FILE: <bc-17.htm> Pooled References GENERAL INDEX [Navigate to MAIN MENU ]
EMBRYOLOGY
/ ONTOGENY / ANATOMY
In Arthropods
(Contacts)
---- Please CLICK on desired underlined categories [ to search for Subject Matter, depress
Ctrl/F ]:
|
Prenatal Development in Hymenoptera
Specifically |
|
|
Common Egg Shapes in
Parasitoids |
|
|
[ Please refer also to Selected Reviews |
|
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 semi fluid; and ligaturing the newly deposited egg so that
one-third of the protoplasm is not used can reduce the size of the mature
embryo. 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. 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 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 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. |