oogenesis and fertilization in thermobia domestica...

OOGENESIS AND FERTILIZATIONIN THERMOBIA DOMESTICA (PACKARD)

BY JOHN T. WOODLANDState Teachers College, Salem, Massachusetts

The materials and methods used in this study were thesame as those described in an earlier paper (Woodland,1957).

OogenesisThe primary oocytes in the vitellarium reach a length of

about 420 microns just before yolk accumulation begins.They measure only about 45 microns wide. Each has alarge central nucleus about 40 microns in diameter. It isa typical vesicular oocyte nucleus and usually has a visiblenuclear membrane. A fine network is visible throughoutthe nucleus and there is a large, eccentric, irregular, granu-lar nucleolus which may be as long as 20 microns. Neithernetwork nor nucleolus is Feulgen-positive. The finely-divided chromatin is so scattered throughout the largenucleus that it is barely visible. The cytoplasm appears veryfinely granular and contains a few inclusions. These are 10to 15 microns in diameter and consist of a dozen or lessclumped globules.When each o’ the vitellaria contains four or five of these

oocytes, yolk accumulation begins. It starts peripherallyin all of the oocytes simultaneously and gradually proceedstoward the center. There appear scattered through theperipheral cytoplasm tiny globules which stain brightorange-red with Mallory’s triple stain. They greatly re-semble the globules of p:otein reserves scattered throughthe fat body surrounding the ovarioles, but are usually alittle smaller. The negative images of small fat dropletsalso occur in the peripheral cytoplasm. The fat dropletsand proteinaceous globules increase in size, forcing thediminishing cytoplasm into a network around them. By

]The research was carried out at the Harvard BiologicalLaboratories, Cambridge, Massachusetts, in partial fulfillmentof the degree of Doctor of Philosophy.

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12 Psyche

the time that small 2at droplets begin to appear in thecenter o2 the oocyte, the peripheral droplets and protein-aceous globules have greatly enlarged (3 to 7 microns indiameter) and ae present in about equal numbers. Thediminishing central layer o cytoplasm around the nucleusis connected by the fine network between the yolk globulesto a thin peripheral cytoplasmic layer, the periplasm. Bythe time the perinuclear cytoplasm has become very thin,the 2at droplets appear to have coalesced, or the visiblepoteinaceous yolk globules, some o which are now as largeas 11 microns in diameter, stand out in fixed preparationsagainst a clear background.The oocyte has been growing only slightly meanwhile,

and is still very narrow in proportion to its length. Beforeoviposition the maximum length o the egg increases byabout two and one-hal2 times, and its maximum widthincreases about eighteen times. Growth is accomplishedchiefly by an increase in the proteinaceous yolk. Just beforeoviposition the egg contains relatively little atty yolk.At the start o the growth period the nucleus moves to

the periphery. The nuclear network condenses at the peri-phery o2 the nucleus and the chromatin becomes distinctlyvisible with the Feulgen technique. Evidence o tetrads isseen. The interior o the large nucleus now appears homo-geneous and has little affinity or the stains used. Beforeoviposition there occur both a marked decrease in nuclearvolume and iurther condensation o2 the chromatin intosmall compact chromosomes.The 2ollicle cells start to secrete the endochorion at the

time when yolk accumulation first begins. The process isbest studied in preparations stained with phosphotungstichematoxylin. Just before secretion of the endochorionstarts, the brown-staining connective tissue sheath sur-rounding the ovariole becomes greatly thickened. It ap.-pears that the ollicle cells withdraw material irom thesheath and secrete it to orm the endochorion. Comparisonwith the accompanying process oi yolk accumulation indi-cates that the sheath is reduced to its ormer size withina relatively short time. The secretion of the exochorion,which occurs much later, is mentioned below.

1958] Woodland--Thermobia domestica (Packard) 13

The external appearance of the newly laid egg of thefirebrat has been described by Adams (1933), Sweetman(1938), and Remington (1948). The present study revealsthat the endochorion (Fig. 5, EN) is about 2 microns thick.Its thickness does not vary appreciably over the whole egg.There adheres to its outer surface a single layer of sphericaldroplets, each about 11 microns in diameter immediatelyafter oviposition. The droplets are rather irregularly placed,but tend to be in groups with large intervening spaces. Inthe spaces are droplets many times smaller than the largeones. Within a ew hours a change occurs. The largedroplets break up into rather evenly spaced ones about 3microns in diameter (Fig. 5, CD). Usually a space of 2microns now occurs between droplets, although pairs o.contiguous droplets are sometimes seen. The very minutedroplets are still scattered among the. larger ones. Theappearance o the droplets is essentially the same on shedchorions long after the nymphs have left them. Possiblythe droplets are present as a thin continuous film beforeoviposition.The droplets adhere firmly to the exochorion. A ew

individual droplets are separated 2rom it by sectioning, butthe other procedures to which the eggs have been subjectedpractically never dislodge them. In contrast, the exochorionis loosened irom the endochorion when the egg contentsshrink during fixation, owing to dissolution of the fattyelements. Moreover, the exochorion is normally loosenedfrom the endochorion during devel.opment, as the volumeo the egg contents is diminished slightly. The surface othe endochorion is then seen to be reticulated into hundredsof small polygonal areas. Most of these polygons are airlyregular hexagons with diagonals usually between 55 and 85microns long. The wall separating adjacent areas is 5microns thick.Sweetman (1938) supposed this hexagonal reticulation

to be produced by the cells of the embryonic tissues, butthe present study showed it to be produced by the ollicularcells that secreted the endochorion. The large size of thehexagons emphasizes the amount the egg has grown sincethe endochorion was secreted.

14 Psyche

The endochorion is hardly ever loosened at all rom theyolk and no vitelline membrane has been ound betweenthem. Heymons (1897) reported a vitelline membrane inLepisma saccharina, but Uzel (1898), who studied the eggso2 the same lepismatid, did not mention it.Between the exochorion and the endochorion at the an-

terior end o the egg is the micropylar area, a circularthickening about 280 microns in diameter (Fig. 5). Thethickening consists oi as many as twenty or more concentriclamellae, each about as thick as the exochorion, with whichthe thickening is identical in staining reactions and to whichit adheres if the latter becomes loosened rom the endo-chorion. The thickening is thinner peripherally than cen-trally, since not all of the lamellae extend to the marginoi the area.

In the micro.pylar area are found three small infundibulardepressions which, if connected, would orm the cornersof an equilateral triangle. Two of the depressions are shownin figure 5 (DP). The depressions, which can rarely bedemonstrated to penetrate the micropylar thickening com-pletely, are filled with olds of the exochorion and with thechorionic droplets described above. There sometimes ap-

EXPLANATION OF PLATE 2All figures represent portions of sections. Fixative: Maximow’s. Stain:

Feulgea’s all figs. except 2 and 5; Mallory’s triple, figs. 2 and 5. Magnifi-cations approximate. Fig. 1. 20 minute old egg, showing sperm head ac-cumulating cytoplasm, 400 x. Fig. 2. 30 minute old egg, showing egg nucleusin anaphase of first maturation division, 500 x. Fig. 3. 21/ hour old egg,showing egg nucleus in anaphase of second maturation division, 500 x.Fig. . 75 minute old egg, showing late telophase of first maturation divi-sion; secondary oocyte nucleus forming in upper left, first polar body inlower right; 500 x. Fig. 5. Longitudinal section through micropylar (an-terior) end of 2 hour old egg, 160 x; CD, chorionic droplet; DP, depres-sion; EN, endochorion; EX, exochorion; EXT, exochorionic thickening.Fig. 6. 90 minute old egg, showing late stage in the contraction of thesperm head, 1250 x. Fig. 7. Egg about 2 hours old, showing male pronuc-leus during its growth period; 1875 x. Figs. 8-11. 3 to 4 hour old eggs, 1250x. Fig. 8. Early stage of union of male and female pronuclei. Fig. 9. Femalepronucleus shown near top just enteriing the sperm plasm; male pronucleus(below). Fig. 10. Female pronucleus (below) and male pronucleus (above)about to unite. Fig. 11. Late stage of union of male and female pronuclei.

PsYcu, 1958 VOL. 65, PLATE 2

EXT

I0 II

WOODLAND TI-IERMOBIA DOMESTICA

16 Psyche

pears to be an opening through the exochorion where itdips into a depression (Fig. 5), but no opening through theendochorion was ound. Other evidence suggests that thereis none. Eggs completely immersed in tap water at 37.5 C.for a period of 3 or 4 days during incubation hatch intohealthy nymphs in about the normal time. (Hatching itselfoccurs under water, but the nymphs cannot get theirabdomens out o the shell. This is because they cannotget traction and also occurs in a small percentage oi eggshatching in an empty glass container.) If openings com-pletely penetrated the chorion, then water should be ex-pected to. enter the egg by osmotic pressure and cause itto burst. If eggs are kept in tap water or as long as sevendays, the incubation period is prolonged by several daysand only about half oi the eggs hatch at all. Those nothatching do not burst nor are they turgid. Presumablythey die rom oxygen lack, as the water was not mechanical-ly oxygenated.The ollicle cells appear to become a syncytium during

the enlargement of the oocyte. This syncytium probablysecretes the micropylar thickening and the thin structure-less exochorion just before the oocyte leaves the ovariole.The chorionic droplets are believed to be added as the eggpasses through the lateral oviduct, or droplets of similarappearance have been seen in the cells o.f the oviducal epi-thelium o emales with large oocytes in the ovarioles.

FertilizationAter the oocyte leaves the gonopore but before it pro-

ceeds down the ovipositor, it is undoubtedly held at the baseo the ovipositor 2or a ew moments while sperms are dis-charged onto it by the spermatheca. The sperms presum-ably enter the probable openings in the exochorion over thedepressions in the micropylar thickening. They can appar-ently penetrate the endochorion directly. They would nothave to penetrate the endochorion directly under the micro-pylar thickening, but could pass between the la.mellae of thethickening and enter nearer the equator o the egg.Whether the entire sperm penetrates the egg was not deter-mined. Within the reshly laid egg, however, may usuallybe identified rom one to six of the very long sperm heads,


each of which is bent and coiled upon itseff many times.The contents of the living, freshly laid egg appear to

consist o colorless yolk spheres in a colorless liquid of lowviscosity. The spheres are about 10 to 15 microns indiameter. In sections of eggs fixed with Maximow’s fluidthe negative images o the iat spheres measure 9 or 10microns in diameter. Most o the more numerous, visible,proteinaceous yolk globules are 14 or 15 microns in diameter.Some o these globules appear structureless, while othersappear finely granular. The globules appear only very slight-ly flattened at the poles with Maximow’s fixative. The otherfixatives used always badly distorted the yolk o youngeggs. The yolk spheres and liquid fill the, entire egg. Cyto-plasm was not identified.

Perrot (1933) stated that the first maturation divisionoccurs while the oocyte is still in the ovariole. He was notable to find any trace oi the prophase of the division. Hereported that the mitotic figure occupies a very small spaceat the periphery of the oocyte and figured the anaphase ofthe division. He stated urther that after this first matura-tion division the nucleus enters a resting stage which hefigured rom a reshly laid egg. The present study did notconfirm this part o Perrot’s work. The only mitotic figuresever found in sections through the vitellarium were thoseof the 2ollicle cells. The anaphase o such ollicular mitosesoften resembles that shown in the first of Perrot’s figuresjust mentioned. Eggs fixed immediately after ovipositionshow the nucleus to be in the metaphase o the first matura-tion division. No nucleus resembling both in appearance andposition that shown in the second of Perrot’s figures wasfound until the beginning o the ormation oi the primaryepithelium.The anastral type o meiosis occurs. The mitotic figure is

located more or less equidistant rom the two. poles of theegg, usually rom 1 to 10 microns rom the surface. Thespindle axis is usually oblique to the egg surface, but isoccasionally parallel to it. The distance between the twopoles of the mitotic figure in metaphase and in anaphase(Fig. 2) is about 20 microns. The metaphase plate is about8 microns in diameter. The chromosomes are very small

18 Psyche [

and close together. During telophase the mitotic figure isno longer 2usiform, but is a spheroid with long axis about14 microns long and short axis about 10 microns long. Inpresumably slightly older eggs a very distinct equatorialconstriction is evident. The two groups o2 chromosomesseparate to a distance oi almost 30 microns. In avorablysectioned eggs most o the eighteen dyads in each groupcan be distinguished (Fig. 4). Many o the chromosomesare very short and V-shaped, so that the dyads look super-ficially like tetrads.The first polar body is not extruded rom the egg and

does not divide. Its chromosomes never become surroundedby a nuclear membrane as do those o the secondary oocyte.The dyads gradually change into an irregular mass, whichremains close to the surface oi the egg and disappearsrelatively quickly. No certain trace o the first polar bodywas ound later than the anaphase o the second maturationdivision.The egg nucleus was never ound in a resting stage be-

tween the maturation divisions. The spheroidal prophasenucleus, with its still distinguishable dyads, is believed toincrease in size, since a series has been ound with long axisvarying rom 8 to 15 microns in length. The second matura-tion division resembles the first in size and orientation, butits chromosomes are slightly more easily distinguishable(Fig. 3). The second polar body degenerates as does thefirst and has not been seen with certainty later than theour-celled cleavage stage. The chromosomes o the emalepronucleus enter a resting stage with distinct nuclear mem-brane. The nucleus is a spheroid with long and short dia-meters o2 9 microns and 5 microns respectively. It showshardly any variation rom egg to egg.

In the majority o reshly laid eggs, cytoplasm is seenstarting to accumulate around one of the sperm heads (Fig.1). This sperm and its sperm plasm are typically ound onthe longitudinal axis oi the egg, about one-third o the wayrom the posterior pole to the anterior pole. The distancerom the maturation spindle is roughly 400 microns. Ifseveral sperms are present in the egg, cytoplasm may ormay not accumulate around more than one. In cases where

1958 Woodland---Thermobia domestica (Packard) 19

cytoplasm accumulates around rom two to six sperms, theirdstribution is such that they are about equidistant romeach other and rom the surface of the egg. Just as muchcytoplasm accumulates around a sperm whether it is theonly one accumulating cytoplasm or whether five others aredoing likewise. Accumulation o the sperm plasm ceases atabout the time the oocyte nucleus has completed its firstmaturation division. By that time the sphere o spermplasm is about 45 microns in diameter.As cytoplasm accumulates around a sperm head, the latter

undergoes a gradual decrease in length, with accompanyinguncoiling and moderate increase in breadth. The Feulgenreaction indicates a simultaneous concentration o2 desoxyri-bonucleic acid toward the anterior end o2 the shorteningsperm head (Fig. 6). Shortening continues until all that isvisible within the sperm plasm is a minute nucleus about1/ microns long. This male pronucleus is ormed at aboutthe time that accumulation o2 sperm plasm ceases. Whilethe egg nucleus is undergoing the second maturation divi-sion, the male pronucleus gradually enlarges (Fig. 7) untilit is about 8 or 10 microns in diameter (Fig. 9).The 2emale pronucleus then migrates rom its peripheral

position to the sperm plasm (Fig. 9). When fixed before itreaches the sperm plasm, it is ound to be rather irregularlyelongated in the direction in which it was presumablytravelling. Cytoplasm has never been identified around it.Both male and 2emale pronuclei are approximately the samesize and their finely divided chromatin appears very similar.Fortunately they can easily be distinguished when theFeulgen reaction is followed by light green counterstain.The nuclear sap o2 the male pronucleus shows great affinityor light green, while that o the emale pronucleus showspractically none at all. It appears 2urther that the move-ment of each nucleus within the sperm plasm just priorto fixation can be detected. For adjoining each nucleus fixedat this stage is a palely-staining streak which is interpretedto indicate the path over which the nucleus has just passed(Fig. 10).As the emale pronucleus enters the sperm plasm the

sperm nucleus starts to move toward it. The two pronuclei

20 Psyche [Mar

come together and their nuclear membranes break downwhere they are in contact with each other (Fig. 8). At thesame time the chromatin of each condenses into a finespireme. The nuclear sap o2 the emale pronucleus simul-taneously develops an affinity for light green, so that the twopronuclei can no longer be distinguished. The spiremes otthe two nuclei become coarser and intermingle before anydistinct chromosomes are visible (Fig. 11). The maturationdivisions occupy about one and one-hali hours each. Unionof the pronuclei occurs during the ourth hour after ovi-position.

Affinities of LepismatidsThe lepismatids for which both embryological and mor-

phological data are available are Lepisma saccharia L.(Heymons, 1896, 1897; Uzel, 1897, 1898), Thermobia do-mestica (Packard) (Woodland, 1952, 1957; Sahrhage, 1953;Wellhouse, 1953), and Ctenolepisma lineata Fabricius(Woodland, 1957). All three belong to Subfamily Lepis-matinae. The data indicate that Thermobia domestica andCtenolepisma lineata are very closely related to each otherand less closely related to Lepisma saccharina, which is moreprimitive han they.Thermobia domestica and Ctenolepisma lineata differ

embryologically from Lepisma saccharina in that in themthe germ disk is iormed at the extreme posterior end of theegg, radial symmetry is maintained until the germ diskstarts to elongate, the embryo does not sink bodily into theyolk, the amniotic pore is not closed by a chitinous plug, andspiracle anlagen are not ound on the ninth and tenth ab-dominal segments. Adults of Thermobia domestica andCtenolepisma lineata differ irom those o Lepisma saccha-rina by lacking parameres and by possessing ventricularcaecae, an anterior projection of the vas deferens beyondwhere the most anterior pair of vasa efferentia empties intoit, and often a third pair of styli. In the former two speciesthe vasa efferentia of the members of a pair of sperm tubesdo not unite before joining the vas deferens and the free endof one member of each pair of sperm tubes is directedmediad, while the free end of the other member is directedlaterad. In addition, the lateral oviducts are relatively

1958] Woodland---Thermobia domestica (Packard) 21

shorter han in Lepisna saccharina. The au’thor considersall of these characters to be secondary or specialized ones.Remington (personal communication, 1949) has noted sev-eral taxonomic characters as evidence for considering Le-pisma saccharina more primitive than he other two species"the cephalic hairs of the former occur singly and do notbear secondary hairs, while those of the latter occur ingroups and bear secondary hairs; also, the former has aless well developed ovipositor.

In spite of the close relationship between Thermobia do-mestica and Ctenolepisma lineata, each has a few specializedcharacters not shared by the other. In Ctenolepisma lineataa modified morula stage is absent, synchrony of cleavage ismaintained longer, and intravitelline separation occurs late.In Thermobia domestica the amnio-serosal folds developonly weakly and there is a transverse division of the distalsegment of the maxillary palpus.

Although the embryology of lepismatids and symphylansappears superficially very different, owing to the differencein rel,ative amounts of yolk in the eggs of the two groups,actually a great deal of embryological affinity exists betweenthem. Some of the characters shared by Thermobia domes-tica and the symphylan Hanseniella agilis (Tiegs, 1940) areof particular interest: (1) The polar bodies are not ex-truded from the egg and degenerate rapidly. (2) A vitellinemembrane is not apparent. (3) Periplasm has not beenidentified in freshly laid eggs. (4) The inner layer is en-tirey mesodermal and is produced withou the formationof a ventral groove. (5) The time and manner of segrega-tion of the germ cells are similar. (6) The surface cellssecrete a cuticle, in Hanseniella before germ band forma-tion, in Thermobia after germ disk formation. (7) Themidgut epithelium is derived from yolk ceils. (8) The neu-ropile of the nerve cord is not covered dorsally by nervecells. (9) Fourteen post-cephalic segments occur in theadult. Anamorphosis occurs in Hanseniella but not, ofcourse, in Thermobia. It may be noted, however, thatHanseniella hatches with 8 post-cephalic segments followedby a pre-anal and an anal segment. During anamorphosis4 more segments differentiate in front of the pre-anal seg-

22 Psyche [March

ment. In Thermobia a distinct pause occurs after differen-tiation of the first 5 abdominal (first 8 post-cephalic) seg-ments. The cercus-bearing (pre-anal) and anal segmentsare prominent during the interval before the remainingabclominal segments are differentiated in ront of them.The characters in which Hanseniella differs from Ther-

mobia may be grouped into several categories. Examples ofcharacters with homo!ogs in some primitive or generalizedinsects, but not in Thermobia, are: (1) Paired arteriesarise from the aorta. (2) The presence of eversible sacsand coxal styli. Homologs of both of these structures arepresent in Machilis. In Hanseniella the two halves of thenerve cord arise laterally from the floor of the germ bandrather than medially as in Thermobia. In Hanseniella themedial position is occupied by the "ventral organs" fromwhich the eversible sacs arise. Examples of charactersmore primitive than those found in primitive insects are"

(1) The adult has abdominal legs. (2) Only one pair ofMalpighian tubules is present. (3) The labial segment isat first not part o the head. A ew o tle characters ofHanseniella, such as the secondarily acquired progoneatec.ndition and the development oi fat body from yolk cells,seem to express affinity with diplopods or as the incorpora-tion of a pre-antennary ganglion into the brain, with chilo-pods. Other characters oi Hanseniella, as the absence ofeyes and the presence of only a single pair of tracheae(cephalic), are specializations which are probably adapta-tions to its environment of decaying oliage and rottinglogs.

The following embryological differences between Han-seniella and lepismatids are considered by the author to bethe result largely o2 the difference in relative volume of yolkin their eggs. In Hanseniella: (1) Cleavage is total (2)The germ band is long and rom the beginning representsthoracic and abdominal as well as cephalic material. (3)Absence of embryonic membranes; the germ band does notsink into the yolk. (4) Early eclosion, with subsequentanamorphosis. Actually nutritive value oi the yolk ratherthan volume is concerned here. Information is not availableon this subject in insects.


Tiegs (1940), however, deems it erroneous to considerthe type of cleavage as simply the mechanical result of thequantity of yolk within the egg. In support of this conten-tion he says that the eggs of symphylans are not unusuallysmall, though cleavage is total. But consider the followingcomparison. The egg of Hanseniella is spherical, averaging0.37 mm. in diameter; the long diameter of the ellipsoidalegg of Thermobia averages 1.00 mm., the short diameter0.80 mm. At hatching, Thermobia measures 1.5 mm. long,exclusive of appendages. We deduce that Hanseniella alsomeasures close to 1.5 mm. long at hatching, for the follow-ing reason. The circumference of a sphere 0.37 mm. indiameter is 1.2 mm. The body of the embryo is curved in acircle around the entire circumference of the egg, but is alittle longer than the circumference since the bent head isdirected inward. We therefore conclude that the egg ofThermobia contains a relatively much larger percentage ofyolk than does the egg of Hanseniella.

Tiegs further supports his statement by noting that sometiny, yolkless insect eggs have superficial cleavage (Fer-nando, 1934). But there is no reason to suppose that super-ficial cleavage, once established, would not be as satisfactoryfor yolkless as or yolk-rich eggs. We do not consider, how-ever, that this fact invalidates the theory that superficialcleavage was originally developed as an adaptation to large,yolk-rich eggs.

Although only one species of perlarian has been thorough-ly studied embryologically, Miller’s detailed account (1939,1940) of Pteronarcys proteus reveals a number of similari-ties between the embryology of this perlarian and that oflepismatids" (1) Practically no cytoplasm is present infreshly laid eggs. (2) The embryonic rudiment representschiefly cephalic material. (3) The germ band is of the im-mersed type. (4) The inner layer represen.ts mesodermonly and is produced without the formation of a ventralfurrow. (5) The mesoderm of the eleventh abdominal seg-ment shows no coelomic sacs. (6) Transitory appendagesappear on the intercalary segment and on abdominal seg-ments two "o ten.

24 Psyche [Mam

LITERATURE CITED

ADAMS, J. A.1933 Biological notes upon the firebrat, Thermobia domestica Packard.

J. N. Y. Ent. Soc., 41: 557-562.

FERNANDO, W.1934 The early embryology of a viviparous psocid. Quart. J. Micr. Sci.,

77: 99-119.

ttYMOS, R.1896 Ein Beitrag zur Entwicklungsgeschichte der Insecta apterygota.

Sitz. -ber. KSnigl. Preuss. Akad. Wiss., Berlin, 51: 1385- 1389.1897’ Entwicklungsgeschichtliche Untersuchungen an Lepisma saccharina

L. Zeitschr. Wiss. ZoS1. 62: 583-631.

MILLER, A.1939 The egg and early development of the stonefly, Pteronarcys pro-

teus Newman (Plecoptera). J. Mo.rph. 64: 555-609.1940 Embryonic membranes, yolk cells, and morphogenesis of the stone-

fly, Pteronarcys proteus Newman. Ann. Ent. Soc. Amer., 33:437-477.

PERROT, t. L.1933 La spermatogense et l’ovogense de Lepisma (Thermobia) dornes-

tica. Htropycnose dans un sexe homogametique. Zeitschr. Wiss.Biol. Abt. Zellf., Mikr. Anat., 18: 573-592.

REMINGTON, C. L.1948 Studies in the North American Thysanura. Unpublished thesis.

Harvard University, Cmbridge, Mass., 1-178.

SAttRI-IAGE, DIETRICH1953 Okologische Untersuchungen an Thermobia domestica (Packard)

und Lepisma saccharina L. Zeitschr. Wiss. ZoSl., 157: 77-168.

SWEETMAN, I-I. L.1938 Physical ecology of the firebrat, Thermobia domestica (Packard).

Ecol. Monogr., 8: 285-311.

TIEGS, O. W.1940 The embryology and affinities of the Symphyla, based on a study

of Hanseniella agilis. Qua.rt. J. Micr. Sci., 82: 1-225.

UZEL H.1897 Vorlufige Mittheilung fiber die Entwicklung der Thysanuren.

ZoS1. Anz., 20: 125-132.

1958 Woodland--Thermobia domestica (Packard) 25

1898 Studien fiber die Entwicklung der Apterygoten Insecten. K. Fried-linder und Sohn, Berlin. 1-58.

WELLOVSE, W. T.1953 The embryology of Thermobia domestica Packard (abstract of

doctoral thesis). Iowa State College J. Sci., 28: 416-417.

WOODLAND, J. T.1952 The styli of the firebrat, Thermobia domestica (Packard). Proc.

Pa. Acad. Sci., 26: 27-32.1957 A contribution to our knowledge of lepismatid development. J.

Morph., 101: 523-577.

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