Zoo1.J. Linn. SOC.,48, pp. 59-81. With 15jigures
Observations on the female reproductive organs and the
poison apparatus of Caraphractus cinct us Walker
(Hymenoptera : Mymaridae)
DOROTHY J. JACKSON
North Chf, St. Andrews, Fqe
Accepted for publication September 1968
~~
Caraphractus cinctus is an arrhenotokous mymarid parasitizing the eggs of Dytiscidae under
water. In the newly emerged female only fully formed eggs are present in the ovaries and the
earlier stages of ovarian development have been studied in the pupa. The two ovaries each contain from 10to 20 ovarioles depending upon the size of the female. T h e two lateral oviducts unite
to form the vagina which is bent upon itself when laying is not in progress. The eggs are stored
in the ovarioles and the female has remarkable control over the deposition of the eggs, since in
most cases she rejects host eggs already parasitized, after probing them with her ovipositor.
The spermatheca is a rigid capsule and the spermathecal duct at its base has a deep U-shaped
bend. There is a large spermathecal gland opening by its awn duct into the spermathecal duct
after the bend. The poison apparatus is well developed though the female does not kill the egg or
paralyse the embryo host. The poison gland is of unusual shape being compact and rounded distally instead of tubular. Dufour’s gland is large and buoyant. The ducts of both glands lead to the
base of the ovipositor. The possible effect of their secretions in rendering a once parasitized
Agubus egg generally unacceptable for further laying is discussed.
CONTENTS
Introduction .
Material and methods
.
The female gaster
.
Theovaries
.
The oviducts .
T h e transit of the eggs to the ovipositor
The bursa copulatrk
.
The spermathecal apparatus
.
The poison apparatus
.
Discussion
.
Acknowledgements .
References
.
Key to figure lettering
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PAGE
59
60
61
63
68
69
71
72
74
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79
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INTRODUCTION
Caraphractus cinctus Walker is a parasitoid of the eggs of Dytiscidae and various
features of its biology have been studied (Jackson, 1958, 1961, 1963, 1966). It belongs
to the family Mymaridae which contains many species of economic importance in the
control of various insect pests, yet no account appears to have been published of the
female reproductive organs of these egg parasitoids, nor of their poison apparatus. Both
show certain characters not recorded for other parasitic Hymenoptera.
60
DOROTHY
J. JACKSON
This paper covers only part of the work done on the female genital system of
Caraphractus. A detailed study is being made of the ovipositor, which presents features
of unusual interest. It is hoped to publish the results in the near future and only brief
references will here be made to the morphology of the ovipositor when this is needed
for an understanding of its relation to other parts of the reproductive system. The terms
used in the present paper for the sclerites of the ovipositor are those employed by
Snodgrass (1933) and the terminology adopted by Scudder (1961) will be referred to
in the later paper.
MATERIAL AND METHODS
The Caraphractus used in these investigations were mostly reared in eggs of Agabus
bipustulatus L. which are laid throughout the greater part of the year, but during the
summer, when the eggs of this host are scarce, those of A. sturmii Gyllenhall and
Ilybiusfuliginosus F. were used. By keeping the parasitized eggs under continuous light
from autumn to spring, diapause, which occurs in Caraphractusin the prepupal state,
was eliminated, and each generation emerged in about a month (Jackson, 1963). Since
the egg shells of these hosts are transparent the parasitoids could be removed for study
from the pupal stage onwards, but most of the females were dissected after emergence.
Pupae of all ages, both alive and fixed have been dissected to examine the ovaries
in their early stages. Many females have been killed whilst laying to study the position
of the egg in the vagina :others have been killed for dissection directly after or within
a few minutes of mating. Carnoy’s fixative was mostly used as it kills instantly and gives
excellent results. Duboscq-Brad fixative was also very good and Barber’s fluid was
found useful. Mayer’s paracarmine proved a most satisfactorystain for all fixed material.
Great difficulty was experienced in making good dissections of living adult females
owing to the extreme buoyancy of the female gaster. After crushing the head and thorax
of a living female the abdomen was much contracted and hard to open. Tergitol, as
recommended by Bender (1943) to reduce surface tension was tried, also very dilute
solutions of a detergent. These helped submergence but spoilt the preparations. Dying
or nearly dead females remained submerged and, as the body was less contracted,
dissection was easier. Living tissues were examined in 0.5% aqueous solution of Trypan
red (pH 8.65) or in Ringer solution (sodium chloride 0.8 parts, calcium chloride 0.02,
potassium chloride 0-02, sodium bicarbonate 0.02 and water 100). The p H of this
solution was 8.13. Successful fresh dissections were later fixed in Pampel’s fluid or in
aceto-carmine. Whole mounts of the gaster were made using Pampel’s fluid which
contracts the viscera less than Carnoy.
The size of Caraphractus adults is very variable depending on the number present in
one host egg and the size of the host. Thus, in a superparasitized egg of A. bipustulatus
females may measure only 0.78 mm from head to apex of abdomen but singleton females
from the same host measure from 1.4to 1.6 mm. The width of the gaster varies depending on whether the female is relaxed or contracted and, in a female of average size (when
two or three individuals are bred in one Agabus egg) killed in Carnoy’s fluid, the gaster
measures from 0.48 to 0.58 mm long by 0.25 to 0.28 mm at the widest part. The length
of a pupa is greater than that of the resulting adult as the pupa is soft and extended.
For the various figures large females have been used, obtained by supplying one or
REPRODUCTIVE
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61
two mated females with many eggs. The drawback to the dissection of the large females
is the excessive fat body. In small females the fat body is reduced and the reproductive
organs stand out more clearly. This study has been based principally ofi dissections of a
great number of females and sections have also been used.
THE FEMALE GASTER
In the living female (emerged from the host) all the segments of the gaster are not
fully exposed, as the posterior segments are partly retracted in a telescopic manner and
the third tergite occupies more than half of the gaster. In an anaesthetized female it is
0.3mrn
FIGURE
1. Lateral view of gaster of large female, fixed Pampel’s fluid, showing position of one
ovary, the other ovary is directly behind it. One lateral oviduct, continuous with vagina is
shown, but the round glands are omitted. Poison gland and reservoir are shown. Chitinous parts
are shaded with lines.
seen that the tergites extend to the ventral side largely obscuring the sternites. Thus,
in the living active female, either in the air or under water, the abdomen is cylindrical
in shape, tapering towards the apex, and all the membranous parts are concealed.
In a newly moulted female extracted from the host egg, the gaster is not contracted
and the segmentation can be studied. The same condition occurs when a female dies a
natural death in water, since the intersegmental muscles relax a few hours after death
and the soft membranous parts are exposed. The position of the ovaries is shown in
Fig. 1 in a female fixed in Pampel’s fluid and Fig. 2, at a lower magnification, shows the
62
DOROTHY
J. JACKSON
skeletal parts alone. Seven tergites, numbers 3 to 9, are visible in the gaster, since the
first abdominal segment, the propodeum, is incorporated in the thorax, and the second
tergite constitutes the petiole. The first gastral tergite is thus the true third. It is much
the largest, tergites 4 to 8 being progressively smaller. The eighth tergite bears the only
pair of gastral spiracles. The last tergite, the ninth, is long and narrow, extending to the
ventral side and to the base of the ovipositor. Dr M. W. R. de V. Graham, who has
kindly examined my figure of the gaster, considers this sclerite may be the combined
ninth and tenth tergites as Domenichini (1953) records for the mymarid, NowickyeZZa
TIU
0.3mm
FIGURE
2. Lateral view of gaster and petiole of singleton female from egg of Agabus bipustulatus,
drawn shortly after death to show exoskeletal parts only.
domenichinii Soyka. This tergite bears on each side near its dorsal surface a sensorium,
the pygostyle, an oval structure with four to five pygostylar bristles, and a few other
long bristles are present nearby. Beneath the lower edge of the ninth tergite in the middorsal line is a fleshy projection presumably the proctiger (Snodgrass, 1933 : 109-113).
There are five visible gastral sternites, the first of which is the third sternite, and the
last the seventh. A delicate intersegmental membrane connects the seventh sternite
with the basal region of the ovipositor. In the living female the ovipositor when at rest
lies close to the ventral side of the abdomen in a shallow groove. The shaft of the
ovipositor is composed of three parts in the adult insect, the two first valvulae and the
united second valvulae which form a sheath. When at rest the ovipositor is protected
by the third valvulae which take no part in laying, remaining in place when the ovipositor
is lowered into a vertical position to pierce the host egg. The basal sclerites of the ovipositor consist of four plates, the paired first and the paired second valvifers. The first
and second valvulae of the ovipositor are united basally with the first and second
REPRODUCTIVE
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63
valvifers respectively and the upward extensions of the valvulae, the rami of the valvulae
curve round the basal sclerites of the ovipositor at each side.
THE OVARIES
The two fan-shaped ovaries contain a variable number of ovarioles, from 10 to 20, in
each ovary. Between the ovaries and just above the lateral oviducts lies the nerve cord
with three ganglia. In the adult the ovaries are entirely filled with fully formed eggs of
varying sizes.
In no stage of development in this insect do all the features characteristic of a polytrophic ovary show at the same time, but they appear at successive stages. The growth
b
r
O.lmm
FIGURE
3. Three ovariolesfrom an early pupa which was pale with some facets of the compound
eyes pink. Fixed Camoy’s fluid.
of the ovaries has been studied by dissecting pupae of various ages, either alive or after
fixation. The age of the pupa can be roughly assessed from its coloration (Jackson, 1961:
278). Pupae less than two days formed are colourless except for the compound eyes in
which some of the facets are pale pink. The ovarioles at this stage are short and comparatively thick and are filled with cells not yet showing differentiation into nutritive
cells and oocytes Fig. 3. This condition may be considered as the germarium stage.
Later, the ovarioles lengthen and show some segmentation into chambers containing
cells of about equal size, and close to the base of the ovariole a small oocyte may show.
By the time the compound eyes of the pupa are dark and the thorax dusky, the number
of oocytes in each ovariole has increased (in females of normal size) to three or four.
The oocytes are mostly interposed between the nutritive chambers but sometimes two
or even three nutritive chambers may lie anterior to one oocyte. The oocytes are small
near the apex of the ovariole and larger near the base (Fig. 4). The follicle cells surrounding each oocyte are most distinct at the ends of the oocyte, and the germinal
vesicle is situated near the anterior end. Each nutritive chamber contains an average
DOROTHY
J. JACKSON
64
of 14 nurse cells or nutritive cells with large nuclei and distinct nucleoli. The wall of the
ovariole is distinct in the early stages (Fig. 3) having elongated nuclei lying parallel to
the ovariole, but in later stages the nuclei are no longer distinguishable.
0.1mm
FIG- 4. Two ovarioles (separated) from an older pupa with thorax dusky, fixed DuboscqBrasil.
By the time the thorax of the pupa is mainly dark, the oocytes have increased in size
and partly overlap each other at the base of the ovariole (Fig. 5). As development
TF
!
O.lmm
FIGURE
5. Two ovarioles from a still older pupa having the thorax dark. Fixed Carnoy’sfluid.
REPRODUCTIVE
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continues and the pupa darkens, the pedicels begin to form in the larger oocytes and the
nutritive chambers decrease in size from the base upwards and degenerate, the apical
chamber being the last to disappear. I n the newly moulted adult, not yet emerged from
the host, all that remains of the nutritive cells is a debris of broken-down tissue at the
apex of each ovariole (Fig. 6).
I n females which have emerged from the host egg, the pedicels of the anterior eggs
can be seen extending to the apex of the ovariole (Fig. 7) and the germinal vesicles no
longer show. The follicular epithelium is greatly reduced but may be seen in fresh
dissections around the pedicel of some eggs. After fixing and staining this epithelium
is recognizable as a delicate membrane with flattened nuclei surrounding each egg. By
this time the chorion of the eggs is fully formed. The ovarioles comprising each ovary are
held in place by the peritoneal sheath, and the terminal filaments of the ovarioles
extend to the dorsal part of the abdomen just behind the petiole. I n a female that has
laid many eggs only one egg may be left in each ovariole, but on account of the elastic
nature of the peritoneal sheath the ovary maintains its shape. If all the eggs are laid the
follicle nuclei show up in the depleted ovary.
Number of ovarioles and of eggs
The number of ovarioles varies according to the size of the females. I n the large
mature female the ovarioles are so bunched together that it is very hard to distinguish
their number and this is more easily estimated in the freshly dissected pupa. I n a large
female (a singleton developing in an egg of A. bipustulatus), the number of ovarioles in
each ovary varied from 16 to 20, and from one such female 153 offspring have been
reared. I n large and medium-sized females two to three oocytes and sometimes four
develop in each ovariole. I n the very small females resulting from superparasitism the
number of ovarioles is usually about ten to each ovary. Such ovarioles are comparatively
thick and short and there is rarely more than one oocyte in each and in the pupa the
nutritive chambers are correspondingly reduced in number. In older pupae, 1 mm long,
about 20 eggs have been found by dissection. From a minute adult (0.78 mm long)
which had laid two eggs producing normal males, 20 eggs were dissected and these were
rather smaller in size than the average egg of a normal-sized female. Size reduction thus
results in the production of fewer ovarioles, each with a reduced number of eggs.
The ovarian egg
In the ovaries of a young laying female the eggs are variable in size and the smaller
eggs tend to be situated near the apex of the ovariole (Fig. 7). The largest egg of a female
of normal size measured to tip of pedicel 225 by 52 ,u and the smallest 150 by 30 p. In a
female that had laid many eggs those that remained in her ovaries were of full size, so it
seems likely that the smaller eggs increase in size during the life of the female. Though
the nutritive cells disappear from the ovarioles before laying commences, the growth
of the smaller eggs will take place at the expense of the abundant fat body present in the
abdomen, as Tiegs (1922) found for Nasonia. T h e eggs situated in the ovarioles at the
sides of the ovary tend to be orientated with the convex side outwards (Fig. 7). The
5
DOROTHY
J. JACKSON
66
RN
8-
0.2mm
I
FIGURE
6. Two ovarioles from an ovary of
a young adult removed from the host before the
female was fuuy coloured. Drawn in Ringer’s solution and stained with Trypan red. In the
largest egg in left ovariole, the pedicel is forming and round it the follicular epithelium shows.
PY
Pt
I
0.2mm
FIGURE
7. General view of female reproductive organs and poison apparatusfrom alarge female
emerged from host, showing one ovary, in whichovariolesare not distinguishable.Drawn from
freshly dissected females, but the chitinousparts together with some of the internal organs are
from fixed and cleared preparations of females of similar size.
REPRODUCTIVEORGANS
AND POISON
APPARATUS
OF CARAPHRACTUS
67
general shape of the egg will be seen from this figure and the pedicel end is always
upwards. When dissected unfixed, the ovarian eggs are covered with droplets which
must be held in place beneath the follicular epithelibm. As the latter slips off, the egg
is fully exposed. In such an egg the vitelline membrane-which lies so close to the
chorion that it cannot be shown in Fig. S-extends right into the pedicel, but if the
egg dies the vitelline membrane enclosing the cytoplasm withdraws from the chorion
at the apical end. Ivanova-Kazas (1954) states that there is no yolk in the egg of Curaphractus reductus R. Kors. The micropylar groove opens near the apex of the pedicel
(Fig. 8) being situated on the concave side of the egg when the latter is viewed laterally.
A very fine membrane, remains of the follicular epithelium, shows around the egg
figured. Stains enter the egg first by the pedicel end, presumably by way of the micropylar groove. After passage through the ovipositor, the egg when dissected from the
r-
~
20r
FIGURE
8. Anterior end of fully formed ovarian egg, showing pedicel and micropylar groove.
The concave side of egg is below and a remnant of follicular epithelium shows around pedicel.
host within ten minutes of laying is much more slender than the ovarian egg. The elastic
character of the chorion is shown by the fact that the egg quickly increases in size as the
embryo develops and its convex and concave side can still be distinguished (Jackson,
1961).
In order to ascertain if oosorption occurred when females have no access to host eggs,
dissections were made of old females that had been deprived of eggs for several days
after emergence, but no conclusive evidence was found of oosorption. The length of life
of a female of average to large size when deprived of hosts is at most about nine days, but
in warm weather less than a week. To test the viability of eggs of deprived females, 11
females were used from four to nine days after their emergence. In all the specimens
tested, three virgin and eight mated females, nearly every egg offered was successfully
parasitized. With four females the first egg offered died or escaped parasitism but with
the remaining seven females (including one nine days old before laying) the first egg laid
in yielded up to four adults. When females have been long without hosts it has been
noticed that they may have difficulty in lowering the ovipositor and it is possible that
mechanical injury to the first eggs may occur. There is thus no evidence of lack of
68
DOROTHY
J. JACKSON
viability of eggs of deprived females. The offspring of six of these mated females was
reared to the adult state and totalled 227, with a sex ratio of 23.8 males. This rather high
female sex ratio (Jackson, 1966, Tables VI and IX) is believed to result from the
separate confinement of most of the females with batches of eggs (from 6 to 15 at
one time) as well as from the supply of some individual eggs consecutively for it has
been found that frequent laying increases the proportion of fertilized eggs deposited.
These results contrast with the observations of King (1962) who found that in hostdeprived females of Nasonia vitripennis (Walker) the proportion of males in the
offspring increased. He suggests that this is due to the increase in the number of eggs
undergoing resorption in the ovarioles at the time of oviposition, since he considers
resorbing eggs are less likely to be fertilized.
THE OVIDUCTS
The lateral oviducts, one leading from each ovary, are short and comparatively wide,
the walls having rather deep epithelial cells (Figs 7 and 11, LO). At the point where they
unite to form the common oviduct orvagina two accessoryglands are situated, one at each
side of the junction. They are doubtless homologous with the uterus glands described
by Pampel (1914) for certain Ichneumonidae and he attributes to them a lubricating
function to facilitate the passage of the eggs down the uterus. On account of their shape
in Caraphractus and for brevity of description I have called them the round glands
(Fig. 7, RG). Each gland shows a comparatively thick nucleated wall and a hyaline
intima which is evidently a cuticular lining. These glands will thus be of ectodermal
origin like the vagina. In freshly dissected females the secretion of the glands is homogeneous and stains with Trypan red. If the gland is ruptured the contents flow out.
However, after fixation with Carnoy’s fluid or other alcoholic fixative, the gland contents assume a peculiar lobulated appearance which has been observed both in virgin
and in mated females.
The common oviduct or vagina is a complicated structure. The terminal part, hidden
by the basal sclerites of the ovipositor, is a simple membranous tube extending from
the apices of the rami of the valvulae to its point of discharge in the base of the ovipositor.
The upper part of the vagina, lying in the body cavity, varies in shape depending on
whether it is contracted or extended. If a female dies naturally in water the vagina is
partially extended, and if a female is killed in Carnoy during laying it is seen at its
full extension (Fig. 9). In females killed when not laying it is contracted, rather in the
form of a sigmoid curve, the shorter, narrower, upper part (hidden in Fig. 7 by the
round gland but visible in Fig. 1) lying above the lower part. When viewed laterally
the outer wall (nearest to the ventral side of the gaster) consists principally of comparatively high epithelial cells, probably secretory in function. The inner wall is apparently membranous, and parallel with it a muscle fibre has been observed. The inner
wall is able to stretch greatly to accommodate the egg in transit (Fig. 9) and it is even
more widely distended immediately after mating to serve as a bursa copulatrix as will
be described later. When not laying it would appear that the female must keep all the
muscles contracted so as to bend the vagina upon itself thus making the passage of an
egg impossible. Small muscle fibres have been observed extending from the rami of the
REPRODUCTIVE
ORGANS
AND POISON
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OF CARAPHRACTUS
69
valvulae apparently to the chitinous intima of the round glands. These muscles will be
homologous with the ‘Eileitermuskulatur,’which Fruhauf (1924) records for Diplolepis
( = Rhodites) rosae L. Pampel(l914) also describes a bending of the oviduct in certain
Ichneumonidae so that the second half runs on the underside of the first, and he
discusses briefly the possible muscles involved.
0.08mm
FIGURE
9. Lateral view of vagina with egg about to enter the hidden terminal part of vagina
which lies between the rami of valvulae of either side and is not shown. From a female killed
in Camoy’sfluid during laying. The rami of the right side are shown with cross-hatchedshading
and also the base of the ovipositor.
THE TRANSIT OF THE EGGS TO THE OVIPOSITOR
In order to study the morphology of the vagina and ascertain the position of the egg
in transit, over 30 females were removed to Carnoy’s fluid while in process of laying and
later dissected and mounted. Since the oviposition act usually lasts about two minutes,
sometimes longer, the female was lifted off the egg 13 to 2 minutes after the ovipositor
was inserted. In 14 females the egg was present in some part of the vagina, in two others
in the lateral oviducts and in five it was suspended from the ovipositor.
Never more than one egg was found in transit. The egg descends the lateral oviduct
and proceeds into the vagina always with the pedicel behind, i.e. in the same position
as it occupies in the ovarioles. In the free upper part of the vagina the egg preserves
much of its normal shape, but as it enters the terminal narrow tube its lower end is no
longer rounded but drawn into a point (Fig. 9). As the egg proceeds downwards the
pedicel becomes short and thickened, while the lower end of the egg is greatly drawn out
and narrowed. Once entirely within the narrowed terminal part of the vagina the egg
has become somewhat sausage-shaped, the upper end is completely rounded and the
DOROTHY
J. JACKSON
70
lower end is pointed as it enters the base of the ovipositor (Fig. 10). There is no doubt
that part of the egg contents flow back into the pedicel, as the egg, narrowed in diameter,
reaches the base of the ovipositor, just as described by Chrystal (1930) for the egg
passing into the ovipositor canal in Ibalia. It will be seen from Fig. 10 that the egg in
its downward passage through the narrowed terminal part of the vagina lies close to the
ramus of the second valvula on each side and to the inner rami of the first valvulae. On
OW
PR
T
0.05mm
FIGURE
10. Optical section of lateral view of lower part of vagina and base of ovipositor, showing
an egg passing into the base of the ovipositor, with duct of poison reservoir opening into the
vagina. These parts are only visible by deep focusing being largely covered by the transparent
second valvifer, of which only the posterior edge is shown. From a female killed in Carnoy’s
fluid whilst laying.
the ramus of each second valvula there are near the basal curve, five to six sensilla with
setae situated on the inner surface, and not fully visible in lateral view. On the inner
ramus of each first valvula there are a variable number of minute oval sensilla scattered
in groups over a wide area, mostly concentrated around the curve near the base of each
ramus but extending almost to the tip. There seems little doubt that these sensilla
form part of the sensory equipment involved in oviposition, and they, together with
other sensilla on the basal sclerites of the ovipositor will be described in a later paper.
It is interesting to find that Callahan et al. (1959 (Fig. 7)) figure a similar group of
sensilla in just the same position on the ramus of the second valvula in the imported
fire-ant, Solenopsis saeerissima V. Richter Forel., while Hermann and Blum (1966)
REPRODUCTIV~
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AND POISON
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record sensory pegs on the posterior surface of this ramus in another ant, Paraponera
clavata (F.).
THE BURSA COPULATRIX
Except in newly mated females the bursa copulatrix is most difficult to recognize.
Fifty females have been killed just after mating and, in good dissections, the bursa was
found in those killed within 30 seconds to ten minutes after mating because of its
distension with readily stainable contents, but in one female dissected 15 minutes after
mating it was nearly empty. No spermatophores have been found. The bursa appears
as an extreme dilatation of the inner membranous wall of the vagina. It forms a some-
PR
t
0 08mm
FIGURE
11. Lateral view of one lateral oviduct, the vagina and bursa copulatrix of a female
killed in Carnoy’s fluid three minutes after mating. Semi-diagrammatic;round glands omitted.
Poison reservoir shown in outline.
what pear-shaped membranous sac but is variable in shape, Fig. 1 1 . It extends upwards
nearly to the round glands. In fresh dissections made in Trypan red the contents of the
bursa are cloudy or faintly granular, but in females killed in Carnoy’s fluid the contents
are coagulated into irregularly rounded lumps which stain very strongly with Mayer’s
paracarmine. In two females fixed within one minute of mating slender filaments found
in the anterior part of the bursa are believed to be spermatozoa. Since, as will be shown
later the spermatheca is usually filled with sperm within two minutes of mating, while
the bursa (in fixed specimens) still shows strongly staining matter in females killed up
to ten minutes after mating, it is evident that the bursa contains residual discharge from
the male which later disperses. It is probable that the matter is mucus, for in the male
Caraphractus the mucous glands are comparatively large. Bishop (1920a)states that in
the queen honey-bee after copulation the sperms separate out of the mass of the mucus
and enter the seminal receptacle alone and the mucus is disposed of later, and he considers (Bishop, 1920b) that it is probably absorbed.
72
DOROTHY
J. JACKSON
THE SPERMATHECAL APPARATUS
The spermathecal apparatus consists of the spermathecal capsule in which the sperm
are stored, the spermathecal duct with a rosette-shaped organ at its first sigmoid bend,
and the comparativelylarge spermathecal gland with its own strong walled duct opening
into the spermathecal duct.
The spermatheca is an elongated capsule of characteristic shape which is continuous
basally with the spermathecal duct. In a singleton female from an egg of A. bipustukztus
the sperm capsule measured 69 p by 30 p. It has a strongly marked, rigid, cuticular
intima and narrow epithelial walls which show refringent particles and, after fixation,
scattered nuclei are visible. No muscles have been observed in its walls. The capsule is
FIGURE
12. Spermathecal apparatus of female killed six minutes after mating. Drawn in
Trypan red with spermatozoa still alive. The spermathecal capsule is shown in optical section.
shown in optical section in Fig. 12. The spermathecal apparatus is situated just beneath
the large terminal abdominal ganglion, and is usually to be found between this ganglion
and the upper edge of the poison gland. In Fig. 7 it is shown rather higher up to allow
for the representation of Dufour’s gland which rises upwards from the plane of the
dissection. In a virgin female the spermatheca appears to contain a faintly opaque
greyish white homogeneous fluid.
When living tissues are dissected in Trypan red (pH 8.65) or Ringer solution (pH
8-13)the sperm remain active within the capsule for over two hours under the coverslip. Such specimens have been studied frequently with oil-immersion lens and a
continuous up-pouring of sperm from the base of the spermatheca at the side nearest to
the spermathecal gland is most noticeable, but a corresponding downward movement
at the other side has not been observed. The sperm mostly move in swathes, both clockwise and anti-clockwise. Their position (above the base of the gland) is always changing,
but frequently gives the effect of a figure of eight. Clusters of black dots, the heads of
REPRODUCTIVE
ORGANS
AND POISON
APPARATUS
OF CARAPHRACTUS
73
the sperm, show in different places, at the top end of one swathe, as shown in the figure.
Solitary sperm are sometimes observed in the less crowded areas. The length of one
spermatozoon is judged to be twice the length of the spermatheca. The continuous uppouring of sperm from the base of the capsule is difficult to understand. It occurs not
only in newly mated females but even in those, killed four to five days after mating,
which had laid many eggs. It may be that some sperm are held permanently at the base
of the spermatheca and are there acted upon by inflowing secretion from the spermathecal gland. The sperm thus remain just as violently active in a long mated female as in
one newly mated, but after death, the sperm are to be found packed irregularly within
the capsule and the swathes have disappeared.
The spermathecal gland is larger than the spermatheca and appears in dissection of
living tissue to be lobular but it is fragile and breaks up with the least pressure. It
contains fluid vacuoles of all sizes, some very large. These are the ‘Fliissigkeitsblasen’
of Weber (1954 :78). The secretions from the gland will be collected in the elongated,
somewhat pear-shaped vesicle (the ‘Endblaschen’of Weber) which is very conspicuous
in Caraphractus and narrows to a strongly sclerotized duct opening into that of the
spermatheca. This vesicle and duct persist long after the delicate glandular tissue of
the dissection has disrupted. After fixation, nucleated cells are visible in the gland but
they are not shown in Fig. 12, which is of a fresh preparation.
The spermathecal duct on leaving the spermatheca has a fairly well-defined sigmoid
curve, the first bend, between the base of the spermatheca and the duct of the spermathecal gland being of a pronounced U-shape. The walls of the duct in this area show
transverse thickenings or ridges and, arising from thelower wall of the duct, is a rosetteshaped body of tissue, possibly a sperm-duct gland, which is known to be present in
some insects (Weber, 1933 :479). This organ stains strongly in the central region with
Trypan red, and lines are apparent radiating out from its attachment to the duct. The
peripheral and larger part of this organ is more fragile and usually shows a somewhat
lobulated outline, with red-stained nuclei near the outer edge. I have failed to find
muscular elements in this organ and its contents are not doubly refractile in polarized
light with crossed Nicols. Numerous dissections have been made of females with living
sperm in the spermatheca, but only in one female has any movement of the rosetteshaped organ been observed. This was a newly mated female in which the spermathecal
apparatus was under observation in Trypan red for nearly three hours. Two and a half
hours after mounting, jerky movements of the whole organ were observed repeatedly,
continuing intermittently for 28 minutes, though the sperm after two hours and 23
minutes had ceased to move. In the honey bee the upper part of the sigmoid bend of the
spermathecal duct shows a muscular apparatus which is believed to constitute a sperm
pump (summary by Snodgrass, 1925, 1956). In the eulophid Dahlbominus fuscipennis
Zett., Wilkes (1965) believes that muscles surrounding the loop of the sperm duct
straighten the loop and open the inner spiral thickening of its walls, allowing the passage
of the sperm to the vagina.
The spermathecal duct of Caraphractus becomes membranous after the second bend
and difficultto trace. Itsjunction with the vagina is near the round glands and so adjacent
to the apical part of the bursa copulatrix. Numerous dissections have been made of
newly mated females but no sperm have ever been seen in the spermathecal duct, even
74
DOROTHY
J. JACKSON
in a female examined within two and a half minutes of mating, though the sperm were
then present in the spennatheca. They must pass into the spermatheca with great
rapidity probably in response to chemical stimuli as Kerr et al. (1962) suggest for
Melipona. King (1961) found that with Nasonia vitripennis sperms were present in the
spermathecal capsule less than one minute after mating. In the honey bee according to
Lord Rothschild (1958) it is usually believed that the spermatozoa enter the spermatheca about five and a half hours after copulation. In a short-lived insect like Caraphractus a speedy passage of sperm must be advantageous as the female has been
observed to lay fertilized eggs 12 minutes after mating.
The genital opening
When a female is engaged in laying, a male will frequently try to copulate with her
but never with success. Mating only takes place when the female is standing still, either
under the water or on a dry surface, and when the ovipositor is in a position of rest.
During laying the egg passes into the base of the ovipositor between the rami of the
second valvulae of each side at the point where a prominent spur arises (Fig. 10, 2)
which is part of an extremely complicated ring-like structure. It is near this point that
the penis of the male makes contact with the vagina of a receptive female but a full
account of the surrounding skeletal parts will be given in a later paper.
THE POISON APPARATUS
This is the name applied by some writers to a group of organs widely present in
Hymenoptera. As will be discussed later, it is by no means certain that in all forms such
organs function as a poison producer but for convenience of description the term will
be adhered to. This apparatus, as is well known, consists of two groups of organs, the
acid gland or poison gland (of most diverse shape in different genera), its reservoir and
duct, and the ‘alkaline’ gland or Dufour’s gland, a tubular organ with a duct opening
like that of the acid gland at the base of the ovipositor.
The acid gland or poison gland is well shown both in the late pupa and in the adult of
Caruphructus. It consists of a number of comparatively large nucleated cells and in
general appearance the gland is like a compact bunch of grapes (Fig. 13). The secretion
from each cell is collected in a minute elongated vesicle or alveolus in each cell, and the
vesicles are continuous with extremely fine, long ducts which unite to form a common
duct entering the distal part of the reservoir. The poison gland of Curaphractus has the
same structure as the ‘Driisenpaket’ described by Weber, 1954: 80, and illustrated
(Fig. 57 b). The gland is large and deeply staining in the newly emerged adult, but it is
reduced in size in a female that has laid many eggs.
The poison reservoir is sac-like and is situated with its proximal end near the base of
the ovipositor (Figs 7 and 13). Its wall consists of a very narrow epithelial layer with
elongate nuclei and an elastic chitinous intima. No muscles have been seen in the walls
of the reservoir either in sections or in whole mounts. Its contents are liquid and pour
out if the wall is broken. In the pupal stage the reservoir is smaller than in the adult and
transversely wrinkled; it is of large size in a newly emerged female ready to lay or in an
old female deprived of hosts. In a female that has laid many eggs it is appreciably
REPRODUCTIVE
ORGANS
AND POISON
APPARATUS
OF CARAPHRACTUS
75
reduced in size due to the contraction of the intima. Hermann & Blum (1966) record
a similar variation in size of the poison sac according to its fulness in the ponerine ant
Paraponera clavata F. In unfixed females of Caraphractus,the contents of the reservoir
are homogeneous, but in specimens fixed in Carnoy’s fluid and stained with Mayer’s
paracarmine, the contents, deeply stained, may be pushed back from the wall of the
reservoir and from its duct, but preserve the same contour, so that the appearance is of
an inner cuticle containing the coloured matter, while the space between it and the
actual wall is colourless. No double contour shows in fresh specimens, but as the
Carnoy’s fluid enters the reservoir the contents will be pushed back from the wall and
coagulated. Bucher (1948) observed in the chalcid, Monodontomerus dentipes Dalm., a
coagulation of the venom in the poison sac on coming in contact with alcohol. It is not
1
0.00 mrn
FIGURE
13. Poison gland and reservoir of a young female extracted from host egg. Fixed
Camoy’s fluid.
clear how the contents of the reservoir are pushed through the duct, but during laying
there is much movement in this area and dissections show that on either side of the
poison reservoir oblique muscles extend from the dorsal margin of the ninth tergite to
the upper edge of the second valvifer and it seems possible that during their activity
they may also compress the reservoir.
The duct ofthe reservoir is very short (Fig. 10). It is slender and curved and opens into
the narrowed terminal part of the vagina at the base of the ovipositor. The duct has the
intima thickened especially on the lower side and it shows up well after treatment with
caustic potash.
Dufour’sgland is strongly developed in Caraphractus and relatively large (Figs 7 and
14). It is widest at the distal end and narrows towards the duct. In a fresh dissection
it is, after the ovaries, one of the first organs one recognizes as it floats upwards as
though buoyant, unless it has been punctured. It is more difficult to find in fixed
preparations. Hermann & Blum (1966) record that Dufour’s gland in the ant, Paraponera clavata (F.)contained a yellowish fluid which floats on water in the form of small
droplets. I n Caraphractus,under an oil-immersion lens, the very thin epithelium of the
walls can be seen. Just at the commencement of the duct the epithelium is enlarged into
an oval swelling over a slight angular widening of the walls (Fig. 15). The duct is very
long and narrow. It curves round the end of the poison reservoir adjacent to the terminal
76
DOROTHY
J. JACKSON
part of the vagina and goes towards the base of the ovipositor but its actual opening has
not been traced. The most noticeable feature of Dufour’s gland is its extreme buoyancy
and such fluid as it contains must be lighter than water and probably of fatty nature as
Blunck (1951) observed in Hemiteles simillimus Tasch. From the narrowness of the duct
in Caraphractus very little fluid could pass along it during laying. In making camera
lucida drawings of this gland it has been noticed that it varies in size in females of similar
size. In Fig. 7 the largest one has been illustrated.
0.08rnm
FIGURE
14. Dufour’s gland from an unfixed female.
3OP
FXCURE
15. Glandular swelling at commencement of duct of Dufour’s gland, from an unfixed
female.
DISCUSSION
In Caraphractus the polytrophic nature of the ovaries is only evident by studying the
ovarian development in the pupal stages. In the emerged female of normal size many
eggs ready to lay are present in the ovarioles. This type of oogenesis, termed proovigenic by Flanders (1950), ensures the production of a large number of eggs during
the short life of the female. The Caraphractus female has never been seen to feed and
spends most of its life under water searching for eggs of Dytiscidae. A similar type of
ovarian development has been described by Seurat (1899) for the braconid Doryctus
gallincs Rheinhard, which has also a quite short adult life without taking any food.
In Caraphractus the female has remarkable control over the number of eggs she
deposits and usually avoids laying in eggs already parasitized (Jackson, 1966). If a
female is provided with only one or two small hosts, such as the eggs of Agabus bipustuZatus, she dies with her ovaries full of eggs. There is no provision for storage of eggs in
the oviducts as Simmonds (1956) found for another chalcid Spalangia drosophilae
A s h . It is difficult to understand how the eggs are prevented from passing into the
lateral oviducts when the ovarioles are full of eggs and no suitable hosts are available.
No resorption of eggs has been observed in this insect such as occurs in those species
REPRODUCTIVE
ORGANS
AND POISON
APPARATUS
OF CARAPHRACTUS
.
77
termed synovigenic by Flanders (1950) in which oogenesis is more or less continuous
throughout life.
From dissections of females fixed in Carnoy’s fluid when not laying it has been found
that the vagina is bent upon itself, but when the female is killed during laying the
vagina is extended (Fig. 9). The control of egg deposition is primarily under control of
the nervous system. It is not the lowering of the ovipositor and its insertion in the host,
though involving intense muscular activity, that triggers off the release of the egg, for
if the host is infertile or in an advanced state of parasitism the ovipositor is promptly
withdrawn without depositing an egg. The female has to be satisfied that the host is
acceptable to lay in before an egg is released and this can only be as a result of nervous
stimuli received from the ovipositor. It is suggested that these nervous stimuli are
transmitted to the round glands causing them to secrete into the vagina a lubricating
fluid inducing the downward passage of the eggs. During one insertion of the ovipositor
two to three eggs are most usually laid. On withdrawal of the ovipositor, as soon as
another suitable host is found, the whole process is repeated, but in a large host like a
Dytiscus egg the female merely moves to attack it at another point.
While no cytological investigation has been made of Caraphractus it is assumed that,
as in species of Opius studied by Genduso (1964), the males will be haploid and the
females diploid, and that the sex of the offspring will depend on whether or not the egg
has been fertilized during laying. In a mated female the passage of an egg into the vagina
must bring about the release of one or more sperm from the spermatheca. As Flanders
(1939) pointed out if the presence of an egg in the vagina alone caused discharge of the
sperm all of the eggs of a female would be fertilized and this is not the case and would,
of course, be fatal to the species. The spermathecal apparatus lies just beneath the large
terminal ganglion and it is believed that the female has some control over the number of
sperm discharged. This has been suggested by experimental work (Jackson, 1966)since
it was found that the female lays more fertilized eggs in a large host or in a quick
succession of small hosts. Moreover when a small host (in the experiments the eggs of
Agabus bipustulatus) is encountered after a long interval, the high proportion of hosts
from which one male and two females emerge can hardly be a matter of chance (Jackson,
1966, Table VIII). This sex ratio must be of great importance to survival when hosts
are widely scattered. The eggs of the large species most commonly parasitized, Dytiscus
marginalis L., are available only during spring and early summer and in these eggs
females predominate with just sufficient males to ensure mating. The winter diapause is
spent mostly in the eggs of A. bipustulatus. It is believed that in Caraphractus a pattern
of sex ratio has been evolved under control of the nervous system of the female which
is most advantageous to the survival of the species both in large and in small hosts.
The poison apparatus of Caraphractus shows all the organs described for other
parasitic Hymenoptera, but the poison gland instead of consisting of one or more long
tubes is a compact organ, rounded distally and opening by a duct into the larger poison
reservoir. Dufour’s gland is very well developed. The poison apparatus is so called
because in many entomophagous Hymenoptera it is known to cause the paralysis or
death of the host. Hase (1924) and Beard (1952) found that the paralysis of the host
caterpillar was caused by the potent venom injected by Habrobracon juglandis
Ashmead. Ratcliffe & King (1967) have shown by experiment that mortality in puparia
78
DOROTHY
J. JACKSON
of Calliphora spp. is induced by an injection of venom from the acid gland of Nasonia
oitripennis, and much of the literature on the venom system of the Hymenoptera is
referred to by these writers. Not in all entomophagous species in which the poison
apparatus is present is it known to have an injurious effect upon the host. Thus Subba
Rao & Sharma (1962) find that Aphidiinae do not paralyse their hosts for egg-laying
and they suggest that the poison apparatus may subserve some other function.
In various phytophagous Hymenoptera such as the Cynipidae which produce plant
galls, the ovipositor and poison apparatus are well developed, and Fruhauf (1924)
suggests that the poison glands act as cement glands to facilitate the passage of the eggs
through the ovipositor and to fasten them in the plant tissue. Imms (1957) also considers
that the fluid injected by Cynipidae during oviposition is a lubricant and that the galls
are produced by reactions of the plant tissues induced by the living larvae. James (1926)
finds a well-developed poison apparatus present in the chalcid Harmolita (Isosoma)
graminicola (Giraud), which makes galls on couch grass. In the fig insects Joseph (1956)
states that the acid gland secretion of Bhtophagapsenes L. produces a cellular multiplication in the ovaries of the fig and it is interesting to find that in another phytophagous
species, Philotrypesis c&ae L. which is unable to form a gall but lives in the gall
formed by Blastophaga, the poison glands are atrophied (Joseph, 1955). Atrophy of the
poison glands and disappearance of the poison sac in the workers of certain stingless
bees is recorded by Kerr & Lello (1962) and they state also that Dufour’s gland has
completely disappeared in the Meliponini as no adhesive covering is necessary for their
eggs. Pampel (1914) observed that Dufour’s gland is absent in the majority of
Tryphoninae in which the eggs do not pass down the ovipositor.
From the above brief summary of some of the literature it is evident that the secretions of the poison glands have varied functions in different insects and that in some
forms parts of the apparatus may be atrophied. Since in Caraphractus the whole poison
system is well developed one would expect it to serve some purpose. Paralysis is ruled
out, for if an Agabus egg containing an embryo is parasitized, the embryo continues to
develop for several days after the egg has been deposited in it (Jackson, 1961). Moreover this mymarid will not parasitize an egg with a larva ready to hatch, but either
ignores it or rejects it with a prick of the ovipositor. Marchal(l936) states that the egg
of the tortricid Cacoecia rosana is killed by Trichogrammacacoenae at the moment that
the egg is pierced for laying or shortly afterwards. This does not happen in Caraphractus
as even a newly laid egg continues to develop after parasitism until it is destroyed by the
Caraphractus larvae within it.
The ability of the female to distinguish between parasitized and unparasitized eggs
by pricking them with her ovipositor suggested that a secretion from the poison
reservoir deposited with each egg laid and perhaps serving also as a lubricant, might
render the host egg unacceptable to another female (Jackson, 1966). At the time this
was written it was not known that Wylie (1965) had put forward a similar idea in regard
to Nasonia vitripennis and he considered that an internal injury to the host by the
ovipositor was also possible. The habits of the two insects are widely different, but in
Caraphractus it has been found that it is not the penetration of the ovipositor into the
egg which renders the host unacceptable to another female, but only the deposition of
an egg (Jackson, 1966: 34).
REPRODUCTIVE
ORGANS
AND POISON
APPARATUS
OF CARAPHRACTUS
79
If a repellent substance is injected into the host during ovipositionthe question arises
if it can act interspecifically as well as intraspecifically. Caraphractus cinctus and the
eulophid Mestocharis bimacularis (Dalman) both parasitize eggs of Dytiscus marginalis
L. (Jackson, 1964). It was observed that females of Caraphractus oviposited in eggs of
Dytiscus which had been parasitized 24 hours previously by Mestocharis and, when one of
these eggs was dissected two days later, six Caraphractuseggs were found, all developing
normally, and ten small Mestocharis larvae. From the remaining eggs only Mestocharis
developed as the Mestocharis larvae survive in competition. While these few experiments indicate a failure on the part of Caraphractus to discriminate against parasitism
by the eulophid, the Dytiscus egg is a large host for the mymarid and it is not known how
many eggs or young larvae of its own species have to be present for discrimination to
take place (Jackson, 1966:33). The Mestocharis female was also observed to show some
discrimination and restraint in laying in Dytiscus eggs already parasitized by its own
species and it took no interest in eggs containing half grown or full grown larvae of
Caraphractus.
Evidence of a certain degree of interspecific discrimination has been recorded by
Lloyd (1940) and Fisher (1961) for other parasitic Hymenoptera. Thus Lloyd found
that Diadromus collaris Grav. showed discrimination of host prepupae of Plutella
maculipennis Curtis containing young larvae of another ichneumonid, Angitia
(Horogenes)cerophaga Grav., by inserting the ovipositor into the host and then quickly
withdrawing it, just as the Caraphractus female does with Agabus hosts containing
eggs, larvae or pupae of its own species. It is interesting to find that with hosts containing
living adult Caraphractus, the female often rejects them after only a brief antenna1
examination. It is in the earliest stages of parasitism that the ovipositor in its probing is
most likely to be repelled by an injected liquid ;later on, the presence of the developing
parasites may itself initiate rejection.
In such a small female as Caraphractusin which the length of the gaster in an average
sized individual is little more than 0.5 mm it is impossible to dissect out the acid gland
with its reservoir and Dufour’s gland and to use them for experimental work. This has,
however, been done for the fire-ant Solenopsis saevissima Fr. Smith by Wilson (1959,
1962) who found that Dufour’s gland is responsible for the odour trail produced by this
ant, while Moser & Blum (1963) discovered that in the Texas leaf-cutting ant, Atta
texana Buckley, it was the true poison gland which produced the trail pheromone. In
Caraphractusthe ducts of both the acid gland and Dufour’s gland lead to the base of the
ovipositor and it is suggested that while the secretion of one or of both glands doubtless
serves as a lubricant to facilitate the passage of the egg down the ovipositor, some
specific ingredient-a pheromone-is incorporated in the secretion and deposited with
each egg laid. This substance must diffuse rapidly through the host for an egg of A g a h
has been rejected within a minute of the first oviposition, and it will render the egg
unacceptable to all but novice females and experienced females long deprived of hosts.
ACKNOWLEDGEMENTS
I have pleasure in acknowledging my appreciation of the help given me by Dr Colin
Muir of the Department of Zoology, St. Andrews University, throughout this investigation and I am also grateful to him and to Dr M. E. R. Lang for their kindness in
80
DOROTHY
J. JACKSON
preparing sections for me. Mr G. J. Kerrich has most kindly read through the typescript of this paper and I greatly appreciate his helpful comments.
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KEY TO FIGURE LETTERING
BC, bursa copulatrix
DG, Dufour’s gland
FM, furcal muscle inserted on spur of second
valvula
IR, inner ramus of first valvula
IW, inner wall of vagina
LO, lateral oviduct
NC, nutritive chamber with nutritive cells
0, oocyte
OR, outer ramus of 1st valvula
Ov, ovipositor
OW, outer wall of vagina
P, petiole
PG, poison gland
PR, poison reservoir
PS, peritoneal sheath
Pt, proctiger
PY,PYgostYle
RG, round gland
6
RN, remains of nutritive cells
RO, rosette organ of spermathecal duct
RS, ramus of second valvula
SLII, third sternite
Sp, spiracle
Spt, spermatheca
SptD, spermathecal duct
SptG, spermathecal gland
T 111, T IX, third and ninth tergites
TF terminal filament
V, vagina
V13,third valvula
Vlf 1, Vlf 2, first and second valvifers
WO, wall of ovariole
X, lower edge of second valvifer
Y, thickening with sensilla on lower edge of
second valvifer
Z, spur of second valvula