Recent Advances in Insect Embryology in Japan
Edited by H. Ando and K. Miya.
ISEBU Co. Ltd., Tsukuba 1985

45

Oogenesis and Embryogenesis of the
Idolothripine Thrips, Bactrothrips brevitubus(Thysanoptera, Phlaeothripidae)

Kazuo HAGA

Synopsis
The oogenesis and embryogenesis of Bactrothrips brevitubus are described and illustrated. The egg has
a discoidal oosome near the posterior pole. Two mycetomes may always be found in each of the egg. The
chorion is polygonally reticulated at the anterior third; neither the micropyle nor aeropyle are observed.
The cleavage center locates at the posterior third of the egg and the energids distribute more abundantly in the posterior half than in the anterior one. At the posterior pole of the egg the ventral plateinvaginates and grows into the core of the egg, and within the yolk double-flexed S-shaped germ-band isconsequently formed. The inner layer is formed by the cell proliferation. Katatrepsis of the embryooccurs at about the middle ·of embryonic development. The embryo rotates within the sagittal plane of
the egg during this process.
The ventral nerve cord in the abdomen is seen to condense at the later phase of embryogenesis, andfinally it becomes one big, spindle-shaped ganglion which situates in the thorax. Two pairs of salivary
glands are invaginated from the labium. An unpaired mandibular gland is present, appearance of which
is similar to the dorsal labial gland. A pair of invaginated type pleuropodia is formed on the first abdominal segment of the embryo. The germ cells are enclosed with the inner layers of the seventh and eighth
abdominal segments, and later migrate to the fifth segment to form gonadal rudiments.
The midgut epithelium is derived from the rudiments occurred at the both ends of the embryo. The
yolk cells form thin expanded membranes enveloping yolk globules during the process of mid-gut formation. Posterior portion of the midgut originally derived from the bipolar midgut rudiments is seen toform a chamber at the later phase of its development, into which liquefied yolk is subsequently incorporated.
The rudiment of malpighian tubules occurs in the telson as four glomerate cell masses as early as theproctodaeum develops.
Six paraneopteran orders are compared from a view point of thtl embryonic development. From theresults of this comparison it is thought that the Thysanoptera possibly situates equidisLmt from the46

Haga, K.

Psocoptera, Homoptera and Heteroptera but far from the Mallophaga and Anoplura.
Thysanoptera must have derived from the ancestral group of Paraneoptera at the early phase of its
ramification.

Introduction
The Thysanoptera is one of the insect orders that have scarcely been studied in the fieldof embryology, and only a few contributions of the embryogenesis are known up to thistime.
The first description on the embryogenesis of the Thysanoptera appeared as early as 1874
by Uljanin who observed Thrips physapus (Terebrantia : Thripidae) embryos externallythrough the chorion. The embryonic development of the mouth-parts of Heliothrips haemorrhoidalis (Terebrantia: Thripidae) was partially studied by Reyne (1972). Bournier(1960, 1966) studied the embryogenesis of Caudothrips (=Bactrothrips) bullai (Tubulifera : Phlaeothripidae), and the gross embryology of Thysanoptera was revealed by him.
Recently, Ando and Haga (1974) observed the pleuropodia of the present material,
Bactrothrips brevitubeus. Most recently, Heming (1979, 1980) studied the embryos of
Haplothrips verbasci (Tubulifera : Phlaeothripidae) with special reference to the origin
and fate of the germ cells and development of the mouth-parts.
The knowledge on the embryology of thrips, however, is still very insufficient as contrasted with other insect orders, and detailed study on the embryogenesis of the order has
never been accomplished.
Since B. brevitubus and allied species often retain eggs in the oviducts, and oviposit justfertilized, or embryo logically developed eggs (Haga, 1975), oviposited eggs as well as thoseretained in the oviduct are employed for observation.
On the other hand, ovaries in the adults of various Thysanoptera are studied anatomically (Jordan, 1888; Uzel, 1895; Sharga, 1933; Melis, 1935; Bournier, 1956; Heming,
1968; Lewis, 1973; Haga, 1975). They show that each four panoistic ovarioles are foundin a ovary without exception, but the type of ligation of the terminal filaments differ in a
sub familial level as discussed by Haga (1975). However, only a contribution on the development of the ovary was given by Heming (1970), who observed Frankliniella lusca (Terebrantia) and Hap[othriPs verbasci (Tubulifera), and no paper concerning the oogenesisof the order has appeared.
In this paper, the oogenesis and embryogenesis of B. brevitubus, together with someobservations on the same topics of the allied species, are studied and described.

Materials and Methods
One of the largest thrips occurred in Japan, Bactrothrips brevitubus Takahashi (Thysanoptera, Phlaeothripidae, Idolothripinae) was used for the present studies. It lived on deadfoliage of evergreen trees, mainly a kind of the chinquapin, Castanopsis cuspidata which
distributes throughout the warm-temperate zone of Japan. In addition, a species of the same
genus, B. honoris (Bagnall) was used for the material of the embryological studies. B.
brevitubus and B. honoris were collected in Mino-o of Osaka, Kasuga-Yama of Nara, andOogenesis and Em bryogenesis of Bactrothrips

47

Mt. Tsukuba of Ibaraki. These two species are endemic in the warm temperate zone.
These thrips were cultured in petri-dishes each with a piece of the wet blotting paper toretain moisture. They were kept in the incubator kept at 25°C throughout or under room
temperature between 20° - 25°C. As their food, the dead leaves infested by certain imperfect fungi were supplied. For the anatomical study, the thrips were .anaesthetized byethylalcohol, dissected in a physiological salt solution as used for Drosophila under a stereomicroscope. For the observation on living eggs, they were immersed in liquid paraffin orsilicone oil KF-96. The chorion became semitranslucent in the liquids, and the embryo
developed nearly alike as those in the air, but they hardly hatched.
For the observations of fixed eggs, they were stained by alcoholic thionine, cleared in
terpineol after dehydration in ethylalcohol and ethylenglycol-monoethylether. For serial
sections, eggs were fixed in the alcoholic Bouin's fluid warmed at about 60°C for half anhour or F AA fiXative for 2 to 24 hours under room temperature. They were embedded inparaffin by Miyakawa's (1978) method, cut at 5-7 .urn thickness, and stained with Delafield's haematoxylin and eosin.
16 mm time-lapse motion pictures were taken for analyzing the morphogenetic movement of developing embryos. The scanning electron microscope and differential interference
microscope were used for the studies on the egg surface and living ovaries, respectively.
Figures were drawn using Abbe's camera lucida or with free hand retouching on thephotomicrographs.

Observations
Ovarian Structure and Oogenesis
A pair of ovaries of B. brevitubus may be found along the both sides of the mid-gut(Fig. 1). The ovary consists of four ovarioles and their apices completely coalesce forming
a common germarium in which any septa cannot be observed (Figs. 2, 3AB).
As no trophocytes or nurse cells are found in the germarium and vitellarium, the ovary ofthis insect belongs to the panoistic type as observed in other thrips.
In the distal part of the common germarium several depressed nuclei are piled with amembranous, triangular terminal filament upon them (Fig. 3). The thread-like apex of theterminal filament is suspended on the dorsal labial gland (= long salivary glnad). in thesame side of the body (Fig. 1).
In the germarium three kinds of cells are recognized (Fig. 3B). The large globular cells ofthem are the primary oocytes, and have little cytoplasm and single nucleus, 5-6 .urn indiameter, with a large nucleolus and numerous peripheral chromatins. The small globularcells are the oogonia lacking such large nucleoli, but have the reticular chromatins. The
remainder cells have a flat or stick-like or irregular shaped nucleus (4. 6 -5 .urn) with
scattered chromatins. They are the rudimentary follicular cells and cytoplasmic projectionsof which are narrowly extended among the other cells. It seems that these cytoplasmic projections connect with each other and form a multinucleate tissue, but the boundary of
the projection may only become observable by the electron microscope.
The oogonia are situated in the distal part of'the germarium, while the remaining part of
it is occupied with the primary oocytes and rudimentary follicular cells. The size of the

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Fig.

Female reproductive system in B. brevitubus, dorsal view, diagrammatic.
abx 10th abdominal segment, aci acicula, bap Bournier apparetus, cod common
oviduct,
dig dorsal labial gland, [us [ustis, h head, lod lateral oviduct, ova ovary,
prt pro thorax, ptt pterothorax, std spermathecal duct, sth spermatheca.
(After Haga, 1975; modified)Oogenesis and Embryogenesis of Bactrothrips

49

nuclei of the primary oocytes is seen to increase gradually from distal to the proximal partof the germarium. No mitotic figures are observed in the germarium.
The germarium continues into four ovarioles. Each ovariole consists of 11-14 egg
chambers each of which contains single oocyte, and rarely two oocytes may be found in
the first and/or second egg chambers.
Oogenesis in B. brevitubus can be divided into five oogenetic stages.
Stage 1:

Previtellogenic stage (Fig. 38).

In this stage, smaller oocytes are cuboid, their height is smaller than width; their nuclei
are noticeably large, occupying about 4/5 of cell body. The follicular cells develop little andform a thin single sheet of cells. The clumps of two or three rudimentary follicular cells arefound among the oocytes.
In the oocyte nucleus a basophilic nucleolus consisting of several droplet-like granules isobserved, and the chromatins are seen at the subcortical layer of the nucleus. The cytoplasm
lacks the vacuoles, bacilliform substances and endobodies described by Ando (1962) in
Epiophlebia superstes of the Odonata. However, the clouded parts slightly stained byhaematoxylin in the cytoplasm are present around the nucleus in the first stage oocyte.
Stage 2:

Early vitellogenic stage (Fig. 3C).

The oocytes become globular or ellipsoid, and are surrounded by the follicular epithelium
made of coarsely arranged flat cells. The oocyte cytoplasm is poor in volume. Relative sizeof the nucleolus to the nucleus becomes smaller at this stage than that at the preceded one,but the size of the dropletlike granules mentioned before is larger.
The clouded parts in the cytoplasm mentioned earlier are also present, and in addition,
unstained, vesicle-like parts are found in the subcortical layer of the oocyte.
The interfollicular tissues between the egg chambers begin to occur in this stage. The
developed interfollictllar tissue consists of more than ten spindle-like flat cells overlappingwith each other, and the difference between 'follicular cells' and 'interfollicular cells' is onlyin shape and location.
Stage 3: Middle vitellogenic stage (Fig. 3D).
The shape of the oocyte changes into long ellipsoid, and the oocytes have a few vacuoles
around the germinal vesicle in which the nucleus is almost diffused, but reticulated chromatins are clearly appeared. The oocyte is covered by the follicular epithelium which is flattenedin the middle portion, and thick at the both ends.
Two mycetomes become observable in this stage. They are found in the anterior andposterior parts in the oocyte. They are similar in size, about 10 JllTl in diameter, and have ahemispheroid structure. The concentric region of the non-vacuolated cytoplasm, about 15
JllTl in diameter, is found around each mycetomes.
Stage 4: Late vitellogenic stage (Fig. 3E).
The height of the oocyte is about twice as long as wide; the germinal vesicle is a little

1,/1

o

::I:

'"

O<l

,p>
~

Fig.

2.

Ovary of B. brevitubus. (Differential interference micrograph of a living ovary.)
Scale : 50 pm
cx calyx,
fe follicular epithelium,
gr germarium,
gv germinal vesicle,
myr mycetomic granule, myt mycetome, nlo nucleolus, pi pedicel, tf terminal filament .

Oogenesis and Embryogenesis of Bactrothrips

51

enlarged, but its ratio to the oocyte is smaller than that in the former stage.
In this stage important and rapid changes take place concerning the germinal vesicle,
oocyte cytoplasm, follicurar epithelium and mycetomes. The germinal vesicle is graduallytransformed into an amoeboid shape while its reticular chromatins become paler and begin
to diffuse. Fine yolk droplets, approximately 1 Ilm diameter, appear in the subcorticallayer of the oocyte cytoplasm. They increase in number and the size, and subsequently
they are observed among the cytoplasmic reticulum. These yolk droplets have an affinity
to eosin and different kinds of yolk are not observable.
The mycetomes in the late stage 4 are doughnut-shaped, that is, the central globule ofabout 13 Ilffi in diameter and the outer circle of about 17 Ilm; the former seems an accumulated body of many minute granules and the latter is a circular layer of cytoplasm
without any vacuoles and yolk droplets.
Stage 5:

Chorion formation stage (Fig.4A).

In this stage, the yolk is fully deposited, and' consequently the ellipsoid oocyte is
greatly enlarged.
As yolk deposition proceeds, the follicular epithelium becomes more thin and is more
expanded. The oocyte of this stage has numerous yolk globules, and the scarce protoplasmic
reticulum and periplasm.
The amoeboid germinal vesicle migrates from the center of the oocyte to the periphery inthis stage. The volume of the oocyte decreases during its migration, and finall-y only a few
nucleolar particles surrounded with nuclear substances are recognized at about the posterior
third of the ventral side of the oocyte where the maturation division takes place.
The mycetomes transform their shape from hemispheroid to spheroid; they are no longer
the aggregation of many granules at the earliest phase of its appearance but the solid ballwhich seems to be made of fibrous substances. Their surrounding cytoplasm is fused to theprotoplasmiC reticulum. The posterior mycetome migrates to the posterior pole of theoocyte and lies above the oosome, while the anterior mycetome is stationing near theanterior fourth of the oocyte. It is often observed that fragmental minute yolk droplets arepresent around these two mycetomes.
The terminal oocyte at the stage 5 is three times larger than those at the previous stage,
and chorion is formed.
Three to several minute discs, about 4 by 2 Ilm and strongly stained by haematoxylin,
appear near the posterior pole of the oocyte. Then they fuse with each other and form an
ooplasm which is measured about 20 Ilm in diameter.
The follicular epithelium of the terminal oocyte is shrunken, condensed, and forms a
corpus luteum in the pedicel after ovulation.
When the eggs are retained in the lateral oviducts and begin to develop, the terminal
oocytes cease to develop further; the yolk deposition and chorion formation becomeabortive, and then are absorbed by the follicular cells which become again tall and columnar(Fig. 6A). At last the oocytes are almost resorbed and only mycetomes are remained, which
may disappear later. These enlarged follicular cells contained transparent droplets form alarge corpus luteum-like structure situating between the ovariole and the calyx which is fully
expanded by the ovoviviparous eggs retaining in the lateral oviducts.

52Haga, K.

og

myt

oc
fe
pf

gv
nl0

if

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ypc
myt
ffe
myll'i'

gv

gv
fe

nl0

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yg

if

ex

Fig.

3. Oogenesis of B brevitubus. A. Structure of ovary. Scale: 50 IJ.m B. Germariumand oogenetic Stage 1.
C. Oogenetic Stage 2.
D. Oogenetic Stage 3.
E.
Oogenetic Stage 4. Scales for B-E : 10 IJ.mcx calyx,
fc follicular cell, fe follicular epithelium, gr germarium,. gv germinal
vesicle,if interfollicular tissue, myr mycetomic granule, myt mycetome, nlo nucleolus, og oogonium, oc primary oocyte, pf prefollicular cell, pi pedicel, tf terminal
filament,
tfn nucleus of terminal filament, vm vitelline membrane, vt vitellarium, yg
yolk globule, ypc yolk particle.

Oogenesis and Embryogenesis of Bactrothrips

53This structure might have a function to retard the oogenesis until these ovoviviparous eggs
are all oviposited or hatched out from their mother (Fig.6B).

Eggs
The eggs of B. brevitubus are laid perpendicularly on the substratum by adhering
substance secreted from the oviducts. Several to 125 eggs deposited are arranged tightly andadhered each other, and form a batch.
The egg is ovoid in shape. Its ventral side somewhat swells as shown in Figs. 4,5,and its
size ranges between 0.58-0.61 mm by 0.26-0.28 mm. The eggs become 0.64-0.66 mm by
0.29-0.31 mm in size during their development.
The chorion is thin, pale yellowish orange and elastic just after oViposition, but it changes
into brownish white and lacks elasticity about two hours later. Anterior third of the egg
surface is reticulated pentagonally and hexagon ally with ridges among these polygons which
are made of minute digital processes and porous grooves (Figs. 5CD). These surface structures are well developed in the anterior fifth of the egg. The posterior two thirds lack thereticulation and are smooth (Fig. 5AE). When hatching a part of the polygonal grooves iscracked at about anterior fifth of the egg.
The author failed to observe any micropylar structures in the eggs of B. brevitubus, andB. honoris as like as B. bullai (Bournier, 1966), while there is a distinct micropyle on theposterior third ventral side of H. verbasci eggs (Heming, 1979). In Bactrothrips, the spermatozoa may probalby pass into the egg through porous ridges near the anterior pole where
many pores penetrate the endochorion (Figs.5CD).
The chorion consists of the exochorion and endochorion. The former is brownish whiteand 1-2 pm thick, and has a rough surface in the anterior third but it is more thin andsmooth one in the posterior two-thirds. The latter is evenly about 2 J1ffi thick and paler,withthe smooth under surface without any pores.
Immediately below the endochorion there is a vitelline membrane (Fig. 4B) which isslightly stained blue by haematoxylin and has even thickness less than 1 J1ffi. There are seen
the thin periplasm of 1-5 pm in thickness, and the internal reticulum.
The female nucleus is found within the cytoplasmic island, about 30 by 14 pm, which isat the posterior third ventral side of the egg (Fig.4B).
The egg has a discoid oosome about 23 by 2-3 J1ffi, near the posterior pole (Fig. 7). It isclearly stained by haematoxylin and contains a few granules which are globular or ellipsoid,
1-2 pm, arranged in a row. They are homologous to those in Drosophila and holometabolous insects (Mahowald, 1972; etc.). Heming (1979) described the oosome ofthe eggs in H. verbasci for the first time.
As already mentioned, each of Bactrothrips eggs have always each two mycetomes (Figs.
7, 8). They are similar with each other in size and shape, globular, about 12-15 J1ffi indiameter, and porous like as made of fibrous substance, with indistinct double layers. They
are not well stained by eosin but slightly stained by haematoxylin. Bournier (1966) foundthe similar mycetomes in B. bullai eggs which are about 20 pm in diameter, and primarily
only single mycetome is situated at the posterior pole, but later it divides into 2 or 3, andthen they are enclosed into the newly formed mid-gut. His observation almost coincides
with the present ob sevation , however, the mycetomes of the Bactrothrips egg are found54

Haga, K.

4
tf

dep chypyl
ant myc
fe

rtr
yl
yp
ch
ant mycpl

mig gvpr

gv
post myc
rpo

post myc

ovp
po
pi

Fig.

4.

Grown oocyte and newly ovulated egg in B. brevitubus.
A. Oocyte of the oogenetic stage 5.
B. Newly ovulated egg.
Scales: 50 I1m
ant myc anterior mycetome, ch chorion,
dep ch depositing chorion,
fe follicularepithelium,
gv germinal vesicle,
if interfollicular tissue,
mig gv migrating germinalpi pedicel,
pi periplasm,
po oosome (pole plasm),
vesicle,ovp plug of ovariole,post myc posterior mycetome, pr protoplasm,
rpo rudimental granule of oosome, rtrchorion reticulation, yl lipid yolk, yp proteid yolk.

Oogenesis and Embryogenesis of Bactrothrips

55

5
E
Fig.

5.

F
Scanning electron micrographs of egg surface.
A-D . B. brevitubus.
A. Lateral view of egg, ventral side down. Scale: 50
p.m
B. Anterior half of egg, showing partial reticulation. Scale: 50 p.m C, D.
Porous structure of reticulation. Scales: 5 p.m
E - F.
B. honoris. E. Lateral view of egg, ventral side down. Scale: 50 p.m
F. Anterior portion of egg, showing reticulation weaker than that of B. brevitubus. Scale: 5 p.m

56

Haga, K.

6

if
fe
rbs
vac

fen

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fen

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Fig.

ovp

6. Resorption of oocyte in ovoviviparity in B. brevitubus.
A. Resorbing terminal oocyte.
Scale: 10 JJ.m
B. Process of resorption, diagrammatic.
bd blastoderm, ch chorion, edcx expanded calyx, fc follicular cell, fcn nucleus offollicular cell, if interfollicular tissue, mig gv migrating germinal vesicle, myt mycetome,
ovp plug of ovariole, ovv ovoviviparous embryo, pi pedicel, rbs resorbed substance,vac vacuole, yg yolk globule.

Oogenesis and Em bryogenesis of Bactrothrips

57

B

A

fe
gv --t-t~

pi

7
ch

Fig.

7.

Development of oosome in B. brevitubus.
A. Terminal oocyte, diagrammatic.
B.
Posterior portion of the terminal oocyte, showing precursor granules of theoosome.
Scale : 10 Jlm
C.
Posterior portion of the ovulated egg, showing position of the oosome.
Scale : 10 Jlm
ant myt anterior mycetome, ch chorion, fc follicular cell,fe follicular epithelium,
gv germinal vesicle,
if interfollicular tissue,
opg precursor granule of oosome,perperiplasm, pi pedicel,
po oosome (pole plasm). posy myt posterior mycetome, vm
vitelline membrane, yg yolk globule.

58

Haga, K.

invariably two and never divide.
In the living egg, two kinds of yolk globules (Fig. 4B), i. e., the lipid yolk and proteid
yolk may be recognizable. The former is transparent, less than 5 JJffi in diameter, and thelatter is about 1 to 16 /J.m. The lipid yolk, however, is almost all resolved during thetreatment of the preparation.

Developmental Stages of Embryo
Based on the external observation and the examination of serial sections, the embryonicdevelopment from its commencement to the hatching of B. brevitubus is divided into thefollowing 11 stages. Heming (1979) also divided the embryogenesis of H. verbasci into 11
stages similar to those of the psocopteran Liposce/is divergens (Go ss, 1952), but he sets 7
stages before katatrepsis while the present author gives 6 pre-revolution stages.
It is unable to time complete developmental stages accurately. In the most embryo logicalstudies, the time of oviposition is arbitrarily set the beginning of the embryonic development, however, in B. brevitubus the developing eggs are often stored in the oviducts andoviposited at various stages as observed by Heming (1979) in H. verbasci. In the present
study, the duration of each stages could be determined by an analysis of the movie films of
the living eggs.
Stage I

(00:00 - 08:00 hr) (Cleavage)

The author could not observe the process of fertilization. The fertilized nucleus divides
several times, synchronously at first but it becomes asynchronous. Cleavage nuclei arrive at
the egg periphery at the end of this stage.
Stage 11.

(08:00 - 18:00) (Ventral plate formation)

This stage is from the arrival of migrating nuclei at the periphery to 'the appearance of theventral plate. The egg is covered by the blastodermal cells, but they are coarse and thin near
the anterior pole of the egg. The boundary between the embryonic and the extraembryonicareas becomes somewhat clear. The ventral plate is formed in the former at the end of thisstage.
Stage Ill.

(I 8:00 - 26:00) (Invagination of Germ-band)In this stage the ventral plate invaginates into the yolk and the extraembryonic area
differentiates into the serosa. The amnion is also formed. The germ-band grows along thelongitudinal axis of the egg.
Stage N.

(26:00 - 36:00) (Early Pre-revolution )At the beginning of this stage the protocephalic lobes are formed. Rudiments of theantennae and gnathal appendages appear. The rudiment of labrum also appears between theantennae. In the elongating germ-band the first and second caudal fold may occur.

Oogenesis and Embryogenesis of Bactrothrips
Stage V.

59

(36:00 - 52:00) (Middle Pre-revolution)

The germ-band elongates further and becomes longest in this stage. Thoracic appendages
develop and the segmentation of the thorax and abdomen becomes distinct. Pleuropodia
appear on the first abdominal segment.
Stage VI.

(52:00 - 64:00) (Late Pre-revolution )The germ-band grows in width. The gnathal and thoracic appendages develop well. The
position of the labrum moves posteriorly, and that of the antennae move anteriorly. The
serosal cuticle is formed.
Stage VII.

(64:00 - 70:00) (Katatrepsis )Embryonic envelopes break at the point of their fusion. Serosal cells begin to contact
towards the anterior pole. The embryo is shortened with slight rotation, then it comes out
from the yolk and moves along the ventral surface of the egg towards the anterior pole. At
the end of this stage, the secondary dorsal organ is formed, and the provisional dorsal closure
is completed.
Stage VIII.

(70:00 - 80:00) (Early Post-revolution)

The pleuropodia develop and their secretion is occurred. Anterior and posterior ribbonsof the mid-gut epithelium elongate. Rectal papillae become distinct in the proctodaeum.
The secondary dorsal organ disappears at the end of this stage.
Stage IX.

(80:00 - 94:00) (Middle Post-revolution)

The gnathal appendages of the embryo collectively form the mouth-cone, in which a pairof maxillary stylets is formed. The right mandible degenerates while the left one begins toform stout stylet. The dorsal closure is almost completed and the mid-gut is formed at theend of this stage. The embryo grows and its head reaches the anterior end of the egg.
Stage X.

(94:00 - 110:00) (Late Post-revolution)

The left mandibular stylet and a pair of the maxillary stylets are chitinized. The compound eyes are formed and the larval integument and major setae begin to appear. The yolk
in the mid-gut is almost liquefied.
Stage XI.

(110:00 - 120:00) (Full-developed Embryo)

The head capsule is formed and hardened as well as pronotal plates, and the tube is sclerotized in this stage. The hypodermal pigmentation occurs under the tergites. The yolk isalmost completely consumed. No egg-teeth is formed. Just before hatching the embryo
begins expanding and retracting movement of its head and prothorax.

ant my=0-post myt~a~

=

~

~

hl

8
Fig.

8. Mycetomes behaviour during embryonic development in B. brevitubus, diagrammatic.
A. Position of two mycetomes. B. Ventral plate is formed. C. Invagination of
the germ-band begins.
D. Germ-band grows along the median egg axis.
E. Two mycetomes anastomose each other. F. Germ-band flexes dorsally.
G. Germ-band flexes again, mycetomes are separated from it. H. Appendages
grow before katatrepsis. I. After katatrepsis, mycetomes situate dorsally. J. Midgut is formed, mycetomes are enclosed in it.
ant myc anterior mycetome, gb germ-band, gc germ cell, hi head lobe, mg mid-gut,
post myt posterior mycetome, rat rudimentary antenna, sdo secondary dorsal organ, thl
thoracic appendage, vp ventral plate.

Oogenesis and Embryogenesis of Bactrothrips
A

61
0

enu

9
Fig.

9.

Migration and transformation of germinal vesicle at the oogenetic Stage 5. in B.
brevitubus.
A. - E.
Successive changes and migration of the germinal vesicle, yolk globule
deposition, transformation and migration of the mycetomes, formation of theoosome. (Chorion and vitelline membrane omitted). Diagrammatic.
F. Egg nucleus and polar bodies. Scale: 10 tIm
ant myt anterior mycetome, cyp cytoplasmic area around the egg nucleus, enu egg nucleus,
fe follicular epithelium, gv germinal vesicle, if interfollicular tissue, myt mycetome,
pb polar body, po oosome, yg yolk globule.

10

1st
2nd
cleavage cleavage

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o

synchronous0

asynchronousFig. 10. Cleavage in B. brevitubus, reconstruction from serial sections and diagrams ofcleavage directions. Bars show the location of cleavage center.
A. After 3rd cleavage (8-cell stage).
B. At 4th cleavage (11 energids).

62

Haga, K.

Maturation and Oeavage
When the eggs are oviposited, the phase of the maturation is different according to thetime that the eggs have spent in the oviduct. The youngest egg observed has two polar
bodies situating close to each other. Depends upon the observations on the oogenesis andthe above-mentioned results, it is assumed that the eggs at the ovulation (pushing out of thecompleted eggs from ovarioles to lateral oViducts) are at the metaphase of the first maturation division, and the second maturation division has already occurred while they werestaying in the lateral or common oviduct.
The polar bodies are observed in the cytoplasmic island adjacent to the egg pronucleus,
which are about 7 by 9 I1m. The author could not observe the process of the fusion of
nuclei, but studied the course of the first cleavage in two instances. In these cases thezygote locates at the posterior third of the egg longitudinal axis, and they are at the metaphase. The size of two nuclei with their surrounded cytoplasm are 26 by 20 Ilffi, and 28 by
20 I1m, respectively. In one case a nucleus has at least 12 chromosomes that are arranged on
the equatorial plane; only previously known chromosomal number in Tubulifera is n=14 in
H. statices (Risler and Kempter, 1961).
After the first cleavage, two energids are found at the posterior fifth and three-sevenths
along the longitudinal egg axis (Fig. 10).
The second cleavage occurs synchronously but its divisional plane is vertical to the firstcleavage. The distances between each pair of the daughter nuclei are shorter than that in
the first cleavage. In one instance the size of these four energids is 14-18 by 16-22 I1m.
The third cleavage occurs ·in the longitudinal direction of the egg, and nearly synchronous, but it is often observed that there are 6 or 7 energids in an egg. After the thirdcleavage, the energids are distributed randomly, and also the synchrony and orientation of
the cleavages become irregular and the uniformities is gradually lost.
When the number of energids increases to about 100, their peripheral migration begins.
In one instance (Table 1) in which containing about 97 energids (the intermediate stage
between 6th and 7th cleavages), they are seen to distribute unevenly in the egg, and a few
energids have a short cytoplasmic tail as if they are migrating towards the periphery (Fig.
lIB).
Two or three energids are seen in contact with both the anterior and posterior mycetomes
before the beginning of the energids migration. The cytoplasm of these energids fuses withthe cytoplasm around the mycetoms.
At the end of Stage I, the energids are most abundant near the posterior third of the egg,
and their number gradually decreases to the distal area where any energids cannot be found.
The energids reach the periphery of the egg probably at the 8th cleavage. The firstarrival of the energid is observed at the posterior fifth of the ventral side of the egg, not far
from the cleavage center. Prior to the first energid's arrival to the periphery, the energids
contacting with the posterior mycetome begin to move posteriorwards, and finally penetrate
into the oosome just below the mycetome, whereupon they will become the primordial germ
cells (Fig. 11 E).
.
The migrating energids have the cytoplasmic coating, about 5 I1m thick, a part of which isoften elongates as trail. When the energids attained to the periphery, they are measured
12-15 Ilffi in diameter. The periplasm at this stage'is only 5-10 Ilffi thick, but later it slightly
increases in thickness most probably due to the cytoplasm brought by arrived energids. At

Oogenesis and Embryogenesis of Bactrothrips

63

this time, however, certain parts of the egg surface still lack the periplasm (Fig. 11).
As an example of the 8th cleavage, about 140 energids are counted, and 70% of which
arrived at the egg periphery, but they are noticeably scanty near the anterior pole (Tables 2,
3).
The arrived cells repeatedly divide tangentially, and increase in number, whereas decrease in their nuclear size occurs. Some of them divide centripetally and their daughter
cells may become the secondary yolk cells.
In the eggs of 5 hours after oviposition, either the 7th cleavage (no energids at the periphery) or 8th cleavage (several energids at the periphery) are observed.

Blastoderm Formation
The cells at the egg surface have a large nucleus with scarce cytoplasm just after arrival.
According to the thin uncontinuing periplasm they are sparsely distributed until their
number increases more than about 1000. Only a few cells can be found near the anterior egg
pole in the 3059 cell-egg (Table 3). As the result of several mitoses, the size of the nuclei
in these cells decreases from about 15 Iffil to less than 5 Iffil in diameter. These cells transform into flattened fusiform, and cover the surface of the egg. They are extended about 20
J.Lm in diameter near the anterior egg pole, but those near the posterior pole are less than 10
Iffil. In succeeding stage the latter group of the cells increases in number, and the density
becomes higher than in the previous stage. In this way the egg attains the blastodermal
stage, but blastodermal cells is demarcated from each other in this stage. They arrange in alayer, but they are thick and cuboid in the posterior region of the egg while thin andflattened in the anterior region. The boundary of the thick blastoderm or embryonic area isdistinct.
When the blastoderm is completed, an egg contains about 2987 cells, about 65 of which(primary yolk cell) still remain in the yolk (Table 3). As the development proceeds, theprimary yolk cells increase in number, but the proportion of numbers of the blastoderm andprimary yolk cells is nearly constant; in one instance about 100 primary yolk cells are recognized among about 5000 cells, which indicates that the proportion of primary yolk cellis approximately 2% of entire cell number. They (6-10 J.Lm in size) are a little larger thanthe blastoderm cells (5-8 J.Lm), and are globular or ovoid with a thin cytoplasm, andrandomly distributed all over the yolk. Some primary yolk cells accompany with the
mycetomes, and their cytoplasm is projected into the yolk.
As mentioned before, two or three cells penetrate into the oosome at the cell migration
stage, and their number increases about 10 until the blastoderm is completed. They are theprimordial germ cells, and repeatedly divide there. Then they aggregate at the site between
the posterior pole and the posterior mycetome (Fig. 11).
As the cells in the embryonic area proliferate further, they increase in thickness. The
embryonic area develops to the ventral plate or embryonic primordium. It is disc-like andoccupies less than posterior one-third of the egg length (Fig. 12).
While the ventral plate formation, the number of the primordial germ cells increases, andreaches about 30 until the commencement of the invagination of the ventral plate. It takes
about 10 hours from the first arrival of the energids at the egg periphery to the commencement of the anatrepsis; this is about 18 hours after the initiation of the embryonic development in B. brevitubus.

64Haga, K.

Table 1.

Distribution of energids of an about 97-cell egg (Stage I) in B. brevitubus.
(Anteroposterior locations).

SECTION NUMBER FROM ANTERIOR POLE

DISTRIBUTION
OF NUCLEINUMBER OF NUCLEIIN CENTRAL YOLK0

60

7 - 12

0

13

- 18

2

19

- 24

8

25

- 30

8

31 - 36

10

37

- 42

9

43

- 48

10

49

- 54

12

55 - 6014

61 - 66

11

67

- 72

5

73

- 78

7

79

- 84

1

85

- 90

0

1 -

(Anterior pole)00(Posterior pole)

97

Oogenesis and Embryogenesis of Bactrothrips

Table 2. Distribution of energids of an about 14Q-cel1 egg (Stage 11) inB. brevitubus.

o ... on periphery,
SECTION NUMBER FROM ANTERIOR POLE

• ... total.

ON PER IPHERYIN CENTRAL YOLK

TOTAL

0

1 - 6

0

0

0

7 - 120

1

1

13 - 180

3

3

19 - 240

3

3

25 - 3004

431 - 361

5

6

37 - 420

66

43 - 48

5

2

7

49 -

54

7

2

9

55 - 6080

8

61 - 6616

0

16

67 - 7211

2

13

73 - 7815

0

15

79 - 8418

0

18

85 - 9014

3

17

91 - 96

1

7

8

- 102

.2

4

6

98

42

140

97

DISTRIBUTION
OF NUCLEINUMBER OF NUCLEI(Anterior pole)(Posteaior pole)65

Haga, K.

66

Table 3. Distrubution of cells in a blastoderm (about 3059 cells of Stage 11) in
B. brevitubus.

o . . . on periphery,• ... total.
Numerals in parenthese mean number of germ cells.

SECTION NUMBER FROM ANTERIOR POLE

1 -NUMBER OF NUCLEION PERIPHERYIN CENTRAL YOLKTOTALDISTRIBUTION
OF NUCLEI(Anterior pole)

5

30

0

30

6 - 1040

141

11 - 1567

0

67

16 - 2076

278

21 - 25

110

2

112

26 - 30

127

2

129

31 - 35

173

4

177

36 - 40

142

!l

150

41 - 45

178

5

183

46 - 50

203

5

208

51 - 55

189

10

199

56 - 60

221

7

228

61 - 65

233

7

240

66 - 70

239

3

242

71 - 75

242

5

247

76 - 80

236

3

239

81 - 85

209

0

209

86 - 90161(3) + 1

165

91 - 95

111(4) + 0115

2987(7) + 653059

Oogenesis and Embryogenesis of Bactrothrips \

67

II
mig

c

per
...:: .

'\ (arr eng.",... ,-,',,::::':',:::~>:':C'"''..........

F
..
~
~~

"

~.'

v.

"

'.'

Fig. 11. Blastoderm formation in B. brevitubus. Scales: 10 p.m
A. Energid division.
B. Migration of energids. C. Blastoderm near anterior
pole.
D. Blastoderm near posterior pole.
E. Posterior portion of an egg in
the blastoderm stage. F. Yolk cells.
arr eng energid arrived to the periphery, bdc blastodermal cell, gc germ cell, mig eng
migrating energid, per periplasm, post myt posterior mycetome, yc yolk cell, yg yolk
globule.

Q\

co

::z:

~
.P'

po:

Fig. 12. Germ-band formation in B. brevitu bus.
A. Blastoderm, lateral view.
B. Ventral plate formation, ventral view.
C. Beginning of invagination of ventral plate, lateral view and ventral view (C').
D. Early stage of germ-band formation, lateral view and ventral view (D').
E. Proceeded stage of germ-band formation, lateral view and ventral view (E').
am amnion, amc amniotic cavity, eba embryonic area, exa extraembryonic area,
germ-band, im mouth of invagination, ser serosa, vp ventral plate.

gb

Oogenesis and Embryogenesis of Bactrothrips

69

Germ-Band Formation
Before the biginning of the ventral plate invagination, the difference of the cell density
between embryonic and extraembryonic areas becomes apparently distinguishable asmentioned above. The orifice of the invagination, at first, appears as a short transverse slit
near the posterior end of the ventral plate, and the primordial germ cells with the posterior
mycetome are situated inside near the mouth. Soon after this slit changes in shape to inverted letter "V".
It seems that the direction of the invagination is first horizontal, then changes perpendicularly and finally invaginating end of ventral plates points anteriorwards and it elongatesalong the longitudinal egg axis; this shift in the direction of invaginating ventral plate is dueto the shifting of the orifice of the invagination to the posterior one-sixth of the egg (Fig.
12).
At this stage the germ-band is a flattened monocellular blind tube of the cells which has anarrow lumen, and its dorsal side is the embryoniC primordium, and the ventral side is the
rudimentary amnion, and the lumen later becomes the amniotic cavity (Figs. 12, 14). The
cells of the caudal end of the germ-band increase in number by mitoses.
As above-mentioned, the posterior mycetome keeps in contact with the caudal end of theinvaginating ventral plate, and when the mycetome reaches the anterior mycetome, the two
mycetomes fuse each other (Fig. SE). These mycetomes separate from the germ-band andare moved by yolk flows, and finally arrive at the anterior one-fourth of the egg on the dorsalside (Fig. SG). In the course of the anatrepsis the primordial germ cells attach again to thecaudal end of the germ-band. As the posterior end of the developing germ-band reaches atthe position of the anterior mycetome, the germband flexes dorsally and curves again posteriorly, and once more flexes dorsad of the egg. Thus the germ-band is formed as doubleflexed S-form as seen from the lateral view and keeps the form until the katatrepsis.
It is about 70 minutes from the beginning of the invagination of the ventral plate to thearrival of the caudal end of the germ-band to the anterior mycetome, and it needs further
about 60 minutes for the double-flexed germ-band is formed.
At about 30 hours after the commencement of the embryonic development (about 20
hours after the beginning of the invagination of the germ-band), the germ-band of B. brevitubus is strikingly elongated. When the double-flexed germ-band becomes longest it isapproximately 1.7 times as long as the egg length.
A flow of yolk globules may be observed at the time of germ-band formation using timelapse microphotography. This yolk flow first occurs along the longitudinal egg axis, fromposterior to anterior, and then the flow is recurrented along the egg periphery from anterior
to posterior. Its velosity is higher along the axis than that along the periphery (Fig. 13B).
A pair of cephalic lobes develops during the invagination of the germ-band. At theoutset, they are flattened cylindroid as like the rudimental gnathal, thoracic and abdominal
regions. As the development proceeds, the germ-band transforms into V-shaped, then later
V-shaped in cross view, and is extended, although its thickness decreased. As alreadymentioned, in the protocephalon and protocorm the rudimentary amnion is a thick cellular
layer, but now it becomes very thin.

70

Haga, K.

110'

120·

130'

80'

40 '

B

Fig. 13.

Development of germ-band in B. honoris. (Reconstructed from 16 mm movie)
A. Time lapse of the germ-band growth. An arrow shows a migration of orificeof the germ-band. A circle indicates the position of the anterior mycetome.
B. Yolk flow convection during the germ-band growth.

71

Oogenesis and Em bryogenesis of Bactrothrips'

14

ile

epm
/

/

r------

/

/

ame

I

/

/

/

/

il

/

am

I

- .-/

/

Fig. 14. Inner layer formation in B. brevitubus.
Serial cross sections of a Stage III embryo.
am amnion,
amc amniotic cavity,
inner layer, He inner layer cell.

epm embryonic primordium,gc germ cell,

il

~

c

B

A

'-I

D

F

E

15

~

~

,t

1~

if

!it .{!
Ii
~

48

G

H

J

L

K

sec

=

ser

.P'

dll
po:

Fig. 15. Embryonic stages in B. brevitubus. (Chorion omitted, diagrammatic).
A. Stage I (cleavage),
B. Stage 11 (blastoderm), C. Stage Ill, D. StageIll',
E. Stage IV,
F. Stage V, . G. Stage VI, H. Stage VII (katatrepsis),I. Stage VIII, J. Stage IX, K. Stage X, L. Stage XI (prolarva).
am amnion,
pdc provisional dorsal closure,
cuticle, ser serosa.

sdo secondary dorsal organ,

sec serosal

Oogenesis and Embryogenesis of Bactrothrips

73

Inner Layer Formation
The inner layer formation begins as early as the caudal end of the germ-band reaches
near the egg center. At the gnathal region, the cells of the dorsomedian part proliferate andform a row of irregularly arranged cells which are very few at the initiation. Then the formation of the inner layer proceeds posterior- and anteriorwards from here. In cross section,
the thoracic region represents a V-shape while it is oval in the abdominal region as mentioned above. In the former, the inner layer is formed on the dorsomedian part with a slightconcave groove (Fig. 14), and it is also formed in the cephalic region.
In B. brevitubus the inner layer formation is of the proliferating type. It seems that thisproliferating type is primitive among the method of the inner layer formation employed by
the insects.

External Changes of EmbryoPre-revolution StageIn the middle Stage III when the caudal end of the germ-band attains near the anterior
mycetome, the first sign of the metamerism can be seen in the gnathal region as slightswellings. Some other swellings appear followingly also in the thoracic region, but thesegmentation is rather incomplete. In the same stage, the inner layer of the gnathal region is
also obscurely segmented.
The mandibular, 1st maxillary and 2nd maxillary segments, three thoracic and 1st
abdominal segments become distinct as early as at the 28-hour stage.
On the other hand, a pair of the labral rudiments or mere swellings contacting each otherappears on the posterior cephalic region
At about 30 hours later (Stage IV), a part of the antennal rudiments adjacent to thelabral rudiments begins to project and develops greatly. They gradually migrate anteriorwards, while the labral rudiments move posteriorwards and later fuse into an appendage.
In about 36-hour stage (late Stage IV), the rudimental gnathal and thoracic appendages
appear simultaneously, but those of the intercalary segment are not recognizable.
In the middle Stage V, the appendages are more obvious; both the antennal and maxillary rudiments elongate and begin to metamerize near the base.
The proctodaeal invagnination is occurred on the ventral side of the enlarged distalsegment of the germ-band, i. e., the telson, in the late Stage V (about 44 hours). The
stomodaeal invagination also occurs at this stage just behind the labrum.
The abdominal region has 11 segments, but the 11 th segment may only be recognized by
the constricted inner layer of the segment in this stage, henceforth it becomes indistinct, andfuses with the inner layer of the 10th segment.
The serosal cuticle appears outside of the serosa in the Stage V; it begins to form in thelate Stage IV.
As the appendages develop, the germ-band gradually enlarged not only in length but also
in width and consequently the spaces between the flexures of the germ-band become
narrower. The telson containing the proctodaeal rudiment and the malpighian tubule
rudiments is faced to the 6th to 9th abdominal segments with a narrow space between them

~

....

::I:

ree

~'"

16

thl
Fig. 16. Katatrepsis in B. brevitubus, diagrammatic, chorion omitted.
am amnion,
ant antenna, cf caudal flexure, fee fusion of embryonic envelopes, pdc
ree rupture of embryonic envelopes,
sdo secondary dorsal
provisional dorsal closure,organ, sec serosal cuticle, sen serosal nucleus, ser serosa, thl thoracic leg.

~

Oogenesis and Embryogenesis of Bactrothrips

75

which is further completely closed (Fig. 28).
The primordial germ-cells that have been attached to the caudal end are moved anteriorwards by the colsing of the space of the flexed part. Thenceforth they are anastomosed with
the inner layers of the 6th and 7th abdominal segments.
The cephalic lobes become a rugged shape until the initiation of the katatrepsis by the
rapid growth of the developing optic lobes. In this period the antennal rudiments elongate
almost reaching the mandibular ones.
In the Stage VI, just before katatrepsis, the antennal rudiments are metamerized into 3
segments as the thoracic appendages. The apices of the 2nd maxillary appendages are incompletely forked, while the 1st maxillary ones do not divide.

Katatrepsis
In Stage VII (64 hr after oviposition), the first indication of kat at repsis movement occurs
in thoracic and abdominal regions of the embryo. This is contraction and relaxation of theseregions which occur along the longitudinal axis of the embryo. This reciprocal movement of
the embryonic regions extends to the cephalic region at about three hours later, and theinterval of the movement becomes shorter and the amplitude of the movement becomeslarger. At 67-hour stage, the embryonic envelopes are ruptured at the cephalic region of theembryo by a pulsative movement (Fig. 16B). The rupture immediately expands and theenvelopes are rapidly hauled to the anterior pole (Fie. 16C).
Thus the embryonic head which occupies posterior half of the egg begins to moveanteriorwards along the ventral side of the egg. Soon later, the embryo completes its revolutionary movement, and the dorsal side of the yolk is enveloped by the amnion (Fig. 16F).
The contracted serosal cells locating anterior to the embryonic head form a cap-like large,
hemispherical secondary dorsal organ with diameter of about 150 Mm. Formation of a
strand from the serosal cells for pulling the embryo as described in Tanypteryx (Odonata;Ando, 1962) was not observed.
In the course of the katarepsis, the embryo moves not only anteriorly, but also rotates
approximately 45 degrees around the longitudinal egg axis before it undergoes further
rotation within the sagittal plane of the egg. This rotation is more apparent in the cephalicregion than in the abdomen at early katatrepsis, then it rotates again the counter direction(Fig. 16FG). In one instance, this phase of katatrepsis took about 18 minutes.
Just after katatrepsis the embryo occupies three-fourths of the egg ventral side. It can berecognized at least three constricted parts on the antennal rudiments. The gnathal segments
are remarkably transformed during the katatrepsis. Firstly, the position of labrum migrates
posteriorly and labrum itself is seen to elongates, and the labium projects ventrally; these
two gnathal appendages soon contact with each other to form a short rostrum. Secondly, apair of maxillary rudiments and the left mandibular rudiment begin to form the longsclerotized stylets which are completed in the Stage X; the right mandibular rudiment, on
the other hand, begins to degenerate.

76

Haga, K.

17

E

F

i1

nb

D

nm

99 1

am

Fig. 17. Ventral nerve cord formation in B. brevitubus, cross view.
A-G. Successive development.
am amnion, ect ectoderm, epm embryonic primordium, ggc preganglionic cell,
ganglion, il inner layer, med median cord, np neurilemma.

ggl

Oogenesis and Embryogenesis of Bactrothrips

77

Post-revolution Stage
Within 2 hours after katatrepsis (72 hours stage), the secondary dorsal organ becomes
obscure during the definitive dorsal closure, and degenerates in the yolk by 80 hours (Stage
VIII to IX). The dorsal closure completes about 10 hours after katatrepsis (Stage IX).
At the early Stage VIII, the anterior and posterior mid-gut epithelia from the stomodaeum and the proctodaeum envelop the yolk. Soon after, the developing embryo fills up
the space in the egg.
In the Stage IX, paired maxillary stylets appear deep in the embryonic head, but they are
not yet chitinized, and lie from near the compound eyes to the apex of the rostrum showing V-letter. A mandibular stylet is also formed at the left side of head, which is thicker
but shorter than the maxillary ones in this stage.
The compound eyes, each consisted of only 2 ommatidia, have become visible because ofdark red pigments deposited in Stage X. Ocelli are not differentiated in the embryonicstages.
In Stage X (about 100 hr after oviposition), the setae are formed and the peculiar structures of the pretarsus of the thoracic legs, i. e., the unguis and sense hairs are differentiated.
Integuments of the thorax and abdomen as well as the head capsule are rapidly formed, inwhich the maxillary and mandibular stylets are chitinized; the latter is stouter than theformer.
In the Stage IX, three longitudinal rows of red hypodermal pigments appear in the dorsal
parts of the thoracic and abdominal segments. In addition, the head, prothorax and 8th10th abdominal segments are partly sclerotized and turn greyish. In this stage the full-grownembryo shows the pulsative movement. In the embryo of B. brevitubus, the eggtooth is notdifferentiated, but the chorion is cracked by the movement along the deep reticulations
from where the first instar larva hatches out.

Organogenesis
Nervous system
A. Ventral Nerve Cord
Ventral nerve cord formation occurs in the Stage VI (28-hr). First the shallow neuralgroove is found in the gnathal region, and soon later, it extends into the thoracic region.
In this stage, the germ-band is formed by evenly arranged columnar cells, but this sequenceof the cells becomes lost near the groove (Fig. 17).
The first appearance of the neuroblasts can be seen at the Stage V (about 40 hr) in thegnathal region. The neuroblasts are 9-11 J.1.m in long diameter, larger than the columnar
epithelial cells which are 4-7 J.1.m; size of the neuroblasts during mitosis exceeds more than
12 J.1.m. Usually it can be observed up to 5 neuroblasts in each side of the germ-band in the
cross section. They divide into two unequal-sized daughter cells, a preganglionic cell and a
new neuroblast, respectively.
After the successive division of the neuroblasts the ganglionic cells are accumulated andform a cone-like pile.
In 50 hr embryo (Stage V-VI), the number of the preganglionic cells increases greatly,

"co

18

B

A

c

E

D

br

proct

-

-

::t:

~
J>'
~

hi
stom

Fig. 18. Concentration of ventral nerve cord in B. brevitubus, diagrammatic.
A. Stage VI, B. Stage VIII, C. Stage IX, D. Stage X, E. Stage XI.
br brain,hi head lobe,
mg mid-gut,
proct proctodaeum,
sdo secondary dorsalorgan, sog suboesophageal ganglion, stom stomodaeum, vnc ventral nerve cord.

Oogenesis and Em bryogenesis of Bactrothrips

A

C

79

E

dc

tc
at
atco

D

st~

Fig. 19. Brain formation in B. honoris.
A. stage IV, cross section,
B. Stage V, sagittal section, C. Stage VI, horizontal section, D. Stage IX, horizontal section, E, Stage XI, sagittal section.
am amnion,
at antenna, atco antennal coelom, atn antennal nerve, br brain, cl
cephalic lobe, dc deutocerebrum, epm embryonic primordium, frg frontal ganglion,
il inner layer, 11 -3 lobus 1 - lobus 3 of protocerebrum, 1r labrum, 1rco labral coelom,
mg mid-gut, nb neuroblast, pcl protocephalic lobe, pgc preganglionic cell, pc pro tocerebrum, ram rudimentary amnion, stom stomodaeum, sog suboesophageal ganglion,
tc tritocerebrum, thg thoracic ganglion.

E

co
o

C

\8."'. '·. '•.·;

0{

cry

am

':-:"'::':.:.:;

pc

cor

,,' . . fv:\,.~
:

Q,~/
prf

~
m

o

sto~'-- ____ prf

cryre,,~;<~,'fIe \',.

-~;;.;;.,.,.;}.');,I;'7-----ory

B~~
Fig. 20. Development of ommatidia in B. honoris.
A. Stage VI, horizontal section.
B. Stage VIII, horiz. s.
C. Stage IX, horiz. s.
D. Stage X, horiz. s.
E. Stage XI, sagittal section.
am amnion,
at antenna,cor cornegean cell, cry crystalline, cryo crystalline cone,dc deutocerebrum,opt optic plate, pc protocerebrum prf postretinal fiber,
ret
retinal cell, sem Semper's cell, ser serosa.

prf

::Ii

I»

~

~

20

Oogenesis and Embryogenesis of Bactrothrips

81

in one instance, their number counted in the gnathal segments was up to 14, that in thethoracic segments was 16 and that in the 8th abdominal segment was 8, respectively. Thenfibrous substances appear in the apical region of the preganglionic cell cones. They join witheach other, thus forming a neuropile which is not stained by haematoxylin. The neuropile
is formed at the first in the gnathal region, then succeeded in the thorax and later in theabdomen of the embryo.
The neuroblasts, preganglionic cells and neuropile are observed in each abdominal segment from the 1st to 10th. By Bournier's (1966) illustration, 9 abdominal ganglia can berecognized in C. bullai.
In the early stage of Stage VI, a pair of ganglia is formed within each segment, and at thesame time, ganglionic commissures and connectives are formed. They are formed at first in
the gnathal region and later followed by the thoracic and abdominal regions.
At the bottom of the neural groove in the thoracic and abdominal segments there areirregularly arranged cells including large ones that have the same affinity to haematoxylin asneuroblasts. They often divide and form the cord thick in the interganglionic areas but
thinner in the ganglionic areas, but do not produce neuropile-like fibers.
It seems that the neurilemma is formed by a part of the ganglionic cells situated at. thedorsalmost of the ganglion which is extremely thinned and expanded into a membrane.
As a consequence each ganglion is completed and all connectives develop from thepremandibular segment to the 10th abdominal segment. Thus the ventral nerve cord formed
at 60 hr in the late pre-revolution stage (Stage VI) consists of 16 ganglia. However, thenumber of the ganglia may not be correctly counted at later stages because the ventral nerve
cord begins to condense immediately after their completion.
The concentration of the ganglia commences in the gnathal segments. Their ganglia aregathered through katatrepsis (Stage VII), and finally form the sub oesophageal ganglion at
the late Stage VIII (80-hr). The condensation of the abdominal ganglia, on the other hand,
begins after katatrepsis. Condensation of the ventral nerve cord in the abdomen first occurs
at the extreme caudal end and then extends cephalad; ventral nerve cord becomes thick
while it shortens. It can be counted 10 abdominal ganglia in the Stage VI embryo, but inthe late Stage IX they consist of only 6 ganglia. Furthermore, this condensation becomes
more significant up to the late Stage X, by which time these abdominal ganglia lost allconnectives and transform into a short, thick, spindle-like synganglion. The ganglion locatesin the metathoracic segment, not in the abdomen.
Three thoracic ganglia also condense, and a pair of connectives between prothoracic andmesothoracic ganglia is noticeably shortened. Another pair of connectives between mesothoracic and metathoracic ganglia is also shortened, but does not disappear. The anterior
half of these condensed ganglia contacts with the suboesophageal ganglion, and the rest
nearly fuses to form the spindle-shaped abdominal synganglion.
The suboesophageal, pro-, meso-, metathoracic and abdominal ganglia have two to several
number of neurosecretory cells. They are larger than the ganglionic cells with a few chromatins and relatively large nucleolus.
In the full grown embryo, the ventral nerve cord consists of two ganglionic blocks, thatis, the suboesophageal ganglion with the prothoracic and mesothoracic ganglia, and themetathoracic ganglion and abdominal synganglion with thin nerve cord elongating into theventral part of the abdomen. These two blocks are contained in the thoracic region of theembryo, as in the adult.

A

"""\r

c

E

00
t.;

hcg

br
nsc

ccd~

rc

,-:/V<!J.(:flY

stom

pj

stom
sog

.'

hcg

... _................. .

sog

nsc

stom

o

br

=

ccd

dll

,po

p;:
sog

stom
cal

nsc

stom

"'~

21
mge

mg

Fig. 21. Development of stomatogastric nervous system in B. brevitubus.
A. Stage VI, cross section.
B. Stage VIII, cross s.
C. Stage IX, cross s.
D. Stage X, cross s. E. Stage IX, sagittal s.
br brain,cal corpus alia turn-like gland,cav cardiac valve, ccd corpus cardiacum-likegland,
cpj cytoplasmic projection,
hcg hypo cere bral ganglion,
mg mid-gut,
mge
mid-gut epithelium,
nsc neurosecretory cell,rcn recurrent nerve,
rsg rudiment of
stomatogastric nerve,
sg stomatogastric nerve,
sog suboesophageal ganglion,stom
stomodaeum.

Oogenesis and Embryogenesis of Bactrothrips
B.

83

Brain

As already explained, the protocephalic lobes are begun to form at the Stage Ill, and aresimilarly thick as the protocorm. However, no histological differentiation of the protocephalic lobes is observed in this stage.
In the following stage, the neuroblasts also occur in the protocephalic lobes which aresingle- or double-layered and accompanied with a small amount of the inner layer. The
neuroblasts may be found in the region along margins of the lobes (Fig. 19D), and thepreganglionic cells are arranged centripetally upon them.
In the Stage V, each protocephalic lobe is slightly constricted into 3 parts. The lateralmost of them somewhat thickens and forms an optic lobe in the middle Stage VI. The
deutocerebral rudiment is formed posterior of the optic lobe rudiment. Neuroblasts of
the rudimental protocerebrum and deutocerebrum actively divide and produce a lot ofganglionic cells. Their volumes rapidly increases after katatrepsis, and the neuropile develops in them.
In the late Stage VIII, thickened protocerebral lobes are in contact with each other, andpaired intercalary ganglia migrate towards the head region. They finally situate both sidesof the frontal ganglion and form a tritocerebrum in the Stage IX, which is much smaller
than the protocerebrum and deutocerebrum.
Though the head region of the embryo elongates, the protocerebrum locates its dorsal
and frontal sides while the deutocerebrum only can be seen near the stomodaeum.
In the grown embryo of B. brevitubus, the compound eyes develop at the both sides of
the head capsule near its apex. The optic plate differentiates from the optic lobe in theStage VI, just before katatrepsis. It is delaminated from the lobe and composed of single
or partly double-layered columnar cells. After katatrepsis the optic plate joins the optic
lobe with the postretinal fiber. Then Semper's cells and retinal cells differentiate in the
optic plate. A crystalline cone is formed as a hyaline vacuole by 4 Semper's cells which areclose together. A compound eye of B. brevitubus has only two ommatidia in the first larvalstage. Two sets of the 4 Semper's cells can be observed on each side of the embryonic head(Fig. 20). In the Stage X, the crystalline cones are nearly completed and brownish dark red
pigments are formed in each ommatidial rudiment. The corneageous cells are not distinct
but the cornea is formed just before hatching.

C.

Stomatogastric Nervous System

In the Stage V and VI, as the developing stomodaeum is prolonged, few neuroblasts
develop in its thickened dorsal wall, but it is difficult to recognize their daughter cells
because size and form of these daughter cells are very similar to the stomodaeal wall cells.
The elongate cell mass forms a dorsal ridge on the stomodaeum, and the mass is occupied
by a round portion made of neurofibrous substances surrounded by coarsely arranged cells
which are not separated from the stomodaeal wall.
The stomatogastric nerve of B. brevitubus is derived from the dorsal wall of the stomodaeum in the Stage VIII.
In the 'next stage, its anterior portion largely develops to form the frontal ganglion while
the posterior portion forms a hypocerebral ganglion, and the rest develops into the recurrent

84

Haga, K.

A

1 urn
mern

G

1 urn

22

Fig. 22.

st

1 urn

I

Ectodermal invaginations in B. brevitubus.
A. Stage VIII, sagittal section.
B. Stage X, corpus allatum-like gland.
C. Stage X, terminal portion of dorsal labial gland and accessory organ.
D. Stage X, pro thoracic gland-like structure.
E. Stage XI, showing position of glands.
F. Stage X, mandibular gland.
G. Stage IX, dorsal labial gland.
H. Stage IX, ventral labial gland.
Scales: for C, D 5 J.J.m, for B, F, G, H, 10 J.J.m
amge anterior mid-gut epithelium, acg accessory organ of dorsal labial gland, at antenna,br brain, cal corpus allatum-like gland, duc duct of gland, dIg dorsal labial gland, lig
ligament,
lr labrum, lum lumen, mg mid-gut, mdg mandibular gland, mem membranous structure,
pvd provisional dorsal closure,
sdo secondary dorsal organ,
sog
suboesophageal ganglion,
stom stomodaeum, tet tentorium, tgs prothoracic gland-likestructure,th 1_ 2 thoracic leg,tr trachea, vcn vacuolar cytoplasm, vlg ventral labial
gland, yg yolk globule.

Oogenesis and Embryogenesis of Bactrothrips

85

nerve.
At the lateral sides of the hypocerebral ganglion, a pair of tiny glandular cell groups isformed in the Stage X. These may be the rudiments of the corpus cardiacum and the corpus
allatum which anastomose each other (Fig. 21).
Some fibrous cytoplasmic projections extending into the epipharynx from the anteriorwall of the stomodaeum are observed after formation of the frontal ganglion.

Ectodermal Invagination
Several ectodermal invaginations in the gnathal and thoracic regions of the germ-band
may be observed in the pre-revolution stage. They are the tentoria, mandibular and labial
glands, corpora allata and a gland in mesothorax.
A pair of tentorial invaginations appears in the ventrolateral sides of labral rudiments at
the late Stage IV, but it does not develop deeply. Although position of the labral rudiments
moves posteriorly to form a mouth-cone, the invaginations of tentoria remain their original
positions and their shallow appearance hardly changes. These tentorial invaginations make apair of pits on the larval and adult head capsule, but these positions somewhat move asymmetrically according to the asymmetric development of the mouth-parts, as occurred in H.
verbasci (Heming, 1980). In B. brevitubus only the anterior arms of the tentoria develop,
while in the adult head of primitive thrips, Aeo[othrips fasciatus, the posterior tentorial arms
also develop (Mickoleit, 1963).
As already stated, a pair of mandibular rudiments is formed, and the size of right rudiment becomes gradually smaller than the left through katatrepsis. In the Stage VI, however,
the invaginations appear in the ventrolateral sides of the mandibular segment, the left sideof which forms a stylet-forming cell mass and the right one transforms into a tubular glandsituated in the ventral right side of the head capsule in the Stage X. The tubular nature andcell size of the gland are similar to the dorsal labial gland, but the secreting duct cannot be
observed.
Peterson (1915) observed the similar unpaired structure in Heliothrips femoralis (Terebrantia) adult head and called it the head gland. Later, Sharga (1933) also described an
unpaired salivary gland near the mouthparts in He. haemorrhoidalis. Probably they are thesame structure with the gland derived from the mandibular invagination in B. brevitubus.
In the labial segment, two pairs of glands invaginate in the late Stage IV. One of themelongates along the stomodaeum and finally locates dorsolaterally in the thoracic andabdominal segments. When the pair of glands completely develops, the glands reach theabdominal segment 4 or 5 at Stage XI. They are the dorsal labial gland (long salivary gland).
Most part of the gland is a simple slender tube made of a single layer of the vacuolate cells
surrounding a narrow lumen, however, the anterior end of the tube reaching the cephalicganglion becomes enlarged considerably and irregularly deforms with a wider space of thelumen.
There is a proliferating cell mass covering the terminal part of the tube. It looks like as a
glandular organ by having rich cytoplasm and a short duct opened into the swollen part ofthe dorsal labial gland. It is very likely that this cell mass is an accessory organ of the dorsal
labial gland.
Another labial invagination is a pair of short and thick ventral labial glands. It is quite

23

D

co

am

~

th

rpp

vnc

res

pp

nb

f,p
thl

=

:l

c

J»

~

sp

9

Fig. 23.

Development of pleuropodia in B. brevitubus.
A. Stage IV, B. Stage V, C. Stage VI, D. Stage VIII,

E. Stage IX.

am amnion, dpp degenerating pleuropodium, ect ectoderm, edch endochorion, exch
exochorion, il inner layer, mes mesoderm, oec oenocyte, pp pleuropodium, proct
rpp rudimental pleuropodium,res reservoir of pleuropodium,proctodaeum,secserosal cuticle, spp secretion ofpleuropodium, vnc ventral nerve cord.

Oogenesis and Embryogenesis of Bactrothrips i87different in structure to the dorsal labial glands. The ventral labial gland is only a cell mass
made of 10-15 cells at the beginning, but it obviously develops in Stage IX. Its cells grow up
to 15 fJIfl in diameter in which vacuolate secreting substances are stored, and are arranged so
as to form single cell layer around a narrow lumen. These vacuoles are basophil and wellstained but young ones are not stained. The ventral labial glands gradually move towards inthe mesothorax and the position of them is finally fixed on the ventral sides of the suboesophageal ganglion. A fine duct threads to the buccal cavity near the hypopharynx.
Another pair of glandular organs can be found in embryos of the post-revolution stage. It
is a small oval body consisting of a few large cells and situates inside of the mesothoracic
stigma near the base of coxa of the mesothoracic leg. Though it is not in the pro thorax, it isvery.likely that this cell mass is the prothoracic gland rudiment. However, its origin and fate
are still unknown.

Pleuropodium
The embryos of B. brevitubus have a pair of pleuropodia on their 1st abdominal segments. The first sign of the pleuropodium formation appears in the late Stage IV, which is aglomerate mass of a few cells separating from surrounding ectoderm in the ventrolateral sidesof the segment. In the Stage V, the pleuropodial cells develop columnar and ventrally project their cytoplasm from the embryonic body wall.
In the Stage VI, the pleuropodia develop further, and their basal parts sink into the mesodermal layer, whereas the apical parts elongate and become tongue-shaped. This tongueshaped apical part ruptures in the Stage IX.
The secretion from the pleuropadia is released into the space around the embryo. Afterthe discharge of the secretion the pleuropodia become withered and degenerate. In the nextstage, their vestiges are only observed among the oenocytes which are formed in the Stage VI
and develop'in Stage VIII and IX. The secreting substances are more thinly diffused, and thevestiges become unrecognizable.
The pleuropodia of Bactrothrips, therefore, are of an invaginated type as those of
Odonata (Ando, 1953).
In general, the pleuropodia are so conspicuous as an embryonic organ that they are observed in many insect orders. The best known function of the pleuropodia is the secretion of
the hatching enzyme in the American grasshopper, Melanoplus differentialis (Slifer, 1937).
However, the pleuropodia in the embryos of Odonata and B. brevitubus are seen to degenerate by the time of hatching. Bournier (1966) observed that the pleuropodia of C. buffaibegin to degenerate just after katatrepsis. He suggested that this organ secretes an enzyme
which contributes rupture of the embryonic membranes and acts as the trigger inducing
katatrepsis. In B. brevitubus and B. honoris, however, the secretion lasts through katatrepsis
until the Stage IX.
Since the secreted substances from the pleuropodia are distributed along the inner surfaceof the chorion, it seems that the chorion is affected by them, but the timing of the secretionis too early to change the nature of the chorion and thus consequently conributes hatchingof the larvae (Fig. 23).

ab 3
ab 2

24

\

co
co

0-- u g c

ab 1
thl

,.
f:

dlg

" ',:",~,

r.~·

:.~.

th2

c

th3

I

,

~

.::.!;

t;·:

~amg

B
::I:

:
!"

rp

~

A

1r

gor

o

E

Fig. 24. Gonad formation in B. brevitubus.
A-B-C.
Stage VI, appendages omitted, diagrammatic, showing enclosing of germ
cells.
D. Stage VIII, sagittal section.
E. Stage X, sagittal section.
ab 1-1 0 abdominal segment 1-10, amg anterior portion of mid-gu t,
gc germ cell, gorgonad rudiment,
hi head lobe,
int intercalary segment, Ir labrum, Ib labium, md
mandible,mx maxilla,
proct proctodaeum, pmg posterior portion of mid-gut, rmt
rudiment of malpighian tubule,
rp rectal papilla,th 1-3 thoracic segment 1-3,
tel
telson, tf terminal filament, vnc ventral nerve cord.

Oogenesis and Embryogenesis of Bactrothrips

89

Gonad
As mentioned in the previous chapter, the germ cells distribute on the caudal end of thegerm-band. They are accompained with the mesodermal cells which are smaller and darker
than the germ cells. While the thickening of the germ-band is occurring before katatrepsis,the most germ'cells are enclosed by the inner layer of the abdominal segment 6 or 7. They
form a pair of gonad rudiments which move cephalad during katatrepsis and fi~ally situatevery close to the 5th abdominal segment. In the Stage VIII and IX, they locate on the fatty
tissue of the 4th, 5th and 6th abdominal segments. They are spindle-like in shape and surrounded by thin epithelium derived from the mesodermal cells (Fig. 24).
At the anterior portion of the gonad rudiment the epithelium is seen to become a noncellular thread which elongates towards the distal end of the dorsal labial gland of the sameside. The posterior portion of the rudiment also elongates, but forms a cellular tubular
structure which may transform thinner and becomes the genital duct in both sexes in the
future.
In B. brevitubus and B. honoris the coelomic cavities of every abdominal segments do notdevelop well.
Some germ cells not enclosed in the abdominal segment are observable near the dorsal
wall of the embryo in the Stage VIII. The non-enclosed germ cells of H. verbasci have been-'
seen to become the yolk cells (Heming, 1979), but those of B. brevitubus seem to be
gradually degenerate and absorbed in the yolk.
The mode of gonad formation in B. brevitubus is almost identical to that of H. verbasci
reported by Heming (1979).

Alimentary CanalAs already mentioned the stomodaeum begins to invaginate at about 40 hours after thecommencement of the embryonic development (Stage V). The stomodaeal invagination
first appears just below the labrum; cells of this part become columnar gradually as theinvagination deepens. The stomodaeal end is encircled by a thin membrane consisting of few
cells that originated from the inner layer, and they form a muscle layer of the stomodaeumin future (Fig. 27).
Then the stomodaeum elongates into the space between the cephalic lobes and gnathal
part of the germ-band. The end of stomodaeum is depressed and slightly expanded, and thecell masses of the mid-gut epithlium are recognized at the end. They grow laterally, forminga pair of ribbons, and the splanchnic mesodermal layer also grows with the ribbon, while thebottom of the stomodaeum is encircled only with a thin membrane.
The proctodaeum is formed in the swollen part of the caudal end of the germ-band, thetelson (Fig. 28). In the Stage V, simultaneously with the stomodaeum formation, a pit
appears in the ventral side of the telson. The invagination deepens in the Stage VI, justbefore katatrepsis. Its wall is thicker than that of the stomodaeum. A part of the inner
layer of the 10th abdominal segment is crowded out in the space between the germ-band andthe yolk, and covers the proctodaeal end. A pair of the posterior rudiments of the mid-gut
epithelium is formed on the apical margin of the proctodaeum in the same manner as theanterior ones (Fig. 29).

90

Haga, K.

In the Stage VI, 4 glomerate cell masses consisting of 4 or 5 cells are formed in theswollen caudal part of germ-band where occurrence of the proctodaeum is expected (Fig.
28), and the proctodaeum is seen to occur after they are formed. These cell masses are therudiments of the malpighian tubules.
The rudiments of the malpighian tubules, in general, evaginate from the blind end of theproctodaeum in the stage of katatrepsis both in exopterygotes (Heymons, 1895; Roonwall,
1937; Butt, 1949; Goss, 1953; Ando, 1962) and endopterygotes (Henson, 1932; Butt,
1934; Okada, 1960; Miyakawa, 1975). In B. brevitubus, however, the rudiments areformed in the ectoderm of the telson as two pairs of glomerate cell masses before the invagination of the proctodaeum. This fact shows that the malpighian tubule is truly ectodermal in origin.
This also indicates that the method of malpighian tubule formation employed by B.
brevitubus is thus entirely different from that by other insect embryos.
The number of the malpighian tubule rudiments has been considered phylogeneticallysignificant, and varies one to three pairs depending on the insect groups. Johannsen andButt (1941) stated that three pairs of the rudiments apparently being the primitive number.
The embryos of B. brevitubus have two pairs of the rudiments, and the number may notchange even in the adult.
In the lateral view the developing stomodaeum becomes arched posteriorly as a result of
the condensation of the gnathal and thoracic segments, and the position of the oral opening
also shifts posteriorly before katatrepsis. At the same stage some cell masses are formed
inside the proctodaeal wall. They are the rudiments of rectal papillae, which are globular atfirst, but they are protruded into the lumen afterward. Five rudiments of the rectal papillae
are observed in the embryos of B. brevitubus, whereas four of them may be found in theadults of other thrips (Jordan, 1888; Uzel, 1895; Sharga, 1933). The developing proctodaeum also contains granular substances which are stained weakly blue by haematoxylin andtransform into a thin membranous structure in the Stage IX.
In the Stage VIII, the anterior rudiments of the mid-gut epithelium mentioned before
develop as a pair of slender ribbons which direct towards the proctodaeal bottom at theposition close to embryonic. dorsum (Fig. 30A); the posterior rudiments elongate similarly
towards the stomodaeal bottom. These ribbons meet with each other medially, forming aring-like structure in cross sections, which is oblong anteroposteriorly as shown in Fig. 30.
The ring is, then, seen to stretch dorsoventrally in the Stage X.
In this stage, the yolk ocuupies dorsal half of the egg, ranging from the secondary dorsal
enlarges, the yolk is consumed and decreases in volume. The position of the secondary
dorsal organ is seen to shift slightly posteriorly towards the posterior end of the egg, andfmally degenerates within the yolk which is enclosed by the developing mid-gut epithelium.
degenerates within the yolk which is enclosed by the developing mid-gut epithelium.
After katatrepsis, there can be observed many yolk cells (vitellophages) distributed allover the yolk, somewhat dense cortically (Fig. 25). They are almost the same in size andshapes, and sometimes two or three yolk cells are seen to aggregate. The yolk cells flatten
and expand to form very thin interstitial membranes which envelop yolk globules. At theoutermost part of the yolk, these membranes fuse with each other and form a thin, loose
and porous membrane enveloping the entire yolk mass.
The enveloped yolk globules are gradually liquefied, a little part of which later flows outof the membrane. The formation of the membrane and the yolk-liquefying begin before theOogenesis and Embryogenesis of Bactrothrips

25

91

sde

vph

Distribution of yolk cells in
Fig. 25.
Stage VIII embryo in B. brevitubus.
(Reconstracted by serial 17 sagittal
sections of a specimen)

stem

proct proctodaeum, sdo secondary dorsalorgan, stom stomodaeum, vph vitellophage.

completion of the mid-gut.
Before the definitive dorsal closure the posterior mid-gut epithelium near the proctodaeal
bottom evaginates to form a small chamber. The chamber (posterior portion of mid-gut;
Sharga, 1933) does not contain any yolk fractions at first, but later, the liquefied yolk may
often be found in the lumen of this chamber, most probably flowed in from the main part ofthe mid-gut. Since this portion so as to become more narrower and finally forms a loop in
the Stage IX, the cross sections of the embryos at this part show three rings of the mid-gut.
The stomodaeal bottom partially forms the cardiac valve which consists of several thickcells arranged circularly. From the cardiac valve to the anterior third of the mid-gut, theepithelial cells transform into tongue-like villi. The distal part of these cells contains a large
vacuole, which is often separated from the cells. These cells may be recognized as secretory,
and it is likely that the cut-off parts are holocrine particles. The rest of the mid-gut epithelium (posterior two-thirds of the mid-gut) consists of flat and thin cells, each of which also
contains a developing vacuole. In Fig. 31., these structures of the mid-gut epithelium areshown.
The spanchnic mesodermal layer which envelops the mid-gut epithelium develops in close
association with the mid-gut ribbons. The single mesodermal layer is recognized in the Stage
VIII and IX, but in early Stage X, thinly expanded cells appear upon the layer. They are

~

26
sdo

eav
amge
amg
de

pmg
pmge

~
~

00

inv

rmt

Fig. 26. Mid-gut formation in B. brevitubus, diagrammatic.
A. Stage IV, B. Stage VI, C. Stage VIII, D. Stage IX,

rev

E. Stage X.

am amnion,amge anterior mid-gut epithelial rudiment,at antenna, amg anterior
portion or mid-gut,
cf caudal flexure,cav cardiac valve, dc dorsal closure, ft fatty
tissue,ilm ileum, 1r labrum,mge mid-gut epithelium,
pmg posterior portion of
mid-gut,pmge posterior mid-gut epithelium,
proct inv invagination of proctodaeum,
pyv pyrotic valve,
rcv rectal valve, rmt malpighian tubule rudiment, rrp rudiment ofrectal papilla,
stom inv invagination of stomodaeum, ser serosa, sdo secondary dorsalorgan, yg yolk globule.

i lm

pyv

1"
~

Oogenesis and Embryogenesis of Bactrothrips
A
ST. VIlI

93

c

f. .~
.

o

---~
i ..,.
H.oo.
H

pc

amge

co.

~
F

27
Fig. 27.

Development of stomodaeum and anterior mid-gut epithelial rudiment in
B. honoris. Scale; lO p.m
A. Stage V, sagittal section,
B. Early Stage VI, sagittal section, C-E. Stage
VIII, cross sections. (c. across brain,D, across thorax, E. across 4th abdominal seglnent).
am amnion,amge anterior mid-gut epithelial rudiment, at antenna, cl cephalic lobe,
dig dorsal labial gland,
ft fatty tissue, ilc inner layer cell, mc
dce deutocerebrum,mesodermal cell, mes mesoderm, pc protocerebrum, rem rudiment of visceral muscle,
stom stomodaeum,
stom inv invagination of stomodaeum, stw stomodaeal wall, vnc
ventral nerve cord,vph vitellophage, vphm membrane made by vitellophages, yg yolk
globule.

D

28

Fig. 28.

Development of proctodaeum and posterior mid-gut epithelial rudiment in
B. honoris (Pre-revolution stage).
A. Stage V, sagittal section. B. Early Stage VI, sagittal section. C. Stage VI,
sagittal section. D. Late Stage VI, horizontal section.
ab 10 10th abdominal segment, am amnion, cf caudal flexure, gc germ cell, il inner
layer,
mes mesoderm, mt malpighian tubule, nb neuroblast, proct inv invagination
rmt malpighian tubuleof proctodaeum,pmge posterior mid-gut epithelial rudiment,
rudiment, rrp rudiment of rectal papilla.

Haga, K.

94

51. VIIIlA
goST. IX

D

29

Fig. 29. Development of proctodaeum and posterior mid-gut epithelial rudiment in
B. honoris (post-revolution stage).
B. Late Stage VIII, horizontal section.
A. Stage VIII, sagittal section.
C. Stage IX, sagittal section. D. Stage X, cross section.
ablg ganglion of 1st abdominal segment, ft fatty tissue, go gonad rudiment, ilm ileum,
mt malpighian tubule,oec oenocyte,
pmge posterior mid-gut epithelial rudiment,
proct proctodaeum,
rev rectal valve,
rem rudiment of visceral muscle, rp rectal
thl Ist thoracic segment,th, g ganglion of 3rd thoracic segment, vnc ventral
papilla,nerve cord, vph vitellophage, yg yolk globule.

A(v)@.':' .. ~....... ~r~ m-~>~;:J':L~,J '<':' ~':~.• ~ge"{,,'>L'~
(d)

vph
yg

vphm

vphm(o)vphm(i)1 i qy

oo

stom

~

::s
CD

B

'"tij '
~

::s

amge

Cl.

tTl

3

~
o

30

~

(v)

(d)

::s
CD

~,

'"o..,
~

""a~

pmge

S.
....

'§'
proct

Fig, 30. Mid-gut formation in B. brevitubus and B. honoris, diagrammatic.
A. Cross view. B. Lateral view.
amge anterior mid-gut epithelial rudiment,
em visceral muscle,
liqy liquefied yolk,
mge mid-gut epithelium,
rem rudiment of visceral muscle,
stom stomodaeum, vph(v) ventral,vitellophage,
vphm membrane made by vitellophages, yg yolk globule.
(d) dorsal, (0) outer, (i) inner.

'"

\11

Haga, K.

96

A

31

B

lP·

lu

em

mge nucleus

mge cell

B

c
D

5T.

Fig. 31.

x

Development of mid-gut epithelium.
A. Development of tongue-like holocrine tissue in B. brevitubus and B. honoris,
diagrammatic.
B. Cross sections of embryonic mid-gut at Stage X in B. honoris,
showing well or less developed villous tissues of three portions indicated byarrows. Scale: 10 J.1m.
cem circular visceral muscle, em visceral muscle,' lem longitudinal visceral muscle,liquefied yolk, lu lumen, mge mid-gut epithelium, vph vitellophage, y yolk.

liqy

Haplothr ~ps distinguendus[Sharga, 1933j

rectumcrop

oesophagus

mid-intestine
Bactrothrips brevitubusA
buccal cavity

Bactrothr ips brevi tuhus(Distended)B
rectal valve
mid-gut
pyrolic valve

Fig. 32.

anterior loop ofanterior mid-gut

malpighian tubule

32

Adult (A) and embryonic (B) al~entary canals in B. brevitubus compared with
Haplothrips distinguendus (Sharga, 1933).

Oogenesis and Embryogenesis of Bactrothrips

97

coarsely distributed, and later differentiate into longitudinal and circular muscles around the
mid-gut at the end of the Stage X.
The pyloric valve is formed between the posterior portion of the mid-gut and the proctodaeal bottom. It is more simple than the cardiac valve, and consists of flat cells which arearranged to form a ring.
Just posterior to the pyloric valve, a slightly swollen part of the mid-gut may be observed,
into which the malpighian tubules open. Sharga (1933) called this portion the ileum in theadult thrips.
Additionally one more type of the valve is distinctly formed between the ileum andrectum which may be called the rectal valve. It is a nozzle-like valve being formed by theinvagination of the proctodaeal wall. Heming (1979) has recognized this nozzle-like valve
as the pyloric valve in H verbasci, but it did not occur at the end of the mid-gut.
In the late Stage XI (Full-grown embryo), the yolk is completely liquefied and almost
consumed in the mid-gut, then the membranes formed by vitellophages disappear. Most of
the anterior portion of the mid-gut becomes empty, while a few yolk fractions are in the restof the mid-gut.
Malpighian tubules develop both anteriorly and posteriorly, and a loop is formed attheir distal portions. The anterior pair of malpighian tubules occur at the ventral side of -theileum and reaches the metathorax, while the posterior pair derives at the dorsal side of theileum, and reaches the 9th abdominal segment.
The stomodaeum in the embryonic stage does not further differentiate to form into thecrop and preventriculus.
The mid-gut formation in insect embryos is still controversial, but is summarized into
three types (Roonwall, 1939; JohannsenandButt, 1941; Ando, 1970): Type!. Mid-gut
epithelium is formed mainly by yolk cells; Type n. Mid-gut rudiments are derived from thestomodaeum and/or the proctodaeum; Type III. Mid-gut epithelium is formed by the midgut rudiments, and a part of the inner layer. The first type is known in Collembola, Thysanura, Odonata. The last type is observed in Phyllobius glaucus (Coleoptera, Jura, 1956)
and others. The most pterygote insects belong to the second type, and the present materials,
B. brevitubus and B. honoris represent Type 11, a typical bipolar formation of the mid-gut.

Discussion
By the present study and recent works mentioned at the beginning of this paper, theknowledge on the oogenesis and embryogenesis in the Thysanoptera has become increased.
Though information on these subjects is still unsatisfactory, it may now be possible tocompare the Thysanoptera with other insects of related orders.
The order Thysanoptera belongs to the Paraneoptera ( = Acercarida of Boudreaux,1979).
Usually the Paraneoptera consists of six orders/suborders, namely, Psocoptera, Mallophaga,
Anoplura, Thysanoptera, Homoptera and Heteroptera. This group considered as the most
evolved in the Exopterygota (= Hemimetabola).
As shown in Table 4, the embryogenesis of only a limited number of the insects belonging
to those taxa have so far been studied. Further study of embryogenesis occurring in theinsects which occupy phylog~netically important status in these insect orders seems to bevery necessary.

Table 4. . List of insects embryologically studied in paraneopteran orders.
HETEROPTERAPSOCOPTERA

Archipsocus fernandi
Liposcelis divergens
Liposcelis bostrychophilus
Lepinotus patruelis
Psyl/ipsocus ramburi
Prionoglaris stygia
Ectopsocus meridionalis

Rhodnius prolixus
Oncopeltus fasciatus
Gerris paludum

Fernando, 1934
Goss, 1952, 53
Seeger, 1979
Seeger, 1979
Seeger, 1979
Seeger, 1979
Seeger, 1979

HOMOPTERA

Siphanta acuta
Icerya purchasi
Macrosiphum tanaceti
Lecaniodiaspis prumosa
Pyrilla perpusilla

ANOPLURA

Pediculus humanus
Pediculus vestimenti
Phthirus pubis
Pedicinus rhesi
Linognathus vituli
Haematopinus eurysternus
Haematopinus suisi

Mellanby, 1935, 36
Newcomer, 1948; Butt, 1949
Mori, 1969, 76

ScMlzel, 1937
Piotrowski, 1953
SchllIzel, 1937
SchcrIzel, 1937
Schlllzel, 1937
SchllIzel, 1937
Young, 1953

Muir and Kershaw, 1912
Shinji, 1919, 24
Uichanco, 1924
Shinji, 1924
Sander, 1956

THYSANOPTERA

Thrips physapus
Heliothrips haemorrhoidalisCaudothrips butfai
Haplothrips verbasci
Bactridothrips brevitubus

Uljanin, 1874
Reyne, 1927
Bournier, 1966
Heming, 1979, 80
Ando and Haga, 1974

MALLOPHAGA

Columibicola columbae
Gyropus ovalis
Trichodectes scalaris

SchllIzel, 1937
ScMlzel, 1937
Schlllzel, 1937

Table S. Comparison in ovary and egg among paraneopteran orders.
PSOCOPTERAMALLOPHAGAANOPLURA

Ovarian type

Polytrophic

Polytrophic

Polytrophic

Ovariole/ovary

3-5

3-5
Present

Present

Absent orpresent

Present or

Present

Micropyle,

AbsentSymbiont

AbsentOosomeAbsentabsentAbsentAbsent

THYSANOPTERAHOMOPTERAHETEROPTERA

Panoistic

Telotrophic

Telotrophic

4

2 - 25

2-8

Present

Present

Absent orpresent
Present

Present
AbsentAbsent orpresent
AbsentOogenesis and Embryogenesis of Bactrothrips

99

Table 6. Comparison in the early embryogenesis among paraneopteran orders.
PSOCOPTERAMALLOPHAGAANOPLURA

THYSANOPTERAHOMOPTERAHETEROPTERA

CleavagecenterCenterCenterAnt. 1/3

Post. 1/3

Ant. 1/3

CenterSynchrony

6th

8th

8th

3rd. 4th

7th

7th

Energid

After 7th

After 8th

After 8th

After 7th

After 9th

After 8th

UnevenEven

Even

Uneven

Even

Even

+

+

+

+

+

+

+

+

Proliferation

Invagi-

Invagi-nationnationmigration
Energid
distribution

Primaryyolk cell
Secondaryyolk cell
Yolk cleavage+

I
Prolifer·
ation

Inner layer
formation++

I

Invagi~

Invagi-nationnationTable 7. Comparison in the organogenesis among paraneopteran orders.
PSOCOPTERAMALLOPHAGAANOPLURA

THYSANOPTERAHOMOPTERAHETEROPTERA

Developed

IIJ developed

III developed

III developed

Developed

Developed

formation *II

II + 1II

II + 1IIII

II

11 or IP

Tentorium

Developed

III developed

III developed

III developed

Developed

Developed

Tl+2+3. Al

Tl+2+3. AO

Tl+2+3. AO

Tl. T2+3. Al

Tl+2+3, AO

Tl+2+3, AO

Coelomic
Cavities

Mid·gut

Ganglia **concentration

Malpighiantubulerudiment

4

4

4

2·4

Rectalpapilla

4·5

>4

4,5

4·5

* Signs after Ando (1970).
** T thoracic ganglion, A abdominal ganglion, + fused,without ganglion.

4·5

1-3 segment (ganglion),

A
PARANEOPTERAB
ACERCARIDAPSOCOPTEROID1pSOCOPTERAPSOCODIDA----yPSOCIDAMALLOPHAGA

...

=
=

--rCORRODENTIA

LPHTHRIAPTERIDA1MALLOPHAGAANOPLURAANOPLURACONDYLOGNATHIDATHYSANOPTEROID-THYSANOPTERAl

THYSANOPTERIDA~THYSANOPTERAHEMIPTERIDA lHOMOPTERAHEMIPTEROID 1HOMOPTERAHETEROPTERAHETEROPTERA

C

PSO

D

~ PSO

--<

MAL
ANO

./'

'-ANO

THY

.............

./' THY

HOM
HET

Fig. 33.

___ MAL

~

E

==
&;
J'"

r:

PSO
MAL
ANO

-""HOM- HETClassification and phylogeny of the Paraneoptera, or Acercarida.
A. Pesson, 1951. B. Boudreaux, 1979.
C., D., E. Three types of the phylogeny of Paraneoptera.

33

Oogenesis and Embryogenesis of Bactrothrips101

The comparison of these orders was done on 19 characters which have a common ornearly common state in the ovarian and egg structures, early embryogenesis and organogenesis of each paraneopteran orders.

Comparison of Embryonic Development in the Paraneopteran Orders
A. Comparison of Ovary and Egg (Table 5)
Paraneopteran ovarian types can be classified into three categories, i. e., the polytrophic
type of the Psocoptera, Mallophaga and Anoplura, the telotrophic type of the Homoptera
and Heteroptera, and the panoistic type of the Thysanoptera, respectively. The last type isconsidered as primitive plesiomorphic form.
On the other hand, Heming (1979) found out the oosome of H. verbasci egg, and thepresent author confirms it in the eggs of B. brevitubus and B. honoris. The oosome is often
observed in the holometabolous insect eggs, but is scarsely known from the eggs of the otherparaneopteran orders.
The mycetome exists in thrips eggs of the Idolothripinae, but does not exist in the Phlaeothripinae as like as those in the Psocoptera. On the contrary, the micropyle is only foundin H. verbasci egg, and the author could not find it in B. brevitubus and B. honoris. The
psocopteran LiposceJis divergens also lacks the micropyle in its eggs.

B.

Comparison of the Early Embryogenesis (Table 6)

Generally the position of the cleavage center locates in the center or in the anterior halfof the insect eggs, however, in the Thysanoptera B. brevitubus, B. honoris and H. verbasci, it
locates in the posterior half of the egg. The cleavage synchrony observed in B. brevitubus
lasts only until the 3rd cleavage, much shorter than that in the other orders.
Usually the energid density becomes even in the any part of the egg until just before
blastoderm formation. However, in B. brevitubus it remains uneven distribution, dense in
the posterior half and rare in the anterior half up to the period of the blastoderm formation.
The yolk cleavage is known in the Mallophaga and Anoplura, but it does not occur in theeggs of B. brevitubus.
It is said that the method of inner layer formation is phylogenetically significant eventhough there are exceptions. Three types of inner layer formation have been known, namely, invagination, overgrowth and proliferation, respectively. In the Paraneoptera the difference in the method may show certain relationships among them. In the Thysanoptera theinner layer is formed by the proliferation type like that in the Psocoptera, in contrast withthe other four orders which have the invagination type.

C.

Comparison in the Organogenesis (Table 7)

Concerning the formation of the coelomic cavity and tentorium, the Paraneoptera can bedivided into two groups, i. e., Psocoptera-Homoptera-Heteroptera group (developed) and102

Haga, K.

Mallophaga-Anoplura-Thysanoptera group (ill-developed). On the other hand, when gangliaof the ventral nerve cord concentrate anteriorwards and make synganglia, the abdominal
ganglia still remain as a block in the Psocoptera and Thysanoptera, but they are completely
contracted and coalesced with the thoracic ganglion in the other paraneopteran orders.
The Thysanoptera and most Hemiptera show the typical method in the mid-gut formation, the bipolar formation as described in the previous chapter.
Results of these comparisons may suggest following items:
1.
2.
3.
4.

5.

The, Mallophaga and Anoplura are close to each other.
The Homoptera and Hemiptera are also close to each other.
The Psocoptera resembles the all other members.
The Thysanoptera is segregated from the other members by having many proper character states.
The Thysanoptera positions nearly eqUidistant from the Psocoptera, Homoptera andHeteroptera, but far from the Mallophaga and Anoplura.

Above-mentioned affinity distances of the paraneopteran orders imply the oldest separation of the Thysanoptera from the other members, and the author agrees with Rodendorf
et al. (1962) regarding the old ramification occurred before the branching of the psocoptera- and Hemiptera stems.
Pesson (1951) classified the Paraneoptera into 3 subgroups, i. e., Psocopteroid (Psocoptera, Mallophaga and Anoplura), Thysanopteroid (Thysanoptera) and Hemipteroid (Homoptera and Heteroptera) (Fig. 32 A). Recently, Boudreaux (1979) proposed systematicsof the supercohort Acercarida (Fig. 32 B). He arranged the Thysanopterida (Thysanoptera)
as a sub cohort at the same level to the Psocida (Psocoptera), Phthirapterida (Mallophaga
and Anoplura) and Hemipterida (Homoptera and Heteroptera). The results of the present
study support these classifications, and are more suitable for the former.
As shown in Fig. 32, it can be thought that there are three cladistic patterns concerning
the phylogeny of the Paraneoptera (Asahina, 1970; Boudreaux, 1979; Heming, 1979,
1980; Kim and Ludwig, 1978; Mound and O'Neil, 1974; Mound et ai, 1980; Pesson,
1951; Rodendorf et ai, 1962; Schliephake, 1975; Schliephake and Klimt, 1979; Seeger,
1979; Sharov, 1972; Stannard, 1957; Wilson, 1971), and the results almost coincide thethird type (32 E).

Acknowledgements
The author would particularly like to express hearty gratitude to Prof. Hiroshi Ando,
Director of Sugadaira Montane Research Center, University of Tsukuba for his constantguidance and encouragement throughout the course of the present study, and his criticalreading of the manuscript.
The author's thanks are due to professors of the Institute of Biological Sciences, University of Tsukuba, Dr. K. Sekiguchi, Dr. H. Kurokawa, Dr. M. Chihara, Dr. T. Shibuya
and Dr. M. Okada for their kind counsels and encouragements. Thanks go also to Prof. M.
Matsuzaki of Fukushima University, to Dr. C. Tsutsumi of Tokyo Gakugei University, toOogenesis and Embryogenesis of Bllctrothrips

103

Dr. T. Yamasaki of Tokyo Metropolitan University, and to Dr. K. Miyakawa of Gakushuin
High School for their helpful advices. His appreciations are extended to Prof. K. Miya of
Iwate University and Dr. H. Mori of Tokyo Metropolitan University for their kind readingof the manuscript.
Most part of the present study was done at the Sugadaira Montane Research Center,
University of Tsukuba, and the author is indebted to the staff and stayed students of theCenter for their friendly supports in various ways.

References
Ando, H., 1953. Studies on the pleuropodium of Odonata. Sci. Rep. Tokyo Bunrika
Daigaku B7: 167-181.
- - - , 1962. The comparative embryology of Odonata with special reference to arelic dragon fly Epiophlebia superstes Selys. Jap. Soc. Promt. Sci. Tokyo 1-225.
____,' 1970. Embryonic development. In Systematic Zoology, IlIa Arthropoda"
Insecta I: 37-130. Nakayama-shoten, Tokyo. (Japanese)Ando, H. and K. Haga, 1974. Studies on the pleuropodia of Embioptera, Thysanoptera
and Mecoptera. Bull. Sugadaira Bioi. Lab. 6: 1-8.
Asahina, S., 1970. Phylogeny and classification. In Systematic Zoology, IlIa Arthropoda,
Insecta I: 203-343. Nakayama-shoten, Tokyo. (Japanese)
Boudreaux, H. B., 1979. Arthropod phylogeny with special reference to insects. John
Wiley & Sons, Inc. 1-320.
Boumier, A., 1957. Un deuxit!me cas d'ovQviviparitt! chez les Thysanoptt!res Caudothrips
buffai Karny (Tubulift!re). Comp. rend. aean. Acad. Sci. 244: 506-508.
_ _ _ _ _ _ , 1960. Sur l'existence et l't!volution du corps dorsai secondaire dans 1'ontogent!se de Caudothrips buffai Kamy (Thysanoptera, Tubulifera). Ibid. 278:
1347-1348.
- - - - - , 1962. L'appareil genital femelle de Caudothrips buffai Kamy et sa pompe
spermatique. Bull. Soc. ent. Fr. 67: 203-207.
_ _ _ _ _ , 1966. L'embryogenese de Caudothrips buffai Kamy (Thysanoptera:
Tubulifera). Ann. Soc. ent. Fr. (N. S.) 11(2): 415-435.
Butt, F. H., 1934. Embryology of Sciara. Ann. ent. Soc. Amer. 27: 565-579.
_ _ _ _ , 1949. Embryology of miIkweed bug, Oncopeltus fasciatus (Hemiptera).
Cornell. Univ. Agr. Exp. St. Mem. 283: 1-43.
Femando, W., 1934. The early embryology of viviparous psocid. Quart. J. micro Sci. 77:'99-119.
Goss, R. J., 1952. The early embryology of the book louse, Liposcelis divergens Badonnel(Psocoptera: Liposcelidae). J. Morphol. 91: 135-169.
- - - - , 1953. The advanced embryology of the book louse, LiposceZis divergens
Badonnel (Psocoptera, Liposcelidae). Ibid. 92: 158-205.
Haga, K., 1972. Thysanoptera occurring on dead leaves and dead branches. Ann. Rep.
Attached High School Osaka Kyoiku Univ. 14: 99-112. (Japanese)- - - , 1974. Postembryonic development of Megathripine species Bactridothrips brevitubus Takahashi (Thysanoptera). Bull. Sugadaira Bioi. Lab. Tokyo Kyoiku Univ. 6:
11-32.
- - - " 1975. Female reproductive system of Megathripine species Bactridothrips brevitubus (Thysanoptera, Insecta). Ibid. 7: 13-24.
Heming, B. S., 1970a. Postembryonic development of the female reproductive system inFrankliniella fusca (Thripidae) and Haplothrips verbasci (Phlaeothripidae) (Thysanoptera). Misc. Publ. En tom 01. Soc. A mer. 7(2): 199-234.

104

Haga, K.

_ _- - - , 1970b. Postembryonic development of the male reproductive system inFrankliniella fusca (Thripidae) and Haplothrips verbasci (Phlaeothripidae) (Thysanoptera). Ibid. 7(2): 235-272.
_____ , 1973. Metamorphosis of the pretarsus in Frankliniella fusca (Hinds)(Thripidae) and Haplothrips verbasci (Osborn) (Phlaeothripidae) (Thysanoptera).
Canad. J. Zool. 51(12): 1211-1234.
_ _ _ _-, 1975. Antennal structure and metamorphosis in Frankliniella fusca (Hinds)(Thripidae) and Haplothrips verbasci (Osbom) (Phlaeothripidae) (Thysanoptera).
Quest. En tom 01. 11: 25-68.
_ _ _ _ _ , \979. Origin and fate of germ cells in male and female embryos of Haplothrips verbasci (Osborn) (Insecta, Thysanoptera, Phlaeothripidae). J. Morphol. 160(3):323-343.
_____ , 1980. Development of the mouthparts in embryos of Haplothrips verbasci(Osborn) (Insecta, Thysanoptera, Phlaeothripidae). Ibid. 164: 235-263.
Henson, H., 1932. The development of the alimentary canal in Pieris brassicae and theendodermal origin of the malpighian tubules of insects. Quart. J. Micr. Sci. 75: 283309.
Heymons, R., 1895. Die Embryonalentwicklung von Dermapteren Ben'1cksichtigung derKeimbllitterbildung. Gustav Fischer, Jena 1-136.
Johannsen, O. A. & F. H. Butt, 1941. Embryology of insects and myriapods. McGrawHill, New York & Lond.: 1-462.
Jordan, K., 1888. Anatomie und Biologie der Physapoda. Zeit. f. wiss. Zool. 47: 541-620.
Jura, C., 1956. Embryogenesis of the alimentary system of the weevil, Phyllobius glaucus
Scop. (Curculionidae, Coleoptera). Zool. Poloniae. 7: 155-176.
Kim, K. C. and H. W. Ludwig, 1978. Phylogenetic relationships of parasitic Psocodea andtaxonomic position of the Anoplura. Ann. ent. Soc. Amer. 71(6): 910-922.
Lewis, T., 1973. Thrips, their biology, ecology and economic importance. Academic Press,
Lond. & N. Y. 1-349.
Mahowald, A. P., 1972. Oogenesis. In Developmental Systems: Insects. 1: 1-47.
Academic Press. London.
Mound, L. A. and K. O'Neill, 1974. Taxonomy of the Merothripidae, with ecological andphylogenetic considerations (Thysanoptera). J. nat. Hist. 8: 481-509.
- - - - - , B. S. Heming and J. M. Palmer, 1980. Phylogenetic relationship between
the families of recent Thysanoptera (Insecta). Zool. J. Linn. Soc. 69(2): 111-14l.
Mellanby, H., 1935. The early embryonic development of Rhodnius prolixus. Quart.
J. Micr. Sci. 78: 71-90.
- - - - - , 1936. The later embryonic development of Rhodnius prolixus. Ibid. 79:
1-42.
Mickoleit, E., 1963. Untersuchungen zur Kopfmorphologie der Thysanoptera Zool. Jb.
Anat. 81: 101-150.
Miyakawa, K., 1973. The embryology of the caddisfly Stenopsyche griseipennis MacLachlan(Trichoptera: Stenopsychidae) V. Kontyu 43: 55-74.
- - - - - , 1978. A paraffin technique for insect eggs. Gakushu'in Kotoka KenkyuKiyo 9: 17-23. (Japanese)Mori, H., 1969. Normal embryogenesis of the waterstrider, Gerris paludum insularis
Motschulsky, with special reference to mid gut formation. Jap. J. Zool. 16: 53-67.
- - - - , 1976. Formation of the visceral musculature and origin of the midgut epithelium in the embryo of Gerris paludum insularis Motschulsky (Hemiptera: Gerridae).
Int. J. Insect Morphol. Embryol. 5: 117-125. 194-207.
Muir, F. and J. C. Kershaw, 1912. The development of the mouthparts in the Homoptera,with observations on the embryo of Siphanta. Psyche 19: 77-89.
Newcomer, W. S., 1948. Embryological development of the mouthparts and related structures of the milkweed bug, Oncopeltus fasciatus (Dallas). J. Morphol. 82: 365-411.

Oogenesis and Embryogenesis of Bactrothrips

105

Okada, M., 1960. Embryonic development of the rice stem-borer, Chilo suppressalis.
Sd. Rep. Tokyo Kyoiku Univ. Sec. B. 9: 243-296.
Pesson, P., 1951. Ordre des Thysanoptera. In Traite de Zoologie 10. Grasse ed. Masson,
Paris. 1805-1869.
Peterson, A., 1915. Morphological studies on the head and mouth parts of the Thysanoptera.
Ann. Ent. Soc. Amer. 8: 20-59.
Piotrowsky, F., 1953. The embryo1ogical development of the body louse Pediculus vestimenti Nitzsch. Part I. Acta. parasitol. Pol. 1(3): 61-84.
Reyne, A., 1927. Untersuchungen iiber die Mundteil der Thysanoptera. Zool. Jb. Anat.
49: 391-500.
*Rhodendorf, B. B., O. M. Martinov, E. Y. Bekker-Midgisova, & A. G. Sharov, 1962. Osynovy Palentologii. 1-560. Moscow.
Risler, H. and E. Kempter, 1961. Die Haploidie der MlInnchen und die Endopolyp1oidie
in einigen gewehen von Haplothrips (Thysanoptera). Chromosoma 12: 351-361.
Roonwal, M. L., 1936. Studies on the embryology of the African migratory locusta, Locusta migratoria migratorioides R. and F. (I). Trans. Roy, Soc. Lond. b226: 391421.
_ _ _ _ • 1937. Ditto (11). Ibid. B227: 175-244.
Sander, K., 1956. The early embryology of Pyrilla perpusilla Walker (Homoptera), including some observations on the later development. Aligarh Muslim Univ. Publ. (Zool.
Ser.) 4: 1-61.
Schliephake, G., 1975. Beitrag zur phylogenetischen Systematik bei Thysanopteren. Beitr.
Ent. 25: 5-13.
- - - - - - , and K. Klimt, 1979. Thysanoptera, FransenfHigler: Die Tierwelt Deutschlands. 66: 1-477.
Scholzel, G., 1937. Die Em bryologie der Anopluren und Mallophagen. Zeit. f Parasitenkunde 9: 730-770.
Seeger, W., 1979. Spezialmerkmale an Eihiillen und Embryonen von Psocoptera im Vergleich
zu anderen Paraneoptera (Insecta); Psocoptera als monophyletische Gruppe. Stuttgartner Beitr. Naturk. A 329: 1-57.
Sharga, U. S., 1933. On the internal anatomy of some Thysanoptera. Trans. Roy. ent. Soc.
Lond. 81(2): 185-202.
Sharov, A. G., 1972. On phylogenetic relations of the order of thripses (Thysanoptera).
Revue d'Ent. de I'URSS 60(4): 854-858.
Shinji, O. G., 1919. Embryology of coccids, with special reference to the formation of theovary, origin and differentiation of germ cells, germ layers, rudiments of the midgut,
and the intracellular symbiotic organisms. J. Morphol. 33: 73-167.
, 1924. Embryology of coccids with special reference to the origin and differentiation of ovarian elements, germ layers, nervous and digestive systems. Bull. Imp.
Coll. Agr. Fores. Morioka 6: 1-61.
Slifer, E. H., 1937. The origin and fate of the membranes surrounding the grasshopper egg;
together with some experiments of the hatching enzyme. Quart. J. Micr. Sci. 79:
493-506.
Stannard, L. J., 1957. The phylogeny and classification of the North American genera of
the suborder Tubulifera (Thysanoptera). Ill. Bioi. Monogr. 25: 1-200.
Uichanco, L. B., 1924. Studies on the embryogeny and postnatal development of theAphididae with special reference to the history of the "symbiotic organ" or "mycetom'.'
Philip. J. Sci. 24: 143-247.
Uijanin, W. N., 1874. Observations on the development of thrips (Physopoda). Izviastiia
Imp. Ob. Luibit Estest. Anth. Ethnogr. 10: 39-43.
Uzel, H., 1895. Monographie der Ordnung Thysanoptera. Ko'niggratz 1-472.
Wilson, S. T., 1971. A revision of the subfamily Heliothripinae of the world. Univ. Press
Xerox Co. 486 '71: 1-256.

Haga, K.

106

Young, J. H.,
85-133.

1953.

Embryology of the mouthparts of Anop1ura. Microentomol.

18:(* ... After Asahina, 1970)

Author's address:

Dr. K. Haga,
Institute of Biological Sciences,
University of Tsukuba, Sakura-mura,
Ibaraki, 305 Japan