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EMBRYOLOGY / ONTOGENY / ANATOMY
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Prenatal Development in Hymenoptera
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Common Egg Shapes in Parasitoids |
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Overview Embryology concerns the origin and
development of the definitive individual organism. Development here is
characterized by cumulative progressiveness in which the significance of each
component process and result is viewed against what precedes and what follows. The embryo is a forming individual
which at all stages of development is adequately provided as to its needs and
environment. Most advances achieved at any period anticipate functions that
appear later. Developmental stages, therefore, contrast with the recurring,
non-progressive, physiological changes that are concerned solely with the
maintenance of life. Embryological development is often
divided into two parts by the incident of birth or hatching: (1) the prenatal
part and the post-natal part. Earlier work in embryology
characteristically focused on prenatal development. Modern concepts consider
post-natal development, although not usually as dynamic, of equal importance.
The embryology of the individual and all subsequent developmental events is
called ontogeny. Early Stages of Ontogeny Organization of the
Ripe Egg.--The ripe egg possesses polarity
or axiation in which there are two poles: the animal and vegetal,
and a main axis connecting them. The animal pole is that end of the egg
which was most active in physiological exchange during oogenesis. The ripe egg is bilaterally
symmetrical. Among the innumerable planes that could divide the egg into
physiological halves, only one finally dominates. Such planes are not
equivalent, however. Eggs are not homogenous, there being a
greater concentration of pure protoplasm at the animal pole. Reserve
materials (yolk) favor the vegetal pole. The internal portion differs
from the gelatinous surface in being semifluid; and the size of the mature
embryo can be reduced by ligaturing the newly deposited egg so that one-third
of the protoplasm is not used. Development of the Egg.--Ripe eggs
undergo aging among some species, resorption in others, and a combination
of both in others. In the Hymenoptera aged eggs may be deposited prior to
resorption and develop either into male or female progeny depending on the
kind of parthenogenesis. In some cases eggs may hatch within the mother,
which kills her. The sate of meiosis at oviposition will vary. Cleavage.--Cleavage is
the subdivision of the one-celled egg into smaller building units
called blastomeres. Such subdivisions are always mitotic. Each
division results in a reduction in size of ensuing blastomeres. The total
mass of living substance available at the start is not increased appreciably
when cleavage is finished. Among most arthropods, the ova are centrolecithal
where the yolk is massed centrally and surrounded by a peripheral shell of
cytoplasm. Cleavage occurs only in the peripheral region and is termed superficial.
Some endoparasitic Hymenoptera and the Collembola that have little yolk (isolecithal)
show total cleavage. Gastrulation.--Gastrulation
is the process through which the three germ layers are formed: the ectoderm,
mesoderm and entoderm. The various germ layers produce the body organs and
other specialized parts. Segmentation.--is also
characteristic among insects. Prenatal Development
in Hymenoptera Specifically Egg orientation is similar among all
Hymenoptera studied. It follows Hallez' law
of orientation (Hallez 1886) within the polytrophic ovariole. The anterior
pole is directed toward the head of the parent female. However, during
oviposition, the posterior pole emerges first, which permits regulation of
fertilization. The dorsal, ventral and lateral sides vary within the same
individual. The embryo remains in the original cephalocaudal axis during the
entire development, but just before eclosion it rotates 180B on the longitudinal axis. The yolk components are called deutoplasm.
Included are protein yolk bodies, lipid yolk bodies and glycogen particles.
Some Chalcidoidea lack yolk altogether. Cleavage usually begins one or two
hours after the egg is laid. Some exceptions are cases where eggs even hatch
inside the mother. The duration of cleavage varies, but generally it is
finished after six to eight hours at room temperature (23BC). Gastrulation occurs in diverse ways
among the Hymenoptera, and differs in different species of the same family.
The duration appears to range from seven to twelve hours. Segmentation occurs early in
development in some Hymenoptera, and later in other species. The duration is
variable. Regarding embryonic envelopes, there
are two membranes, the serosa and amnion, that usually envelop
insect embryos. However, in the Hymenoptera, one or both may be rudimentary
or entirely lacking. Embryonic envelopes function both in protection and
nutrition, and usually occur well developed in species with little yolk. Eggs
with little yolk are usually minute when deposited in the host. Then,
probably by osmosis or active absorption of host fluid, they gradually become
larger (Imms 1931, Simmonds 1947). Expanding eggs of this type have been
called hydropic eggs (Flanders 1942a). Flanders (1942d) found in Coccophagus
capensis Compere, that only the fertilized egg produced a trophic
membrane. Membranes are known by various names.
Hagen (1964) stated that during eclosion when the trophamnion is
broken and cells of the membrane float free in the host's haemolymph, these
cells increase in size proportional to the growth of the larval parasite;
they become greatly enlarged while retaining their trophic function because
the larva feeds upon these cells (Jackson 1928, O. J. Smith 1952). Host nutrition
influences the development of these cells and in turn influences the
parasitoid larva. Some membranes persist, covering the larva. For example,
the chorion may remain intact until after first larval ecdysis (Flanders
1964). Formation of entoderm, mid-gut,
stomodaeum, proctodaeum, gonads, head, abdominal and thoracic appendages,
dorsal closure, mesoderm and ectoderm, is discussed by Bronskill (1959). Hatching of the egg usually occurs when
histogenesis is complete. Exceptions are cited by Ivanova-Kazas (1948-58).
First-instar larvae of many endoparasitoids are precociously emerged embryos
(protopod larvae) such as Platygaster (Imms 1931). Eggs with embryos can be deposited when
partially or completely incubated only through the copulatory pore. The larvae,
upon hatching, commence to feed. Completely incubated eggs do not always
hatch immediately and may overwinter in the completely incubated condition.
Hatching in ectoparasitoids may require a relative humidity of over 90% and
under 100% at the egg site (Gerling & Legner 1968 ). Specific host
organs may serve as oviposition sites, and egg chorions may be variously
coated to avoid encapsulation in the host (Flanders 1934). Egg Size and Shape.--Eggs can reveal
important information about the taxonomic groups of the organism which
develop them. A survey of eggs within the Insecta shows they are variable in
terms of number and size and plastic in terms of shape (Hinton 1981).
Nevertheless, these characteristics are typically stable at the species level
and frequently constant at the family level. This constancy at one taxonomic
level pitted against variability at another creates an interesting blend of
features which can be informative in terms of classifying insects and
understanding their biologies. Parasitic insect eggs express variation in
terms of size and shape. This variability is in part a consequential artifact
of the enormous number of taxa involved and in part generated by the biology
and developmental requirements of the insect embryos contained in these eggs.
The variability in size and shape partially reflects a compromise between
needs of the developing embryo and problems associated with oviposition. The primitive nomenclature and early
literature associated with the shapes of parasitoid eggs was characterized by
Clausen (1948), reviewed by Hagen (1964), and summarized here. That schema is
briefly discussed here, but research on egg morphology of the Insect during
the past 20 years has shown that shape of the egg alone is not diagnostic and
unrelated taxa share identical shapes. With the application of scanning
electron microscopy it is now apparent that chorion morphology, eggshell
complexity and micropylar position, number and configuration are all equally
important features which must be described, studied and understood.
Collection of this kind of information is tedious, time consuming and
expensive. Moreover, the number of taxa for which egg anatomy must be
collected is very large if we are to obtain an accurate picture of parasitoid
biology. Egg biology and morphology has obviously lagged considerably behind
other pursuits involving parasitic insects. Common Egg Shapes
in Parasitoids.--Most of the
names for egg shapes used by Pantel (1910) for his study of the Tachinidae
were subsequently adopted for other groups of insects. These are briefly
reviewed: Acuminate eggs are characteristically long, narrow and generally adapted
for extrusion from the long ovipositor of parasitic Hymenoptera which attack
insects that form galls or live in galleries and tunnels. This kind of egg
has been described for some Ichneumonoidea and Chalcidoidea. Encyrtiform eggs are
unusual in that they change shape after oviposition. Inside the ovary they
are typically shaped as two spheres connected by a stalk. After oviposition
one bulb collapses and the egg appears stalked. All encyrtiform eggs are
deposited internally with the collapsed sphere projecting from the stalk
outside the body of the host. An aeroscopic
plate, used for embryonic and larval respiration, usually is found on the
stalk and sometimes projects onto the body of the gg. This type of egg is
characteristic of the Encyrtidae, but more recently has been reported in the
Tanaostigmatidae (LaSalle & LeBeck 1983). It has not been found in the
Eupelmidae, a family considered close to the Encyrtidae. The Hymenopteriform egg may be
viewed as the hypothetical ancestral form or the generalized type. Its shape
is typically sausage-like with rounded poles and whose body is several times
longer than wode. This is the generalized egg form expressed by Hymenoptera
and it is also found in some Diptera (Nemestrinidae, Bombyliidae,
Cecidomyiidae). A Macrotype egg was
proposed by Pantel (1910) for large eggs with a thick, opaque dorsal surface
and thin, flat and transparent ventral surface. Macrotype eggs are oblong in
dorsal aspect and semicircular in lateral aspect. Surface features which may
be present include a flange margin for the ventral surface, and spumaline for
adhesion to the host. Macrotype eggs typically have an extensive chorionic
respiratory system. Macrotype eggs are restricted to the Tachinidae and were
subdivided into dehiscent and indehiscent forms. The Membranous egg is variable
in size but the chorion is thin, transparent and appears membraous. The
surface reticulation pattern and pliancy provide an impression of membrane.
This is an egg typically ejected from the female which contains a mature
embryo which is ready to emerge. Eclosion occurs soon after oviposition. Eggs
are often glued to the host and site specificity has been suggested. The
distinction between macrotype and membranous eggs is sometimes lost. This egg
shape is representative of Diptera (Tachinidae, Sarcophagidae). Microtype eggs are
typically minute, variable in shape, with dorsal and lateral surfaces thick
and dark, ventral surface thin and membraneous. Embryonic development occurs
in the uterus. This egg type must be consumed by the host if development is
to proceed, but the stimulus for hatching is unknown. Microtype eggs are
widely distributed among the Tachinidae. The Pedicellate egg is an
apparent variation of the stalked egg in which one end is modified to anchor
the egg to the integument or seta of the host. Most pedicellate eggs are deposited
externally on the host, but a few are internal and attached to the host via
the ventral surface of the egg. The pedicel may originate from the stalk,
from the body of the egg or from a modified micropylar structure. This form
of egg is widely distributed among parasitic Hymenoptera, including
Chalcidoidea, Ichneumonoidea and Diptera (Cecidomyiidae, Conopidae,
Tachinidae). Stalked eggs are
elongate with a constricted stalk-like projection from the one or both of the
poles of the body of the egg. The stalk is of variable length, sometimes
corkscrew shaped, and often several times longer than the remainder of the
egg. This type of egg is found in some Diptera (Pyrgotidae) and most of the
major superfamilies of parasitic Hymenoptera, including the Chalcidoidea
(most families), Chrysidoidea, Cynipoidea, Evaniioidea, Ichneumonoidea and
Proctotrupoidea (most families). Polyembryony in Entomophages Polyembryony representes a form of
asexual reproduction in which many embryos develop from repeated division of an
egg or zygote. The phenomenon has been reported in several groups of insects,
including the Coleoptera and Hymenoptera. Among the parasitic Hymenoptera,
polyembryony is known in the Braconidae, Platygasteridae, Dryinidae and
Encyrtidae. Cruz (1986b) described in detail the development of Copidosomopsis
tanytnemus Caltagirone, and egg-larval parasitoid of the Mediterranean
flour moth, Anagasta kuehniella (Zeller). Because of its curiosity, polyembryony
has been extensively studied. It was first described by Marchal (1898, 1904)
and Martin (1914). Other examples are Daniel (1932), Doutt (1947, 1952), Imms
(1931), Kornhauser (1919), Leiby (1922, 1929), Leiby & Hill (1923, 1924),
Marchal (1898, 1904, 1906), Martin (1914), Paillot (1937), Parker (1931),
Patterson (1915, 1917), Silvestri (1906, 1923, 1937). The generation time in polyembryony
varies from several weeks to almost a year. Embryo development begins just as
in monoembryony. Polar nuclei, however, do not enter directly into the
blastula stage, but produce an embryonic membrane called the trophamnion
which surrounds the developing embryo-like area. The trophamnion extracts
nutrients from the host haemolymph. The embryo then divides into small groups
of cells called morulae enclosed by the trophamnion.
The trophamnion then changes into a chain-like structure with the morulae
arranged in a row or branching cluster. This finally breaks up and separate
embryos are formed. The number of embryos from a haploid egg equals one-half
that from a diploid egg. Examples are reported from Litomastix (Copidosoma)
koehleri (Blanchard) (Doutt 1947, Flanders 1942). Polyembryony has been considered a
process which restores a nucleocytoplasmic balance which is upset by osmosis
of the host cytoplasm through the chorion. Perhaps more interesting from the
viewpoint of parasitoid bioloty is the examination of polymorphic larvae
within C. Tanytnemus by Cruz (1981, 1986a). It was shown that
precocious larvae represent a so-called "defender morph." The
defender morph is characterized by a well developed head, mouthparts and high
motility. This morph attacks and kills or injures the larvae of competing
internal parasitoids. The number of larval instars found in
Hymenoptera is variable, but five seems to be most common. The Aphelinidae,
however, possess three instars and the Encyrtidae are variable. The number of
mandible sets are the best evidence for instars. Larval dimorphism may occur within the
same instar, and sexual dimorphism is often striking. The most distinctive
parasitic stage in the life cycle is the primary or first-instar larva (protopod larva). Various methods of locomotion are found
from slug-like to jumping. The fastest locomotion is characteristic of those
species which lay their eggs apart from the host (Clausen 1976). Larvae are also variously protected,
the greatest protection being in the form of spines, plates, etc., which are
characteristic of the more exposed larvae. Strong mandibles are found in
species that show aggressiveness between the larvae (Salt 1961). These care
characteristically endophagous forms. Other species protect themselves by
producing a cytolytic enzyme (Thompson & Parker 1930, O. J. Smith
1952, Salt 1961, Gerling & Legner 1968 ). [e.g., Lounsburgia on
black scale ]. Larval Feeding.--Egg parasitoids and other endophagous species are
thought to absorb much of their food through the cuticle. Observations on
ectophagous parasitoids (Gerling & Legner 1968 ) show a
peculiar type of lacerating-like feeding in which the mandibles are used only
for rasping followed by an imbibing of oozing fluids from the host. Such
feeding wounds heal rapidly, causing the parasitoid larva to move to other
feeding sites. Different instars prefer to congregate on different body
regions (Gerling & Legner 1968 ). Similar feeding marks are also
found on synthetic parasitoid diets (S. N. Thompson, pers. comm.). Larval Respiration.--First-instar
larvae exhibit the greatest diversity in respiration (Clausen 1950).
Endophagous larvae either respirate through the integument or obtain air from
the outside of the host through tube-like mechanisms (a membranous cocoon
attached to the host's tracheae). The final instar may possess a completely
different spiracle arrangement and number (Hagen 1964), while early instars
may lack spiracles altogether. Larval Anatomy.--Several
distinctive larval forms are found in parasitic insects: Eruciform larvae are shaped like a caterpillar. Anatomically they are
characterized by a well developed head capsule, thoracic legs and abdominal
prolegs. The eruciform larva is seen in Lepidoptera and Symphyta. It
represents the ancestral type for Hymenoptera larvae, and presumably the form
from which other types evolved. The Hymenopteriform larva represents the generalized larval form
seen in apocritous Hymenoptera. Characteristically the body is spindle-shaped,
without thoracic legs, featureless with pale to translucent integument and
the head capsule is weakly developed of absent. The Mandibulate apocritous
larva has a sclerotized, unusually large head, large falcate mandibles and a
body that is tapered posteriad. It is found in endoparasitic and
ectoparasitic species. Caudate apocritous
larvae have a specialized body characteristically segmented, with long
flexible caudal appendages. The function of caudal appendages has not been
established, but sometimes they are progressively reduced in later instars
and lost in the last instar. The caudate form is displayed by some
endoparasitic ichneumonid larvae. The Vesiculate apocritous
larva has the proctodaeum everted, and displays short caudal appendagtes with
vesicles at the bases. It is found in some endoparasitic Braconidae and some
Ichneuumonidae. Mymariform apocritous
larvae display a head and caudal end each bearing a conical process anterad.
The abdomen of some species is segmented. The larval form is found in
Mymaridae and Trichogrammatidae. The Sacciform apocritous larva is ovoid, featureless and without
segmentation. It is found in Dryinidae, Mymaridae and Trichogrammatidae. The Polypodeiform (cf.
vesiculate) apocritous larva is endoparasitic, segmented with paired, short
flexible projections from thoracic and abdominal segments. It occurs in
Cynipoidea and Proctotrupoidea. Hypermetamorphosis.--This is found
in some endopterygote insects whose larvae change form, shape or substance
during successive instars as a normal consequence of development. Examples
are found in, but not restricted to, Coleoptera (Meloidae), Strepsiptera,
Diptera (Acroceridae, Bombyliidae), Lepidoptera (Epipyropidae), and
Hymenoptera (Eucharitidae, Perilampidae). The Teleaform apocritous
larva is hypermetamorphic (e.g., Scelionidae: Proctotrupoidea) and
unsegmented, weakly cephalized with prominent protuberances or curved hooks
at the cephalic extremity. The body is posteriorly prolonged into a caudal
process which has one or more girdles or rings of setae around the abdomen. Cyclopoid larvae are
hypermetamorphic, endophagous Hymenoptera, (e.g., some Proctotrupoidea). It
is characterized by a large swollen cephalothorax, very large sickle-like
mandibles and a pair of bifurcate caudal processes. The larva resembles the
nauplius larva of crustaceans. Planidium is the
hypermetamorphic, migratory, first-instar larva of some parasitic insects.
Morphologically it is characterized by a legless condition and somewhat
flattened body which often displays strongly sclerotized, imbricated
integumental sclerites and spine-like locomotoray processes. The term most
appropriately is restricted to Hymenoptera (Euchartiidae, Perilampidae and
some Ichneumonidae) and Diptera (Tachinidae). It is incorrectly used
interchangeably with Triungulin (Heraty & Darling 1984). Eucoiliform larvae are
found in apocritous Hymenoptera which are hypermetamorphic (e.g.,
Eucoilidae). The primary larval form displays three pairs of long thoracic
appendages but lacks the cephalic process and girdle of setae of the
teleaform larva. Subsequent instars display a polypodeiform larval form. It
has also been found in Charipidae and Figitidae. Prepupa.--This stage
begins when the last larval instar ceases to feed, voids meconium and shows
scarcely any external movement. Rapid changes take place throughout the body.
Although this is often referred to as a resting stage, it is by no means a physiological resting time! The length of time
that it takes prepupae to form differs within the same species or can
occur simultaneously for eggs deposited in a 24-hr period (Gerling &
Legner 1968
, Legner 1969). The linking
of the mid- and hind guts begins when the last larval instar is fully-fed,
and is completed at the prepupal stage. Prepupae usually remain for less than
24 hrs, and the meconium is shed either freely in pellets, or encased in a
peritrophic sac (Gerling & Legner 1968 ). In some species the meconium
is discharged only when adult (e.g., Trichogramma). Meconia may serve
to identify the species (Flanders 1942b). Pupa.--Most
hymenopterous parasitoids that pupate in the relatively dry remains of the
host do not spin cocoons; the fully-fed endophagous larvae while immersed in
host fluids can, however, construct membranous cocoons. Similar cocoon-like
structures are found between gregarious (polyembryonic) pupae [an exception
is Diversinervus smithi]. The length of the pupal stage can be
variable or remarkably equal among the progeny of one female/day (Legner 1969). Rate of Development.--The overall rate
of parasitoid development is known to be affected by host density, and
usually accelerates with a higher average density of the host (Legner 1969,
Olton & Legner 1974). Exit From the Host.--The progeny of one female/day
may either all exit the host immediately after eclosion from the pupa, or
they may remain inside for variable lengths of time depending on when the
adult bites through the encasing host (Legner 1969). Male Reproductive System.--Most
intensive work has been done on Spalangia cameroni Perkins
(Gerling & Legner 1968 ). The male internal reproductive system in this species
matures during the last few days of pupal life. One day before emergence the
testes are already filled with fully developed sperm arranged in bundles
within the sperm tubes. Numerous large cells are present in the testes in
addition to these sperm bundles, which are more apparent at the anterior end
of the testes. The testes become depleted of sperm during the last day of the
pupal stage. The testes of emerging males, although depleted, still retain
more or less the external appearance of those of unemerged males. However, a
few days later they assume the shape of long thin tubes. Unidentified cells
and sperm residues are present in these old testes, and its seems that no
sperm producing function is carried out by them during the adult male's life. The seminal vesicle is composed of two
chambers, an anterior globular cavity and a posterior elongated one. The
anterior part is mostly thin walled with two slightly thickened valvelike
areas on its walls. The walls of the anterior portion undulate continuously
from the final pupal period until males die. Sperm enter the vesicle about
1/2 day before emergence where they are maintained in a helix-like formation.
The constantly undulating vesicle walls massage the sperm, seemingly to keep
them alive, but some independent movement is characteristic (Gerling &
Legner 1968
). Exercise 17.1--Define embryology and distinguish it
from ontogeny. Exercise 17.2--What are the characteristics of the
early stages of ontogeny? Discuss post natal development in Hymenoptera. Exercise 17.3--What is polyembryony? Exercise 17.4--Discuss prenatal development in
Hymenoptera. Exercise 17.5--How does the function of the testes
in Spalangia cameroni differ from other known examples?
Describe the morphology and function of the seminal vesicle. REFERENCES: [Additional references may
be found at MELVYL Library ] Baerends,
G. P. & J. M. van Roon. 1950. Embryological and ecological investigations
on the development of the egg of Ammophila campestris Jur. Tijdschr.
Ent. 92: 53-122. Bellows,
T. S., Jr. & T. W. Fisher, (eds) 1999. Handbook of Biological Control:
Principles and Applications. Academic Press, San Diego, CA. 1046 p. Bledowski,
R. & M. K. Krainska. 1926. Die Entwicklung von Banchus femoralis
Thoms. Bibl. Univ. Lib. Polon. 16: 1-50. Bodenstein,
D. 1953. Embryonic development. In: "Insect Physiology," K.
D. Roeder (ed.). John Wiley & Sons, Inc., New York. 780 p. Bonhag,
P. F. 1958. Ovarian structure and vitellogenesis in insects. Ann. Rev. Ent.
3: 137-60. Bronskill,
J. F. 1959. Embryology of Pimpla turionellae (L.) (Hymenoptera:
Ichneumonidae). Canad. J. Zool. 37: 655-88. Bronskill,
J. F. 1960. The capsule and its relation to the embryogenesis of the
ichneumonid parasitoid Mesoleius tenthredinis Morl. in the
larch sawfly, Pristiphora erichsonii (Htg.) (Hymenoptera:
Tenthredinidae). Canad. J. Zool. 38: 769-75. Butschli,
O. 1870. Zur Entwicklungsgeschichte der Biene. Z. wiss. Zool. 20: 519-64. Clausen,
C. P. 1940. Entomophagous Insects. McGraw-Hill Book Co., Inc., New York &
London. 688 p. Clausen,
C. P. 1950. Respiratory adaptations in the immature stages of parasitic
insects. Arthropoda 1: 197-224. Clausen,
C. P. 1976. Phoresy among entomophagous insects. Ann. Rev. Ent. 21: 343-68. Cooper,
K. W. 1959. A bilaterally gynandromorphic Hypodynerus, and a summary
of cytologic origins of such mosaic Hymenoptera. Biology of eumenine wasps.
Pt. VI. Bull. Fla. St. Mus. 5: 25-40. Counce,
S. J. 1961. The analysis of insect embryogenesis. Ann. Rev. Ent. 6: 295-312. Cruz, Y.
P. 1981. A sterile defender morph in a polyembryonic hymenopterous parasite.
Nature 294 (5840):446-47. Cruz, Y.
P. 1986a. The defender role of the precocious larvae of Copidosomopsis
tanytnemus Caltagirone (Encyrtidae: Hymenoptera). J. Expt. Zool. 137:
309-18. Cruz, Y.
P. 1986b. Development of the polyembryonic parasite Copidosomopsis tanytnemus
(Hymenoptera: Encyrtidae). Ann. Ent. Soc. Amer. 79: 121-27. Daniel,
D. M. 1932. Macrocentrus ancylivorus Rohwer, a polyembryonic
braconid parasite of the oriental fruit moth. New York Agric. Expt. Sta.
Tech. Bull. 187: 101 p. Doutt,
R. L. 1947. Polyembryony in Copidosoma koehleri Blanchard.
Amer. Naturalist 81: 435-53. Doutt,
R. L. 1952. The teratoid larva of polyembryonic Encyrtidae (Hymenoptera).
Canad. Ent. 84: 247-50. Doutt,
R. L. 1959. The biology of parasitic Hymenoptera. Ann. Rev. Ent. 4: 161-82. Flanders,
S. E. 1934. The secretion of the colleterial glands in parasitic chalcids. J.
Econ. Ent. 27: 861-62. Flanders,
S. E. 1938. Cocoon formation in endoparasitic chalcidoids. Ann. Ent. Soc.
Amer. 31: 167-80. Flanders,
S. E. 1942a. Oosorption and ovulation in relation to oviposition in the
parasitic Hymenoptera. Ann. Ent. Soc. Amer. 35: 251-66. Flanders,
S. E. 1942b. The larval meconium of parasitic Hymenoptera as a sign of the
species. J. Econ. Ent. 35: 456-7. Flanders,
S. E. 1942c. Sex differentiation in the polyembryonic proclivity of the
Hymenoptera. J. Econ. Ent. 35: 108. Flanders,
S. E. 1950. Regulation of ovulation and egg disposal in the parasitic
Hymenoptera. Canad. Ent. 82: 134-40. Flanders,
S. E. 1959. Embryonic starvation, an explanation of the defective honey bee
egg. J. Econ. Ent. 52: 166-67. Flanders,
S. E. 1964. Dual ontogeny of the male Coccophagus gurneyi Comp.
(Hymenoptera: Aphelinidae): a phenotypic phenomenon. Nature 204(4962):
944-46. Flanders,
S. E. 1967. Deviate-ontogenies in the aphelinid male (Hymenoptera) associated
with the ovipositional behavior of the parental female. Entomophaga 12:
415-27. Gatenby,
J. B. 1917. The embryonic development of Trichogramma evanescens
Westw., monembryonic egg parasite of Donacia simplex. Quart. J.
Microscop. Sci. 62: 149-87. Gatenby,
J. B. 1920. The cytoplasmic inclusions of the germ cells. Part VI. On the
origin and probable constitution of the germ cell determinant of Apanteles
glomeratus, with a note on the secondary nuclei. Quart. J. Microscop.
Sci. 64: 133-53. 54.
Gerling, D. &
E. F. Legner. 1968. Developmental history and reproduction of Spalangia cameroni, parasite of synanthropic flies. Ann. Entomol. Soc. Amer. 61(6): 1436-1443. Geyspitz,
K. F. & I. I. Kyao. 1953. The influence of the length of illumination on
the development of certain braconids (Hymenoptera). Ent. Obozsenie 33: 32-35. Grandori,
R. 1911. Contributo all' embriologia alla biologia dell' Apanteles glomeratus
(L.). Reinh. Redia 7: 363-428. Hagen,
K. S. 1964. Developmental stages of parasites. In: "Biological
Control of Insect Pests and Weeds," P. H. DeBach (ed.). Reinhold Publ.
Corp., New York. pp 175-92; 213-19. Hallez,
P. 1886. Loi de l'orientation de l'embryon chez les insectes. Compt. Rend.
103: 606-08. Hegner,
R. W. 1915. Studies on germ cells. Part IV. Protoplasmic differentiation in
the oocytes of certain Hymenoptera. J. Morphol. 26: 495-561. Heraty
& Darling. 1984. Syst. Ent. 9: 308-18. Hinton,
H. E. 1981. The Biology of Insect Eggs. Vol. 1-3. Pergamon Press, Oxford.
1125 p. Howe, R.
W. 1967. Temperature effects on embryonic development in insects. Ann. Rev.
Ent. 12: 15-42. Imms, A.
D. 1931. Recent Advances in Entomology. Blakiston & Sons, London. 374 p. Ioff, N.
A. 1948. Contribution to the question of the embryonic development of ichneumonids
[in Russian]. Compt. rend. acad. Sci. U.S.S.R. 60: 1477-80. Ivanova-Kazas,
O. M. 1948. Characteristics of embryonic development of parasitic Hymenoptera
in connection with parasitism. [in Russian]. Uspekhi Sovremennoi Biol. 25:
123-42. Ivanova-Kazas,
O. M. 1950. Adaptations to parasitism in the embryonic development of the
ichneumon fly, Prestiwichia aquatica (Hymenoptera). [in
Russian]. Zool. Zhur. 29: 530-44. Ivanova-Kazas,
O. M. 1952. Embryonic development of Mestocharis militaris R.-Kors.
(Hymenoptera: Chalcididae). [in Russian]. Ent. Obozrenie, Moscow 32: 160-66. Ivanova-Kazas,
O. M. 1954a. The effect of parasitism on the embryonal development of Caraphractus
reductus R.-Kors (Hymenoptera). [in Russian]. Leningrad Obsoch.
Estestvoispytatelei Trudy 72: 57-73. Ivanova-Kazas,
O. M. 1954b. On the evolution of embryonic development of Hymenoptera. [in
Russian]. Trudy Vsesoyuz. Ent. Obschch., Moscow 44: 301-35. Ivanova-Kazas,
O. M. 1954c. On the evolution of the embryonic development in Hymenoptera.
[in Russian]. Doklady Akad. Nauk. SSSR, Moscow (n.s.) 96: 1269-72. Ivanova-Kazas,
O. M. 1956. Comparative study of embryonal development in aphidiids (Aphidius
and Ephedrus). [in Russian with German summary]. Ent. Obozr. 35:
245-6. Ivanova-Kazas,
O. M. 1958. Biology and embryonic development of Eurytoma aciculata
Ratz. (Hymenoptera: Eurytomidae). [in Russian with English summary]. Ent.
obozrenie 37: 1-18. Ivanova-Kazas,
O. M. 1964. Forms of polyembryony in animals. Zool. Zh. 43(5): 641-46. Iwata,
K. 1959. The comparative anatomy of the ovary in Hymenoptera. Part III.
Braconidae (inc. Aphidiidae). Kontyu 27(4): 231-38. Iwata,
K. 1959. The comparative anatomy of the ovary in Hymenoptera. Part IV.
Proctotrupoidea and Agriotypidae (Ichneumonidae) with description of ovarian
eggs. Kontyu 27: 18-20. Iwata,
K. 1960. The comparative anatomy of the ovary in Hymenoptera. Part V.
Ichneumonidae. Acta Hymenopterologica 1: 115-69. Iwata,
K. 1960. The comparative anatomy of the ovary in Hymenoptera. Supplement of
Aculeata with descriptions of ovarian eggs of certain species. Acta.
Hymenopterologica 1: 205-11. Iwata,
K. 1962. The comparative anatomy of the ovary in Hymenoptera. Part VI.
Chalcidoidea with description of ovarian eggs. Acta Hymenopterologica 1(4): 383-91. Jackson,
D. J. 1928. The biology of Dinocampus (Perilitus) rutilus
Nees, a braconid parasite of Sitona linesta L. Part I. Zool.
Proc. London Zool. Soc. 1928: 597-630. Johannsen,
O. A. & F. H. Butt. 1941. Embryology of insects and myriapods. McGraw-Hill
Book Co., Inc., New York. King, P.
E. & J. G. Richards. 1968. Oosorption in Nasonia vitripennis
(Hymenoptera: Pteromalidae). J. Zool. Lond. 154: 495-516. King, P.
E. & N. A. Ratcliffe. 1969. The structure and possible mode of
functioning of the female reproductive system in Nasonia vitripennis
(Hymenoptera: Pteromalidae). J. Zool., London 157: 319-44. King, P.
E., J. G. Richards & M. J. W. Copland. 1968. The structure of the chorion
and its possible significance during oviposition in Nasonia vitripennis
(Walker) (Hymenoptera: Pteromalidae), and other chalcids. Proc. Roy. Ent.
Soc. London (A) 43(1-3): 13-20. Kornhauser,
S. J. 1919. The sexual characteristics of the membracid Thelia bimaculata
(Fab.). I. External changes induced by Apelopus theliae (Gahan).
J. Morphol. 32: 531-635. Krivosheina,
N. P. 1969. The ontogeny and evolution of the Diptera. Nauka Press, USSR. 292
p. LaSalle,
J. & L. M. LeBeck. 1983. The occurrence of encyrtiform eggs in the
Tanaostigmatidae (Hymenoptera: Chalcidoidea). Proc. Ent. Soc. Wash. 85:
397-98. Lassmann,
G. W. P. 1936. The early embryological development of Melophagus ovinus
with special reference to the development of the germ cells. Ann. Ent. Soc.
Amer. 29: 397-413. 57.
Legner, E. F. 1969.
Adult emergence interval and reproduction in parasitic Hymenoptera
influenced by host size and density.
Ann. Entomol. Soc. Amer. 62(1): 220-226. Leiby,
R. W. 1922. The polyembryonic development of Copidosoma gelechiae,
with notes on its biology. J. Morphol. 37: 195-285. Leiby,
R. W. 1929. Polyembryony in insects. Trans. 4th Intern. Congr. Ent. 2:
873-87. Leiby,
R. W. & C. C. Hill. 1923. The twinning and monoembryonic development of Platygaster
heimalis, a parasite of the Hessian fly. J. Agric. Res. 25: 337-50. Leiby,
R. W. & C. C. Hill. 1924. The polyembryonic development of Platygaster
vernalis. J. Agric. Res. 28: 829-40. Maple,
J. D. 1937. The biology of Ooencyrtus johnsoni (Howard), and
the role of the egg shell in the respiration of certain encyrtid larvae
(Hymenoptera). Ann. Ent. Soc. Amer. 30: 123-54. Marchal,
P. 1898. Le cycle evolutif de l' Encyrtus fusicollis. Bull.
Soc. Ent. de France (1898): 109-11. Marchal,
P. 1904. Recherches sur la biologie et le developpement de hymenopteres
parasites. I. La polyembryonie specifique ou germinogonie. Arch. de Zool.
Exp. et Gen. 2: 257-335. Marchal,
P. 1906. Recherches sur la biologie et le developpement des Hymenopteres
parasites. Les Platygasters. Arch. Zool. Exp. et Gen. 4, Ser. 4: 485-640. Martin,
F. 1914. Zur Entwicklungsgeschichte des polyembryonalen Chalcidiers Ageniaspis
(Encyrtus) fusicollis Dalm. Ph.D. Thesis, Zool. Inst. Univ.
Leipzig. p. 419-79. Maxwell,
D. E. 1958. Sawfly cytology with emphasis upon the Diprionidae (Hymenoptera:
Symphyta). Proc. 10th Intern. Congr. Ent. (1956) 2: 961-78. Nelson,
J. A. 19l5. The Embryology of the Honey Bee. Princeton Univ. Press,
Princeton, New Jersey. 120.
Olton, G. S. &
E. F. Legner. 1974. Biology of Tachinaephagus zealandicus
(Hymenoptera: Encyrtidae), parasitoid of synanthropic Diptera.
Canad. Entomol. 106(8):
785-800. Paillot,
A. 1937. Sur le developpement polyembryonaire d' Amicroplus collaris
Spin., parasite des chenilles d' Euxoa segetum Schiff. Compt.
Rend. Acad. Sci. (Paris) 204: 810-12. Pampel,
W. 19l3. Die weiblichen Geschlectsorgane der Ichneumoniden. Ztschr. f. Wiss.
Zool. 108: 290-357. Pantel,
J. 1910. Recherches sur les Dipteres a larves entomobies. I. Caracteres
parasitiques aux points de vue biologique, ethologique et histologique.
Cellule 26: 27-216. Parker,
H. L. 1931. Macrocentrus gifuensis Ashmead, a polyembryonic
braconid parasite in the European corn borer. U. S. Dept. Agric. Tech. Bull.
230: 1-62. Parker,
H. L. 1933. The interrelations of two hymenopterous egg parasites of the
gypsy moth, with notes on the larval instars of each. J. Agric. Res. 46:
23-34. Patterson,
J. T. 1915. Observations on the development of Copidosoma gelechiae.
Biol. Bull. 29: 291-305. Patterson,
J. T. 19l7. Studies on the biology of Paracopidosomopsis. I. Data on
the sexes. Biol. Bull. 32: 291-305. Roonwal,
M. L. 1939. Some recent advances in insect embryology with a complete
bibliography of the subject. J. Roy. Asiatic Soc. Bengal, Sci. 4: 17-105. Salt, G.
1931. Parasites of the wheat-stem sawfly, Cephus pygmaeus
Linneaue, in England. Bull. Ent. Res. 22: 479-545. Salt, G.
1932. Superparasitism by Collyria calcitrator Grav. Bull. Ent.
Res. 23: 211-15. Salt, G.
1961. Competition among insect parasitoids. Symposia Soc. Exper. Biol. 15:
Mechanisms in Biol. Competition, p. 96-119. Schnetter,
M. 1934. Morphologische Untersuchungen über das Differenzierungszentrum in
der Embryonalentwicklung der Honigbiene. Z. Morphol. Okol. Tiere 29: 114-95. Schneider,
F. 1941. Eientwicklung und eiresorption in den Ovarian des Puppenparasiten Brachymeria
euploeae Westw. (Chalcididae). Z. angew. Ent. 29: 211-28. Seurat,
M. 1899. Contributions a l'etude des Hymenopteres entomophages. pH.D. Thesis
a la Faculte des Sci. de Paris Ser. A (329): 159 p. Shafer,
G. D. 1949. The Ways of a Mud Dauber. Stanford Univ. Press. 78 p. Shafiq,
S. A. 1954. A study of the embryonic development of the gooseberry sawfly, Pteronidea
ribesii. Quart. J. Microscop. Sci. 95: 93-114. Silvestri,
F. 1906. Contribuzioni alla conoscenza biologica degli imenotteri parassiti.
I. Biologia del Litomastix truncatellus (Dalm.). Bol. Lab. Zoo.
Gen. e Agr. Portici 1: 17-64. Silvestri,
F. 1923. Contribuzioni alla conoscenza dei Tortricidi delle querce. Bol. Lab.
Zool. Gen. e Agr. Portici 17: 41-107. Silvestri,
F. 1937. Insect polyembryony and its general biological aspects. Bull. Mus.
Comp. Zool., Cambridge, Mass. 81: 469-98. Simmonds,
F. J. 1947. The biology of the parasites of Loxostege stricticalis
L., in North America--Meterous loxostegei Vier. (Braconidae,
Meteorinae). Bull. Ent. Res. 38: 373-79. Smith,
H. D. 1930. The bionomics of Dibrachoides dynastes (Foerster),
a parasite of the alfalfa weevil. Ann. Ent. Soc. Amer. 23: 577-93. Smith,
H. D. 1932. Phaeogenes nigridens Wesmael, an important
ichneumonid parasite of the pupa of the European corn borer. U. S. Dept.
Agric. Tech. Bull. 331: 1-45. Smith,
O. J. 1952. Biology and behavior of Microctonus vittatae
Muesebeck (Braconidae). Univ. Calif. Publ. Ent. 9: 315-44. Tanquary,
M. C. 19l3. Biological and embryological studies on Formicidae. Bull. Ill.
State Lab. Nat. Hist. 9: 417-79. Telfer,
W. H. 1965. The mechanism and control of yolk formation. Ann. Rev. Ent. 10:
161-84. Thompson,
W. R. & H. L. Parker. 1928. Contribution a la biologie des chalcidiens
entomophages. Ann. Soc. Ent. de France 97: 425-65. Thompson,
W. R. & H. L. Parker. 1930. The morphology and biology of Eulimneria
crassifemur, an important parasite of the European corn borer. J.
Agric. Res. 40: 321-45. Tiegs,
O. W. 1922. Researches on the insect metamorphosis. I. On the structure and
postembryonic development of a chalcid wasp, Nasonia. II. On the
physiology and interpretation of the insect metamorphosis. Trans. Roy. Soc.
S. Australia 46: 319-527. Tothill,
J. D. 1922. The natural control of the fall webworm (Hyphantria cunea
Drury), in Canada together with an account of its several parasites. Canad.
Dept. Agric. Tech. Bull. 3: 107 p. Tower,
D. G. 19l5. Biology of Apanteles militaris. J. Agric. Res. 5:
495-508. Vance,
A. M. 1927. On the biology of some ichneumonids of the genus Paniscus
Schrk. Ann. Ent. Soc. Amer. 20: 405-17. White, M. J. D. 1954. Animal Cytology and Evolution. 2nd ed.
Cambridge Univ. Press, Cambridge. 454 p. |