FILE: <bc-18.htm> Pooled References GENERAL INDEX [Navigate to MAIN MENU ]
OOGENESIS--OVISORPTION
In
Arthropods
(Contacts)
---- Please CLICK on desired underlined categories [to search for Subject Matter, depress
Ctrl/F ]:
|
Classification of Hymenoptera by the
Female's Reproduction |
|
|
Variability in Ovisorption Process
among Hymenoptera |
[Please refer also to Selected Reviews |
|
History Biological
control workers are thought to have been the first to consider the phenomenon
of ovisorption as a nutrient storage mechanism in insects. Weyer (1927)
working with ants was presumably the first to recognize ovisorption at all;
and later Flanders (1935) related ovisorption to the effectiveness of
parasitoids in controlling their hosts. Insect physiologists also noted the
phenomenon almost simultaneously in other orders of insects (Pfeiffer 1939;
Wigglesworth 1936, 1948a, 1948b; Highnam et al. 1963). General
Characteristics When certain parasitic Hymenoptera which ovulate yolk-replete eggs
are withheld from their hosts, the processes of oogenesis and ovisorption
occur synchronously and enable the female to deposit newly formed viable eggs
after a period of inhibited oviposition (usually 3-4 days). Parasitoid species
that show this particularly well are Brachymeria
euploeae Westwood, Peridesmia phytonomi Gahan, Pteromalus
puparum L., Encyrtus fuliginosus Compere, and Metaphycus helvolus
(Compere) and Nasonia vitripennis (Walker) (Flanders
1935, 1942b,e; Schneider 1941, Medler 1962, Hopkins & King 1964, 1966;
King & Richards 1968a, King & Ratcliffe 1969). Non-viable eggs in the process of disintegration may be
deposited, as well as viable, partially-collapsed eggs (Flanders 1942b,e),
whose deposition in the host appears to be indiscriminate (Gerling &
Legner 1968 ). Such
deposition of partially absorbed viable eggs may produce the diploid males in
Bracon hebetor (Flanders 1943); or embryonic starvation and
thence deposition of defective eggs in the honeybee (Flanders 1957, 1959b).
They may be prerequisites to worker caste determination in ants, bees and
wasps (Flanders 1945b, 1952, 1956). They may also change the normal sex ratio
in Nasonia vitripennis (King 1962).
Ovisorption occurs when conditions are unfavorable for the deposition of any
mature (ripe) eggs (Flanders 1942e, Edwards 1954b, LaBergrie 1959, Phipps
1966). It may occur following parasitism as in Bombus terrestris
(Palm 1948). The processes of host-feeding,
oviposition and ovisorption are closely related and affect the fecundity,
longevity and host killing capacity of the parasitoid (Legner & Gerling 1967, Legner &
Thompson 1977). Physiology
of Ovigenesis-Ovisorption Classic work has been conducted on other orders by
physiologists (Wigglesworth 1936, 1948a,b; Ito 1942, Pfeiffer 1945),
emphasizing the role of the corpus allatum in oogenesis and resorption. The neurosecretory
cells were recognized as a source of stimulation of the corpus
allatum and the ovaries (Wigglesworth 1936, 1948a,b). The role of the corpus cardiacum
was also recognized (Pfeiffer 1945). In Calliphora, allatectomy experiments showed effects on
ovary development and yolk deposition (Thomsen 1952). The medial
neurosecretory cells of the brain, when cauterized, have the same effect
(Thomsen 1952). Histological, biochemical and histochemical work on
Coleoptera (Schlottman & Bonhag 1956), on Orthoptera (Highnam 1962,
Highnam et al. 1963, Lusis 1963; Pfeiffer 1945), and studies on diapause of Leptinotarsa decemlineata (de Wilde 1962,
deWilde & de Boer 1961) suggested that the nervous system controls the
amount of protein in the haemolymph, stimulating the corpora allata / ovary
system for the deposition and ovisorption of eggs. The protein uptake by the
oocytes is controlled by the corpus allatum (Strong 1965, Telfer 1965).
Ovisorption is, therefore, an integrated process in which the brain, corpora
allata, corpus cardiaca, plus physical and chemical environmental factors
complement their actions. The role played by the different parts of the
system varies with the insect species (Englemann 1968). Ovisorption was defined by deWilde (1964) as "the
capacity of the follicle cells to dissolve and absorb the oocyte."
Several factors can contribute to the production of this phenomenon in which
vitellogenesis is interrupted and the oocyte, wholly enveloped in its
follicle, may die. Follicle cells cease to participate in alimentary egg
formation; they may divide amitotically, and absorb the dead oocyte. Their
nuclei become pycnocytic, the cells breaking down and being absorbed through
the ovarian sheaths (King 1963, Richards & King 1967). Thomsen (1952)
showed that ovisorption is brought about by the integration of several
neurosecretory, physical and chemical factors. Doutt (1964) maintained that
from a biological control viewpoint, this physiological characteristic is a
very important one in parasitoids where effectiveness as natural enemies of
pests will depend in part on their conservation of reproductive material
which is correlated with a high host searching capacity. Vitellogenesis
(Yolk Formation) Bonhag (1958) reviewed the process of vitellogenesis, followed
by another review by Telfer (1965) in light of rapid developmental progress
in this aspect of insect physiology. In the process, apparently blood
proteins are transferred directly to the developing yolk in the oocytes.
There is a large number of different kinds of blood proteins synthesized in
insects, the site of any single one not being definite. In all insect
ovaries, the chain of follicles comprising an ovariole is continuously
surrounded by a cellular sheath (the ovariole wall) and a basement lamella,
the so-called tunica
propria (Bonhag 1958, Bier 1967, King & Ratcliffe 1968).
During yolk formation the individual oocyte is directly enveloped by a single
layer of follicle cells whose outer surface adheres to the inner side of the
basement lamella. In some insects there is, in addition, a vitelline membrane
lying between the oocyte surface and the follicle cells (King & DeVine
1958). All membranes are thought to be permeable to blood proteins.
Intercellular spaces form in the follicle cells synchronous with the onset of
blood protein penetration. There is also some evidence that nurse cells
atrophy before the onset of chorion formation and much of their cytoplasm
literally flows tho=rough the connectives into the oocyte. Some portion of
the nurse cells remains outside the chorion, however, after its formation
(see Telfer 1965). A role of the nurse cells in yolk formation is indicated
in some insects, but seems to be rather insignificant in others (Telfer
1965). When the individual follicle has reached the stage where yolk
formation should commence, its further development in many insects requires
the presence of the corpus allatum (secreting a juvenile hormone). Another
hormone is produced later which activates the final stages of oocyte
formation (see Telfer 1965 for an extensive treatment of hormonal control of
yolk formation). In a number of insects which form eggs prior to the emergence
of the adults, the fat body in addition to the blood is one of the primary
storage sites of yolk precursors (Telfer 1965). Classification
of Parasitic Hymenoptera Using the Female Reproductive System Parasitic Hymenoptera may be divided into two general types:
(1) proovigenic and (2) synovigenic. In proovigenic species
oogenesis is largely, if not entirely, completed prior to egg deposition. Most
of the eggs are laid shortly after eclosion from the pupa, and the
oviposition period is usually so short that relatively large numbers of
females are needed to search a given area effectively. The maintenance of
such a parasitoid population requires a relatively large population of hosts.
Synovigenic species, on the other hand, generally synchronize oogenesis with
egg-deposition. They possess a prolonged oviposition period, and they are
thought to be more effective in biological control because they are longer
lived and, consequently, can reproduce at lower densities of the host
population. Synovigenic species may be further divided into two
sub-groups: (1) where ovulation is internally
induced and (2) where ovulation is externally
induced. In the group where ovulation is internally induced there are
additionally two types: (a) the Ophion-type where the oviducts are
almost as long as the ovary. This includes ectoparasitic species with uterine
incubation as well as some endoparasitoids. Most of the Ophion-type species do not have oviducts modified for egg
storage; (b) the Apanteles-type, which has oviducts that
are shorter than the ovary and are modified for egg storage. All of these
species are endoparasitic (e.g., Chelonus),
with no ectoparasitoids known. In the group of synovigenic species where ovulation is
externally induced, the oviducts are not adapted to storage of ovulated eggs.
One subgroup of this type is the Monootene-type, where only one
ripe egg at a time occurs in each ovariole (e.g., Signiphora). A second sub-group, the Polyootene-type,
has several ripe eggs at a time in each ovariole (e.g., Nasonia, Spalangia).
In these species ovisorption sets in when the pressure of accumulated eggs
reaches a certain point (Schneider 1941). Polyootene-type species may deposit
partially absorbed eggs (e.g., Spalangia
cameroni). Such eggs may be
laid in the absence of hosts, as shown in Phaeogenes
nigridens (Wesmael) (Smith
1932); or they may be laid on the hosts, as in Spalangia cameroni
(Gerling & Legner 1968 ). Hymenoptera may also be classified according to the amount of
yolk contained in the ripe eggs. Thus, we have yolk-deficient hydropic
species and yolk-replete anhydropic species. It is necessary for anhydropic eggs to
be eliminated from the oviduct, for if not, in some species the larvae will
hatch and perforate the oviduct wall, killing the parent female (Chewyreuv
1911, 1912). In some species with hydropic eggs, ripe eggs may be stored in
the enlarged oviducts pending conditions suitable for oviposition (Flanders
1942). Because development is stimulated only by substances present in the
host, the hydropic eggs in the oviducts remain in a quiescent condition
during the life of the female. When hosts are lacking, a portion of the eggs
of hydropic species of Ascogaster
is stored in the oviduct. Then, ovulation ceases and ovisorption takes place
in the ovarioles. Variability
in Ovisorption Process Among Hymenoptera In ectoparasitic species, ovisorption probably proceeds with
greater rapidity than oogenesis (Flanders 1942). Delayed ovulation may result
in the deposition of slightly absorbed eggs of low viability. A decrease in
oviposition rate may account for the observation by Whiting (1940) that the
percentage of non-hatching eggs deposited by Bracon hebetor
increases with the age of the ovipositing female. Whiting also pointed out
that in Bracon hebetor embryonic development
occurs in almost every nonhatching egg. Consequently, it seems probable that
eggs which have not regressed beyond a certain point may hatch, and the
larvae by feeding avidly on the host, may complete their development. In worker ants, the honeybee and certain wasps, the resorption
of developing eggs has been described by Weyer (1927). In some parasitic
Hymenoptera a temporary withdrawal of hosts will allow ovisorption and
oogenesis to occur synchronously, thus enabling a female after a period of
inhibited oviposition to deposit viable eggs as if no interruption had
occurred (Flanders 1942). If the absence of hosts is prolonged, such species
may maintain their reproductive capacity by complete ovisorption and
cessation of oogenesis, a state that Flanders (1935) considered phasic castration or imaginal
diapause. Withdrawal from hosts for even a limited period of time
(3 days) does have a pronounced significant effect on the fecundity and
longevity of the female thereafter, however (Legner & Gerling 1967). This work
involved three genera of parasitic Hymenoptera and was conclusive beyond a
doubt. Nevertheless, Lloyd (1940) reported that the daily fecundity of the
ichneumonid Diadromus collaris was unaffected by periods
of inhibited oviposition; and Flanders (1942) maintained that in several
chalcidoids parasitic on black scale the substitution of ovisorption for
ovulation during periods of isolation apparently maintained the normal
oviposition curve. In certain pteromalids, ovisorption may be followed by a long
period of castration, five months or more at 26.7BC, which begins and ends
spontaneously (e.g., Dibrachoides). The fate of the chorion in ovisorption has sometimes been
questioned. In no species is it known that the chorions, or remnants of an
absorbed egg, are discharged either into the oviduct or through either the
ovipositor or the copulatory opening. The accumulation of egg remnants in the
ovarioles, which often occurs, seems not to interfere with ovulation. In the Encyrtidae, Flanders (1942) observed that the remains
of an aeroscopic
plate indicated that ovisorption has occurred. In one species, Encyrtus fuliginosus Compere, the exochorion of each disintegrated
eggs appeared to have been extruded into the body cavity. In this species the
longevity of ovipositing adults is longer than that of adults that do not
oviposit. Apparently, internal organs such as the heart, auxiliary pumps,
etc., become clogged with chorions! Partial ovisorption occurs in Spalangia cameroni
after 10 days without hosts (Gerling & Legner 1968 ). Such
partially-resorbed eggs were deposited. Complete resorption apparently occurs
only in individuals that were given an opportunity to oviposit and host feed
early in life. Ovisorption Rate.--In Signiphora
only one mature egg and one developing egg occur in any given ovariole, the
rest of the structure being composed of germarium (Quezada 1967). It was
reasoned that this was logical since the species had an extremely rapid rate
of egg development and resorption (two hours!). If Signiphora females were not provided with hosts for five
days, ovisorption was complete and the germarium was no longer capable of
generating more eggs. Two days are usually required for resorption and three days
for oogenesis in most species. In the honeybee, with an excess of 300
ovarioles, the process of ovisorption must be continuous since there are
usually never more than about 1000 eggs deposited each day. Each ovariole in the
honeybee contains several (4-6) ripe eggs at any given time. The yellow ring
present in ovarioles of older queens gives evidence for the tremendous amount
of ovisorption in the honeybee. Effect of Ovisorption
on Longevity.--Ovisorption may enable a starved female to outlive a male
(King & Hopkins 1963). It may enable hymenopterous parasitoids with
anhydropic eggs to retain their reproductive potential during periods of
unfavorable environmental conditions, although fecundity is sometimes lowered
after ovisorption has occurred, and the sex ratio of the offspring may be
affected by partial resorption (King 1962: work with Nasonia vitripennis). Research on Nasonia
vitripennis.--In Hymenoptera, ovisorption usually occurs before the
formation of either the vitelline membrane or the chorion, but may be either
before or after yolk formation (King 1968a). However, Nasonia is exceptional in that the oldest eggs with
developed chorions are the first to be resorbed (King 1968a). The egg
membranes are removed by enzymes, which are apparently released from the
follicle cells (enzymes = Leucine amino peptidase and esterase) (Richards
& King 1967). The earlier onset of ovisorption in older individuals
probably results from the reduction in reserve food materials stored in the
fat body so that under conditions of starvation the protein in the haemolymph
is depleted more rapidly in older starved individuals (King 1968a). King also
restated the fact that the speed of ovisorption is not affected by the age of
the individual (Edwards 1954, King 1963). Exercise 18.1--Discuss ways in which ovisorption might influence the
sex ratio of a parasitic species. Exercise 18.2--Distinguish synovigenic from proovigenic species. Exercise 18.3--Recognize the difference between Ophion-type and Apanteles-type
species. Exercise 18.4--How quick is the ovisorption process? Exercise 18.5--How does ovisorption affect the longevity of the
organism? REFERENCES: [Additional
references may be found at MELVYL
Library ] Bellows,
T. S., Jr. & T. W. Fisher, (eds) 1999. Handbook of Biological Control:
Principles and Applications. Academic Press, San Diego, CA. 1046 p. Bier,
K. 1967a. Lamp brush chromosomes and RNA supply in insect oocytes. Umschau Wiss. Tech. 67(14): 453 Bier,
K. 1967b. Origin and sites of synthesis of macromolecular reserve substances
in eggs. Umschau
in Wissenschaft und Technik 67(15): 494. Bier, K. W. & D. Ribbert. 1967.
Structure and function of occyte chromosomes and nucleoles as well as of
extra-DNA during oogenesis of panoistic and meroistic insects. Chromosoma 23(2): 214-54. Bonhag, P. F. 1958. Ovarian
structure and vitellogenesis in insects. Ann. Rev. Ent. 3: 137-60 Bracken,
G. K. 1969. Effects of dietary amino acids, salts, and protein starvation on
fecundity of the parasitoid Exeristes
comstockii (Hymenoptera:
Ichneumonidae). Canad. Ent. 101: 91-96. Chewyreuv,
I. J. 1912. Parasites and hyperparasites in the insect world. Messager Ent.
1: 1-77. Doutt,
R. L. 1959. The biology of parasitic Hymenoptera. Ann. Rev. Ent. 4: 141-82. Doutt,
R. L. 1964. Biological characteristics of entomophagous adults. In: "Biological Control of
Insect Pests and Weeds," P. H. DeBach (ed.). p. 145-67. Reinhold Publ.
Corp., New York. 844 p. Edwards,
R. L. 1954a. The effect of diet on egg maturation and resorption in Mormoniella vitripennis (Hymenoptera,
Pteromalidae). Quart. Rev. Micr. Sci. 95: 459-68. Edwards,
R. L. 1954b. The host-finding and oviposition behavior of Mormoniella vitripennis (Walker) (Hym.,
Pteromalidae), a parasite of muscoid flies. Behaviour 7: 88-112. Flanders,
S. E. 1935. An apparent correlation between the feeding habits of certain
pteromalids and the condition of their ovarian follicles (Pteromalidae,
Hymenoptera). Ent. Soc. Amer. 28: 438-44. Flanders, S. E. 1942a. Sex
differentiation in the polyembryonic proclivity of the Hymenoptera. J. Econ. Ent. 35: 108. Flanders, S. E. 1942b. Deposition
of non-viable eggs by Hymenoptera. J. Econ. Ent. 35: 283. Flanders, S. E. 1942c. The
larval meconium of parasitic Hymenoptera as sign of the species. J. Econ. Ent. 35: 456-57. Flanders, S. E. 1942d. Abortive
development in parasitic Hymenoptera induced by the food plant of the insect
host. J.
Econ. Ent. 35: 834-35. Flanders, S. E. 1942e. Oosorption
and ovulation in relation to oviposition in the parasitic Hymenoptera. Ann. Ent. Soc. Amer. 35: 251-66. Flanders, S. E. 1943. Partial
oosorption as a possible cause of diploid males in Microbracon hebetor.
The American Naturalist 77: 479-80. Flanders, S. E. 1945. Is
caste differentiation in ants a function of the rate of egg deposition?
Science 101: 245-46. Flanders,
S. E. 1950. Regulation of ovulation and egg-disposal in the parasitic
Hymenoptera. Canad. Ent. 82: 134-40. Flanders,
S. E. 1952. Ovisorption as the mechanism causing worker development in ants. J. Econ. Ent. 45: 37-39. Flanders, S. E. 1956. The
mechanisms for sex-ratio regulation in the (parasitic) Hymenoptera. Insectes
Sociaux 3: 325-34. Flanders,
S. E. 1957. Ovigenic-ovisorptic cycle in the economy of the honey bee. Sci.
Month. 85: 176-77. Flanders,
S. E. 1959. Embryonic starvation, an explanation of the defective honey bee
egg. J.
Econ. Ent. 52: 166-67. 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. Highnam,
F. C. 1962. Neurosecretory control of ovarian development in Schistocerca gregaria. Quart. J. Microscop.
Sci. 103: 57-752. Highnam,
F. C., O. Lusis & L. Hill. 1963. Factors affecting oocyte resorption in
the desert locusts Schistocerca
gregaria (Forskal). J.
Insect Physiol. 9:
827-37. Hinton, H. E. 1969. Respiratory
systems of insect egg shells. Ann. Rev. Ent. 14: 343-68. Hopkins,
C. R. & P. E. King. 1964. Egg resorption in Nasonia vitripennis
(Walker) (Hymenoptera, Pteromalidae). Proc. Roy. Ent. Soc. London (A) 39:
101-07. Hopkins,
C. R. & P. E. King. 1966. An electron-microscopical and histochemical
study of the oocyte periphery in Bombus
terrestris during
vitellogenesis. J. Cell Sci. 1: 201-16. King,
P. E. 1962. The effect of resorbing eggs upon the sex ratio of the offspring
in Nasonia vitripennis (Hymenoptera,
Pteromalidae). J. Expt. Biol. 39: 161-65. King,
P. E. 1963. The rate of egg resorption in Nasonia
vitripennis (Walker)
(Hymenoptera: Pteromalidae) deprived of hosts. Proc. Roy. Ent. Soc. London
38: 98-100. King,
P. E. & C. R. Hopkins. 1963. Length of life of the sexes in Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) under
conditions of starvation. J. Exptal. Biol. 40: 751-61. King,
P. E. & N. A. Ratcliffe. 1968. The composition of yolk in the eggs of Apanteles glomeratus (L.) (Braconidae: Hymenoptera). Entomologist 101(1263):
178-79. King,
P. E. & N. A. Ratcliffe. 1969. The structure and possible mode of
functioning of the female reproductive system in Nasonia vitripennis
(Hym.: Pteromalidae). J. Zool. 157: 319-44. King,
P. E. & J. G. Richards. 1968. Oosorption in Nasonia vitripennis
(Hymenoptera: Pteromalidae). J. Zool. 154(Pt. 4): 495-516. King,
P. E. & J. G. Richards. 1968. Accessory nuclei and annulate lamellae in
Hymenopteran oocytes. Nature 218 (5140): 488. King,
P. E. & N. A. Ratcliffe. 1969. The structure and possible mode of
functioning of the female reproductive system in Nasonia vitripennis
(Hym., Pteromalidae). J. Zool. 157(Pt. 3): 319-44. King,
P. E., J. G. Richards & M. J. W. Copeland. 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: 13-20. King,
R. C. & R. L. DeVine. 1958. Oogenesis in adult Drosophila melanogaster.
VII. The submicroscopic morphology of the ovary. Growth 22: 299-326. LaBergrie,
V. 1959. Embryonic diapause in the unlaid egg of parasitic Hymenoptera. C. R. Hebd. Seanc.
Acad. Sci. Paris
249: 2115-17. 48.
Legner, E. F. & D. Gerling.
1967. Host-feeding and oviposition on Musca domestica by Spalangia cameroni, Nasonia vitripennis,
and Muscidifurax raptor (Hymenoptera: Pteromalidae)
influences their longevity and fecundity.
Ann. Entomol. Soc. Amer. 60(3):
678-691. 167. Legner, E. F. & S. N. Thompson. 1977.
Effects of the parental host on host selection, reproductive
potential, survival and fecundity of the egg-larval parasitoid Chelonus sp. near curvimaculatus, reared on Pectinophora
gossypiella and Phthorimaea operculella. Entomophaga 22(1): 75-84. Lusis, O. 1963. The
histology and histochemistry of development and resorption in the terminal
oocytes of the desert locust, Schistocerca
gregaria. Quart. J. Micr.
Sci. 104, 3rd Series: 57-68. Medler,
J. T. 1962. Development and absorption of eggs in bumblebees (Hymenoptera,
Apidae). Canad. Ent. 94: 825-33. Palm,
N. E. 1948. Normal and pathological histological studies on the ovary of Bombus natr (Hymenopt.) Opusc. ent. (Suppl.) 7: 1-101. Pfeiffer, I. W. 1945. Effect
of the corpora allata on the metabolism of adult female grasshoppers. J.
Exptal. Zool. 99: 183-233. Phipps,
J. 1966. Ovulation and oocyte resorption in Acridoidea (Orth.). Proc. Roy.
Ent. Soc. London
(A) 41: 78-84. Quezada, J. R. 1967. Biological
studies of Signiphora "borinquensis"
(Hymenoptera: Thysanidae), new species, a parasite of diaspine scales. M.S.
Thesis, University of California, Riverside. Richards,
J. G. & P. E. King. 1967. Chorion and vitelline membranes and their role
in resorbing eggs of the Hymenoptera. Nature, London 214: 601-02. Rockstein,
M. 1964. Physiology of Insects: Chap. 2: "Reproduction." Vol. I:
18-22. Academic Press, London. 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. Telfer, W. H. 1965. The
mechanism and control of yolk formation. Ann. Rev. Ent. 10: 161-72. Thomsen,
E. 1952. Functional significance of the neurosecretory brain cells and the
corpus allatum in the female blowfly, Calliphora
erythrocephala Meigen. J.
Exptal. Biol. 29: 137-72. Velthius,
H. H. W., F. M. Kluppell & G. A. H. Bossink. 1965. Some aspects of the
biology and population dynamics of Nasonia
vitripennis (Walker)
(Hymenoptera: Pteromalidae). Entomologia exp. appl. 8: 205-07. Weyer, F. 1927. Die rudimentaren
Keimdrusen im Lebensablauf der Arbeiter von Formica rufa
L. und Camponotus ligniperda Latr. mit
Berücksichtingung der übrigen sozialen Hymenopteren. Zool.
Anz. 74: 205-21. Weyer,
F. 1928. Ovaries of the workers in social Hymenoptera. Z. Wiss. Zool. 131: 345-501. Whiting,
A. R. 1940. American Naturalist 74: 468-71. Wigglesworth,
V. B. 1936. The function of the corpus allatum in the growth and reproduction
of Rhodnius prolixus (Hemiptera). Quart. J.
Microscience 79: 91-121. Wigglesworth,
V. B. 1948a. Functions of the corpus allatum in Rhodnius prolixus.
J. Exptal. Biol. 25: 1-15. Wigglesworth, V. B. 1948b. The hormonal regulation of growth
and reproduction in insects. Adv. in Insect Physiol. 2: 247-336. |