera were removed from the cultures? anesthetized with GO2? and their oothecae were expelled by finger Ipreslsure against the base of the abdomen. Because ootheca fornation was rarely observed, the exact age of the eggs was unknown. Therefore? the length of an end egg in each ootheca was measured with an ocular micro- meter and its size was used in lieu of age. All weights were determined on torsion balances sensitive to 0.01 and 0.05 mg. Oothecae were air-oven dried at about 100å¡C to con- etant weight. All determinations were made on eggs en- closed in oothecae (rahher than on individual eggs), but cal- culations are presented on a per egg basis. The ootheca itself (fig. 5, arrow) is so reduced in this species that its inclusion in the calculations is a negligible factor, particu- larly with older eggs which have greatly increased in size. lSometimes an ootheca contained one or two eggs which failed to develop; these were easily removed without dam- age to the remaining eggs and were not included in the weight determinations. The usual number of eggs in an 06theca is 12 (Hagan, 1941) ; of 51 oothecae examined by us, the number of eggs ranged from 9 to 13 (including undeveloped eggs) ? with a mean of 11.4 per ootheca. Hagan (1954) thinks that this average may be due to altered environment, food, and captivity. In Hawaii he seldom found lesls than 12 eggs per ootheca and usually more than that number, although he did not record the data. EXPLANATION OF PLATE 4
Figures 2-4. Diploptera dytiscoides. Fig. 2. Female with an everted uterus (as a result of once having had her abdomen squeezed to remove an ootheca) and a recently formed ootheca (arrow) which she extruded
because it could not be retracted into the brood sac (X3.8). Fig. 3. Female, after accidentally being exposed to high temperatures, prema- turely aborting an ootheca containing well-developed embryos ( X 3.8). Fig. 4. End view of abdomen of female; genital segments separated to show 4 embryos visible in the brood sac. Note eye (arrow) of embryo ( x 7.5).




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Psyche
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EVIDENCE FOR INTRA-UTERINE NUTRITION
The weight, water, and dry matter changes which ac- companied the increase in egg size are shown in figure I; a series of oothecae containing eggs of different sizes are ~hown in figures 5-9. The smallest eggs (0.93 mm.) un- doubtedly were from a very recently formed ootheca. Hagan (1951) stated that the freshly deposited egg is approxi- mately 1.20 mm. long. The largest eggs (6.9 mm.) repre- sent fully matured embryos, inasmwch as some of the eggs in this ootheca began to hatch shortly after they were manually extruded from the female
(figs. 9-13). The dif-
ference in size between the smallest and largest eggs represents more than a seven-fold increase during em- bryogenesis. The size and weight of the eggs increase with acquisition of both water and solids. However, most of the weight increase arises from absorption of water. From the smallest to the largest eggs there was an increase of about 50 times in the almount of dry matter and about 85 times in water content. Visible differentiation was ac- companied by the first observed increase in dry matter (fig. I, arrow). Prior to differentiation the eggs absorbed water only, and the dry matter [content dropped from about 34% to about 26%. After differentiation became visible, the dry matter content remained at approximately 26% throughout development.
'The increase in the size of
the egg? as Hagan (1951) pointed out, cannot arise from the small amount of yolk available? nor icould the increase in dry weight be interpreted on this basits. Obviously, ad- ditional nutriment is supplied by the mother to the eggs in the brood sac. The exact source of this nutriment is not known; Hagan (1941) suggested that nutriment may be secreted by the maternal accessory (colleterial) glands. Diploptera is unique among cockroaches in gaining solid matter from the mother during embryonic development. In oviparous cockroaches (Blatta orientalis L., Blattella vaga Hab., Blattella germnica (L.) ) and false ovovivi- parous species (Nauphoeta cinerea, Pycnoscelus surina- rnensis (L.), and Leucophaea mderae (F.) ) solid matter is lost during em~bryogenesis, although water is absorbed from the ootheca or directly from the mother (Roth and



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19551 Roth and Willis - Diploptwa dytkcoides 59 0 =WET WEIGHT
=DRY MATTER
LENGTH OF EGG IN MILLIMETERS
Figure 1. Wet weight, water, and dry matter changes of the eggs of Diploptem dytiscoides with increasing age (as indicated by increase in size). All determinations were made on oothecae containing 9 to 13 eggs, but the data are plotted on a per-eggs basis and include the weights of the oothecae. Arrow indicates first sign of visible differentiation of the embryo.
Willis, 1955). The gain or loss in water or solids by the eggs of various cockroaches during em~bryogenesi~~ is comlpared in table I. Only the egg of DipZoptera changes greatly with a truly tremendous gain in water and solids.



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60 Psyche [June
And yet, morphologically, the reproductive system of Dip- loptera is comparable to that of Blatta orienta-lis, although some of the structures in Diploptera have become modified with its altered physiology (Hagan, 1941). TABLE 1
Changes in wet weight, water, and solids of the eggs of several species of cockroaches during embryogenesis'
Species
1 Factors by which initial weights changed, I Per egg2
1 Wet weight Water Solids
Blatta orientalis3 1.21
1.35 0.96
Blattella vaga 1 1.12
1.32 0.81
Blattella germanicu 1.21
1.49 0.74
Nauphoeta cinere- 2.11
4.62 0.81
Diploptera dytiscoides \ 73.47
85.80 49.28
Of all the viviparous cockroaches, Diploptera is the most highly evolved: the oothecal covering is reduced, and the small size and number of eggs and the comparatively large size of the vestibule apparently make it possible for the female to transfer the ootheca into her (brood sac without exposing the majority of eggs outside her -body. Strictly speaking, Diploptera may be the only known case of true viviparity among cockroaches, in that the eggs are ap- parently rarely extruded beyond the vestibule and the embryos derive nourishment
(other than yolk or water)
from the female.
BIOLOGICAL OBSERVATIONS
We have frequently observed courtship and copulation. lThe data for species other than Diploptera were computed from Both and Willis (1955).
except for B. orientalis (see footnote 3), the weights of the oothecae were included in the computations, and therefore the actual changes would be somewhat larger; the youngest eggs had been recently deposited and the oldest were about ready to hatch. Factors less than unity in- dicate a decrease in weight.
"Based on eggs removed from the ootheca; the youngest eggs were 11 days old and the oldest 32 days old (about 1 week prior to hatching), so that the changes might have been somewhat higher if recently laid and fully developed eggs had been used.




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lg551 Roth and Willis - Diploptera dytiscoides 61 The active male follows the female and palpates her body or genital region. He then partly raises and flutters his wings, turns his terminal abdominal segments toward the female, pushes backward under her and grasps her geni- talia. Once they are hooked together, the male swings around into the typical opposed 'position with his head 180' from the female's. Newly emerged, teneral females are very attractive to, and are courted by, older males; 2 males were attracted to a female that was only partly out of its last nymphal skin and went through weak courting move- ments. Surprisingly, these young females mate normally (fig. 14) and in laboratory cultures the mating of teneral females is a common occurrence. According to Hlagan (1951, p. 320), sexual maturity in DipZoptera ". . . follows physical maturity rather promptly, if the presence of well developed follicles in the last nymphal instar is any cri- terion." Teneral females have been seen in copula before their wings had become fully extended; examination of one such female, after she had been in copula for more than an hour and had separated from the male, showed that she had received a spermatophore (fig. 15). Another teneral female, isolated while still in copula, separated from the male about 30 minutes after isolation. Sixty- seven days later, she give birth to 13 nymphs; temperature and humidity were uncontrolled during the gestation period. We have observed four females forming oothecae. When the first female was seen, her terminal abdominal seg- ments were slightly separated. We anesthetized the insect and, upon microscopic examination, found about 6 eggs aligned vertically in a double row in her vestibule. After the female had recovered, she began pulsating" movements, expanding- and telescoping the end segments of her ab- domen. While viewing the posterior end of the female during these movements, we could see the first egg through a hand lens. None of the eggs protruded completely be- yond her body. About three hours after the female ceased her ovipositing motions, she was dissected. The ootheca, containing 10 eggs, had rotated (rnicropyles to the left) and it lay partly in the vestibule and partly in the brood sac. The other three females were discovered in the stock



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62 Psyche [June
colony by Dr. Barbara Stay of our laboratory. Two of these were observed expanding the end of the abdomen. Although the oothecae did not protrude beyond the ends of the abdomens, the distal ends of the oothecae could easily be seen in profile as the females separated their genital segments. The axes of the eggs were vertical at this time. These oothecae were rotated a short time later, cephalic ends of the eggs to the females' left, and retracted into the 'brood sac. The females were then dissected; the oothecae contained 11 and 10 eggs, respectively.
The fourth female was seen with the first egg and parts of the succeeding two eggs protruding beyond the end of her abdomen. The axes of the eggs were vertical, but with- in a few minutes the female rotated the ootheca, as above, and retracted it. This ootheca was later found to contain 13 eggs and the female's right ovary had seven and the left six ovarioles. These observations show that our a priori hypothesis of oothecal formation in Diploptera (Roth & Willis, 1954) is correct, being similar to that found in other cockroaches.
Protrusion of eggs .beyond the end of the abdomen dur- ing oothecal formation apparently depends on such factors as size and number of eggs and size of the female. From our observations, it seems likely that few eggs protrude beyond the female's body and that protrusion occurs rather infrequently.
Since writing the above we have seen oviposition several more times ; ovipositing females were recognized when they repeatedly expanded and contracted their genital segments. The first laid egg was visible for only a short time from behind or from the 'side. Rotation and retrac- tion of the ootheca occurred rapidly, in a matter of minutes. EXPLANATION OF PLATE 5
Figures 5-13.
Eggs of Diploptera dytiscoides (X5). Figs. 5-9. Eggs of various ages showing increase in size. Actual lengths of the eggs as follows: fig. 5. 1.7 mm. (note lack of visible differentiation; upper limit of thin oothecal membrane indicated by arrow) ; fig. 6. 3.1 mm.; fig. 7. 4.3 mm.; fig. 8. 5.7 nim.; fig. 9. 6.9 mm. (arrow indicates a strand of greatly stretched, perforated oothecal membrane). Figs. 10-13. Sequence showing hatching of 2 eggs from ootheca shown in figure 9; hatching occurred within 3-minute period.




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64 Psyche [fine
The rapidity of the ovipositional sequence explains why oviposition had not been seen previously in Diploptera. In only one instance did we see a newly formed o6theca completely extruded by a female. We had previously re- moved an ootheca from this female by finger pressure against her abdomen; apparently this manipulation had damaged her reproductive organs and she was unable to direct the subsequently formed otitheca into her brood sac (fig. 2). A similar abnormality has been observed in Nawphoeta cineyea, (Roth and Willis, 1955). Females of Diploptera that were accidentally exposed to temperatures above 100å¡F were seen to abort Gthecae containing ap- parently dead eggs in various stages of development (fig. 3) ; this effect of high temperature has been observed in Pycnoscelw sumkwrm& by Roesex (1940).
Kotin-sky (1909) found a female of Diploptera d-ytis- coides which, upon being captured, dropped a "batch of embryos" which had been projecting from her abdomen; he concluded from this that the species is viviparous. In Diyloptera, the fully developed eggs lie diagonally in the brood sac with their cephalic ends pointed posterio-lateral- ly. The head of the full-grown embryo nearest the genital opening of the female may protrude slightly from the brood sac; if the female's genital segments are spread apart, the embryo's head may be readily seen (fig. 4). We have observed hatching of Diploptera several times. The abdomens of females carrying fully developed embryos be- come so distended that the intersegmental membranes be- tween the abdominal sternites are visible. The mature embryos are extruded head first (figs. 16-18). They ap- pear by pairs, swallowing air, the heads of successive pairs EXPLANATION OF PLATE 6
Figures 14-18. Diploptera dytiscoides. Fig. 14. Older, dark-colored male in copula with a recently emerged, teneral female. Fig. 15. Spennato- phore (narrow region is the anterior part) removed from a mated teaeral female.
Figs. 16-18. Female giving birth ; time interval between figures 16 and 17 was 9 minutes; that between 17 and 18 was 22 minutes. This female gave birth to only 6 individuals; the others of the brood failed to emerge from th
about X 13 all other figures about
twice natural size.)




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66 Psyche [June
appearing before the preceding pair has completely freed themselves from their embryonic membranes. The embry- onic membranes slip back toward the nymphs' caudal seg- ments while they are still held by the genital segments of the female.
When the nymphs drop from the mother
and move off, the membranes are left behind attached to the vestigial ootheca in the posterior part of the female's genital cavity. The ootheca and embryonic membranes adhere to the female until all the eggs hatch, after which the female expels them, if necessary, with the aid of her hind legs. Thus, the birth product of Diploptera is an em- bryo devoid of a ohorion, ootheca, and even the embryonic membrane. This type of birth is characteristic of truly viviparous insects (Hagan, 1951). In Nauphoeta and a number of other so-called ovoviviparous species the final birth product is frequently, if not always, the ootheca containing fully matured embryos which begin to hatch after the ootheca has passed beyond the caudal extremity of the female (Roth and Willis, 1954). We have found the pleuropodia of the embryos left behind with the ootheca and embryonic membranes ; apparently the pleuropodia are severed from the body at or before hatching time. We (1954) have questioned whether the so-called ovo- viviparous cockroaches are truly viviparous because their oothecae are first extruded externally during formation and then retracted into the brood sac. Hagan (1954) sug- gests that the extrusion and retraction of the ootheca into a brood sac represents ". . . a special case of maternal care of the ootheca and its ova." Some oviparous Homop- tera plalce their eggs in a fold in the hypodermis, a loca- tion foreign to the reproductive system, until they hatch (Hagan, 1953).
The extrusion and retraction of the eggs of the so-called ovoviviparous cockroaches is comparable to the homopteran behavior, with the exception that the oviposition site is a brood sac within the reproductive system.
When the new-born nymphs of Diploptera eliminate the air which distends itheir bodies (fig. 18), they may eat the embryonic membranes and sometimes the ootheca as well. These first instar nymphs are unduly large in com-



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19551 Roth and Willis - Diploptera dytiscoides 67 parison with the nymphs of other species of cockroaches, even those with adults twice the size of the adult Diplop- t era.
Mr. George Riser, formerly of our laboratory, working on the life history of Diploptera, has found that at 85OF. eggs hatch about 58 days after the female has mated; al- lowing albout a week after copulation for oothecal forma- tion, embryogenesis takes about 50 days. He also found that nymphal development took about 38 days for males (9 individuals) which molted only 3 times; females (13 individuals) took about 50 days to mature and underwent 4 molts.
Molted skins are not eaten \by nymphs or adults. We thank Dr. Harold Hagan for his interest and for critically reading the manuscript.
The eggs of the viviparous cockroach Diploptera dytis- coides 'absorb both water and solid matter from the female. During embryogenesis, dry matter in the eggs may in- crease about 50 times and the water content may increase about 85 times. In its embryonic development, Diploptera is unique among cockroaches in that the embryo gains solids from the mother in addition to the yolk initially present in the egg.
In laboratory colonies, teneral females mate normally with older males. The ootheca is formed as in other species of cockroaches: the eggs are extruded from the oviduct and arranged vertically in an ootheca within the vestibule. Sometimes one egg (the first laid) may protrude beyond the end of the abdomen, but most of the eggs remain with- in the vestibule while the female rotates the ootheca and starts retracting it into her brood sac. The number of eggs per ootheca ranged from 9 to 13, with a mean of 11.4. Embryogenesis takes 50 or more days. The embryos hatch in pairs, being extruded head first from the female. Male nymphs took about 38 days to mature, molting 3 times; females became adults after about 50 days, molting 4 times.




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68 Psyche
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FULLAWAY, D. T. and N. L. H. KRAUSS.
1945. Common insects of Hawaii. Tongg Publ. Co., Honolulu, Hawaii. 228 pp.
HAGAN, H. R.
1939. Diploptera dytiscoides, a viviparous roach with elongate pleuro- podia. Ann. Ent. Soc. Amer. 32 (2) : 264-266. 1941. The general morphology of the female reproductive system of a viviparous cockroach, Diploptera dytiscoides (Serville) . Psyche. 48 (I): 1-9.
1951. Embryology of the viviparous insects. The Ronald press Co., New York. 472 pp.
1953. Balanced and unbalanced evolutionary sequences with observa- tions on the hazards to fertilization in insects. Biol. Rev. City College of New York. 15 (1) : 19-24.
1954. Personal communication.
KOTINSKY, J.
1909. Notes and exhibitions. Proc. Hawaiian Ent. Soc. 2 (2) : 71. ROESER, G.
1940. Zur Kenntnis der Lebensweise der Gewachshausschabe Pycnos- celus surinamensis L. Die Gartenbauwissenschaft. 15: 184-225. ROTH, L. M. and E. R. WILLIS.
1954. The reproduction of cockroaches. Smithsonian Misc. Coll. 122 (12) : 1-49.
1955. Water content of cockroach eggs during embryogenesis in re- lation to oviposition behavior. Jour. Exp. Zool. 128.



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