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DIAPAUSE
IN DEVELOPMENTAL STAGES
AND
THE IMAGO of Arthropods
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Overview Diapause
refers to the state of arrested growth or reproduction that is typical of
many hibernating or aestivating arthropods (Lees 1956). One must distinguish
diapause from quiescence. Some borderline cases do occur, but certain
physiological mechanisms can be recognized in the diapausing insect which are
absent in the quiescent (Tauber & Tauber 1976). Harvey (1962) stated that
diapause is a state of developmental arrest which persists even when
environmental conditions are favorable for growth. In some insects the arrest
is facultative: environmental stimuli direct the organism either to continue
or to terminate development. In other insects the arrest is obligatory. In
both facultative and obligatory diapause, control over development is
exercised by the endocrine system (Beck 1968). The principal
stimulus for the onset of diapause is photoperiod, although temperature,
water and diet may be involved. Diapause may terminate abruptly when the
brain regains its full function. All insect stages may enter diapause. In the
larva and pupa diapause is an arrest in molting controlled by the
brain-thoracic gland system. In adult insects diapause is characterized by an
inhibition in the maturation of eggs associated with corpus allatum failure
(deWilde & Boer 1961). Diapause in the early embryo of Melanoplus differentialis involves an interruption in embryogenesis. Each of the
following endocrine organs of insects is associated with some form of
diapause: (1) brain-thoracic gland, (2) corpus allatum and (3) subesophagael
ganglion. It is recognized that insect diapause is an endocrine deficiency
syndrome of the prothoracic glands (or the corpora allata). There is little
doubt that diapause found in the growing stages is due to a temporary absence
of neurosecretory activity in the brain. The the case of adult diapause there
may be active inhibition of the corpora allata (deWilde 1962). Direct and Indirect Action
of Photoperiod.--In
parasitic insects, development is in many cases dependent upon the
physiological state of the host. In some instances, however, parasitoids have
their own independent photoperiodic responses. In Apanteles glomeratus
(L.) reared on Pieris brassicae and in Apanteles spurius Wesmael reared on several different species of hosts,
pupal diapause is determined by the photoperiod applied during the larval
stage (Danilevskii 1961, deWilde 1962). There also may be interactions of
photoperiod with temperature as found in Neodiprion
sertifer (Geoffroy)
(Sullivan & Wallace 1967). It is possible to select photoperiods
that induce diapause in the parasitoid, the host remaining in the active
stage (Geyspitz & Kyao 1953). In Pteromalus
puparum (L.) reared on Pieris brassicae, Pieris
napi (L.) and Pieris rapae (L.), photoperiodic responses of the host and
parasitoid are difficult to separate. But in P. napi,
rearing the pupa at 17°C in a 12-hr day induces diapause in 100% of the
parasitoids without interfering with the development of the host pupa
(Maslennikova 1958). Perception of the Photoperiod.--The insect's eyes may be involved in perception, but the brain is probably directly involved
in receiving the stimulus through the body of the insect directly (deWilde
1962). Photoperiodicity in Geographic Races.--Photoperiod
is one of the most important isolating factors in intraspecific geographical
differentiation and, hence, in insect evolution. Photoperiodic response in
local strains of an insect species may differ according to the geographical
latitude at which they occur without being accompanied by distinguishing
morphological features. These strains may differ in intensity of response, in
the effect of temperature on the response and in the critical photoperiod. Increasing
latitude causes local insect populations to be more univoltine and showing
more obligatory diapause. Moreover, photoperiod-induced diapause tends to be
more intense in populations of high latitudes. Seasonal Forms and Activities Controlled
by Photoperiod.--There
are two forms: (1) long-day
and (2) short-day. Seasons
exert their influence according to the particular form.
Sensitive Stages.--Sensitivity
is never extended to the whole life cycle in insects. All stages except the
pupa may be receptive, but in most cases sensitivity is intensified in a
limited number of instars. The sensitive stage and the responsive stage are
usually different (Ryan 1965). In Hippelates
eye gnats the egg enters diapause following a period of desiccation (Legner, Olton & Eskafi 1966). Larvae of the navel
orangeworm, Amyelois transitella, enter diapause following a period of
drought (Legner 1983). The causes of diapause in parasitic
Hymenoptera are not simple. In many species the individuals may enter a state
of diapause at a time when the environment is favorable to continuous
development and increase of the species (Flanders 1944, 1972; Simmonds 1948). Photoperiodic Induction.--There
are generally two rates of induction found in insects: one where the required
level is gradually built-up and the other where a few to many cycles are
required. Diapause can be easily reversed by periods promoting normal
activity. Of course this depends upon at what stage the insect is at the
time. Temperature
effects on diapause are variable (Saunders 1967, 1968) and temperature may
also affect the induction of diapause through photoperiodic influences
(Sullivan & Wallace 1967). High temperatures tend to avert diapause in
long-day species, although low temperatures may avert diapause in some cases
also. Apparently temperatures are important in determining whether or not
photoperiod can act. Temperature and photoperiod act differently on different
developmental stages to cause diapause (Eskafi & Legner 1974). Diapause
Termination The duration
of diapause is extremely variable among species. Nine days to 200 days and
even 12 years (e.g., Sitodiaplosis
sp. midge) are known. A general
requisite for breaking diapause is the taking up of water from the
environment, which is probably related to the increasing metabolic activity
of awakening insects. The effects
of temperature are variable. Tropical species require generally a higher
temperature to break diapause than do temperate species. Diapause
in Parasitic Insects Specifically There is
considerable variability in the expression of diapause among parasitic
insects. The following examples give some of the more commonly expected
behaviors: The eggs of
parasitoids deposited in host larvae usually hatch, but the parasitoid larvae
do not undergo further development until the host forms the puparium.
Examples are found in Diplazon
fissorius Grav., Stilpnus anthomyiidiperda, Tachinaephagus
zealandicus, Agathis lacticinctus, Figites
spp. and Phygadeuon spp.
Sometimes this behavior is regarded as a form of quiescence rather than
actual diapause, however. Some
parasitoids additionally exhibit a second form of arrest, a definite diapause
which is expressed at the end of the last larval instar after the host has
been consumed. Certain Diptera which serve as hosts for hymenopterous
parasitoids form their puparia prematurely in the fall when parasitized.
Varley & Butler (1933) observed this in parasitized larvae of a
chloropid. Parker (1935)
showed that the larva of the satin moth parasitized by Apanteles solitarius
(Ratzeburg) terminate their diapause earlier than do unparasitized larvae.
Schneider (1950, 1951) showed that Diplazon
pectoratorius (Thunberg)
caused premature pupation in its syrphid host. The induced pupation was the
direct action of a substance secreted by the parasitoid. Parasitoids attacking the pink
bollworm are stimulated to enter diapause along with their host (Legner 1983). Endocrine Processes Involved.--It
is now recognized that insect diapause is an endocrine deficiency syndrome of
the prothoracic glands (or the corpora allata). There is little doubt that
diapause found in the growing stages is due to a temporary absence of
neurosecretory activity in the brain. In the case of adult diapause, there
may be active inhibition of the corpora allata (deWilde 1982). Doutt (1959)
believed that the intervention of diapause in some stage of the life cycle of
a parasitic species is often essential if there is to be synchronization of
development between host and parasitoid. Theories and Experiments.--Flanders (1944) considered diapause in parasitoids to be adaptive in that it delays
development until the host attains the stage presumably most suitable for the
nutritional requirements of the parasitoid. Simmonds (1946, 1947, 1948),
however, considered diapause as due to some physiological maladjustment during development. He did not
consider diapause as adaptive so as to enable a species to survive a period
unfavorable to further growth, but rather a pathological state due to previous environmental or intrinsic
influences. [Also see Etzel &
Legner 1999] The causes of
diapause in parasitic Hymenoptera are not simple. In many species the
individuals may enter a state of diapause at a time when the environment is
favorable to continuous development and increase of the species (Flanders
1944, Simmonds 1948). The
physiological state of the parent female prior to and at the time of
oviposition can influence the proportion of her progeny that enter diapause
(Simmonds 1946, 1947, 1948, Saunders 1962, 1965, 1966a,b). In Spalangia drosophilae Ashmead, as the female ages a decreasing
percentage of her progeny enter diapause. In the ichneumonid Cryptus inornatus Pratt , progeny from females which in
development had passed through a period of diapause showed a much lower
incidence of diapause than did progeny from females which had developed
without diapause. If the adult female's life were prolonged by a change in
diet, diapausing progeny were increased from 2.5% to 36.5%. Simmonds also
found in S. drosophilae that diapause
incidence increased if low temperatures prevailed during development. In Cryptus, diapause increased if
the quality of the larval food was changed in the form of providing an
unnatural host. Schneiderman
and Horwitz (1958) supported Simmonds' findings of the influence of maternal
physiology on diapause in the progeny. Schneiderman believed that the trigger
stimulus acts at an early stage in the life cycle while actual diapause is
not manifested until much later. Exposing female Nasonia vitripennis
to low temperatures during ovigenesis caused diapause in the offspring at the
end of the last larval instar. Temperatures below 15°C were necessary to
break diapause in larval Nasonia. It seems well
established that in some endoparasitic species diapause is induced only by
being in hosts that are themselves in a condition of diapause (Doutt 1959).
An example in Trichogramma cacoeciae Marchal which
parasitizes eggs of Archips rosana L. Flanders
(1942, 1944) considered the undeposited yolk-free eggs of many species as
being in a state of diapause which permits them to be stored in oviducts or
modified portions of the ovary. Further development is dependent on immersion
in the nutrient body fluids of the host. Doutt (1959) suggested that this may
be quiescence rather than diapause.
Metaphycus helvolus Compere is forced into imaginal
diapause when it is isolated from its host for two r three weeks
(Flanders 1942, 1944). Ovisorption is complete and diapause is broken only
when the female can feed on the body fluids of the host. The term
"imaginal diapause" should probably be limited to obligatory
resting stages such as occur in Tiphia
vernalis Rohwer (Clausen
& King 1927) and in Porizon
parkeri Blanchard (Parker et
al. 1950). The
reproductive arrest that occurs in Peridesmia
sp. and Cedria paradoxa Wilkinson and in
social Hymenoptera, is a facultative phenomenon known as phasic castration (sometimes called agravidity). Andrewartha
(1952) agreed that diapause in the adult stage may take the form of a failure
to ripen eggs or sperm and may be manifest by an extended preoviposition
period. He cited work of Skoblo (1941) on Habrobracon
brevicornis (Wesmael). The
preoviposition period of the adult was greatly prolonged by subjecting the
feeding larvae to temperatures in the lower ranges. In the navel orangeworm, Amyelois transitella, variable percentages of field collected
larvae enter diapause. Three of its imported parasites, Pentalitomastix and two Goniozus spp. also enter diapause with their host.
Diapause seems triggered by several seasonally varying factors, and there are
possibly latitudinal effects present (Gal 1978, Legner 1983). Exercise 23.1--What is diapause? Distinguish it from quiescence? Exercise 23.2--What causes the diapause condition? What stages are
effected? Exercise 23.3--How may photoperiod be involved with diapause? Exercise 23.4--How may diapause be broken? Exercise 23.5--Can you think of ways in which diapause might be
useful in biological control work? REFERENCES: [ Additional references may be found
at MELVYL Library ] Andrewartha, H. G.
1952. Diapause in relation to the ecology of insects. Biol. Rev. 27: 50-107. Beck, S. D. 1968.
Insect Photoperiodism. Acad. Press, London. 188 pp. Bellows, T. S., Jr.
& T. W. Fisher, (eds) 1999. Handbook of Biological Control: Principles
and Applications. Academic Press, San Diego, CA. 1046.p. Danilevskii, A. S.
1961. Photoperiodism and seasonal development of insects. Oliver & Boyd
Ltd., Edinburgh & London. 383 p. deWilde,
J. & J. A. deBoer. 1961. Physiology of
diapause in the adult Colorado beetle. II. Diapause as a case of
pseudo-allatectomy. J. Insect Physiol. 6: 152-61. Doutt, R. L. 1959. The
biology of parasitic Hymenoptera. Ann. Rev. Ent. 4: 141-182. 1974 Eskafi, F. M. & E. F. Legner. 1974. Fecundity, development and diapause in Hexacola sp. near websteri, a parasite of Hippelates
eye gnats. Ann.
Entomol. Soc. Amer. 67(5): 769-771.Flanders, S. E. 1944. Diapause
in the parasitic Hymenoptera. J. Econ. Ent. 37: 408-11. 264. Etzel, L. K. & E. F. Legner. 1999. Culture and Colonization. In: T. W. Fisher & T. S. Bellows, Jr.
(eds.), Chapter 15, p. 125-197, Handbook
of Biological Control: Principles and
Applications. Academic Press, San
Diego, CA 1046 p. Flanders,
S. E. 1972. The duality of imaginal
diapause inception in pteromalids parasitic on Hypera postica.
Ann.
Ent. Soc. Amer. 65: 105-08. Gal,
A. 1978. Der Einfluss der Temperatur auf die Fruchtbarkeit, Entwicklungs- und
Uberlebensrate von Paramyelois
transitella (Lep.,
Pyralidae). Mitt. Dtsch. ges. Algem. Angew. Ent. 1: 265-69. Geyspitz,
K. F. & I. I. Kyao. 1953. The
influence of the length of illumination on the development of certain
braconids (Hymenoptera). Entomol. Oboz. 33: 32-35. [in Russian]. Harvey, W. R. 1962. Metabolic
aspects of insect diapause. Ann. Rev. Ent. 7: 57-80. Hodek,I. 1965. Several
types of induction and completion of adult diapause. Proc. 12th Intern.
Congr. Ent. (1964): 431-32. Lees, A. D. 1956. The physiology and
biochemistry of diapause. Ann. Rev. Ent. 1: 1-16. 1979 Legner, E. F. 1979. Emergence
patterns and dispersal in Chelonus
spp. near curvimaculatus and Pristomerus hawaiiensis, parasitic on Pectinophora
gossypiella. Ann. Entomol. Soc. Amer. 72(5): 681-686. 1983 Legner, E. F. 1983. Patterns of field
diapause in the navel orangeworm (Lepidoptera: Phycitidae) and three imported
parasites. Ann. Entomol. Soc. Amer.
76(3): 503-506. 1966 Legner, E. F., G. S. Olton & F. M.
Eskafi. 1966. Influence of physical factors on the
developmental stages of Hippelates collusor in relation
to the activities of its natural parasites.
Ann. Entomol. Soc. Amer. 59(4):
851-861. Maslennikova, V. A.
1958. On the conditions determining the diapause in the parasitic
Hymenoptera, Apanteles glomeratus L. (Braconidae) and Pteromalus puparum (Chalcididae). Rev. Ent. 37: 538-45. Ryan, R. B. 1965. Maternal
influence on diapause in a parasitic insect, Coeloides brunneri
Vier. (Hymenoptera, Braconidae). J. Insect Physiol. 11: 1331-36. Saunders, D. S. 1962b.
The effect of age of female Nasonia
vitripennis (Walker)
(Hymenoptera, Pteromalidae) upon the incidence of larval diapause. J. Insect
Physiol. 8:
309-18. Saunders,
D. S. 1964. Rearing tsetse-fly
parasites in blowfly puparia. Bull. Wld. Hlth. Org. 31: 309-10. Saunders,
D. S. 1965. Dispause of maternal
origin. Proc. 12th Internatl. Cong. Ent., London 1964. p. 182. Saunders,
D. S. 1965a. Larval diapause induced
by maternally-operating photoperiod. Nature, London 206(4985): 739-40. Saunders, D. S. 1965b.
Larval diapause of maternal origin: induction of diapause in Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae). J. Expt.
Biol. 42: 495-508. Saunders,
D. S. 1966a. Larval diapause of
maternal origin. - II. The effect of photoperiod and temperature on Nasonia vitripennis. J. Insect Physiol. 12: 569-81. Saunders,
D. S. 1966b. Larval diapause of
maternal origin. - III. The effect of host shortage on Nasonia vitripennis.
J. Insect Physiol. 12:
899-908. Saunders,
D. S. 1967. Time measurement in
insect photoperiodism: reversal of photoperiodic effect by chilling. Science
156(3778): 1126-27. Saunders, D. S. 1968.
Photoperiodism and time measurement in the parasitic wasp, Nasonia vitripennis. J. Insect Physiol. 14: 433-50. Saunders,
D. S. 1973. Thermoperiodic control
of diapause in an insect: theory of internal coincidence. Science, Wash.,
D.C. 181(4097): 358-60. Saunders,
D. S. 1974. Evidence for
"daw" and "dusk" oscillators in the Nasonia photoperiodic clock. J. Insect Physiol 20: 77-88. Saunders,
D. S. 1974. Spectral sensitivity
and intensity thresholds in Nasonia
photoperiodic clock. Nature, London 253(5494): 732-34. Saunders, D. S. 1978.
Internal and external coincidence and the apparent diversity of photoperiodic
clocks in the insects. J. Comp. Physiol. A-127: 197-207. Saunders, D. S. 1981.
Insect photoperiodism-- the clock and the counter: a review. Physiol. Ent. 6:
99-116. Saunders, D. S. &
D. Sutton. 1969. Circadian rhythms in the insect photoperiodic clock. Nature,
London 221(5180): 559-61. Saunders, D. S., D.
Sutton & R. A. Jarvis. 1970. The effect of host species on diapause
induction in Nasonia vitripennis. J. Insect Physiol.
16:
405-16. Schneiderman,
H. A. & J. Horwitz. 1958. The induction and
termination of facultative diapause in the chalcid wasps Mormoniella vitripennis
(Walker) and Tritneptis klugii (Ratzeburg). J. Expt.
Biol. 35: 520-51. Schneiderman,
H. A., J. Horwitz & C. G. Kurland. 1956a.
An analysis of the action of low temperatures in terminating the diapause of Mormoniella. Anat. Rec. 125: 557. Schneiderman,
H. A., J. Kuten & J. Horwitz. 1956b.
Effect of x-irradiation on the postembryonic development of a chalcid wasp. Anat. REc. 125: 625-26. Schneiderman,
H. A., J. Weinstein & J. Horwitz. 1957.
Recovery of diapausing larvae of a chalcid wasp from x-radiation. Anat. Rec.
128: 618-19. Simmonds, F. J. 1946. A
factor affecting diapause in hymenopterous parasites. Bull. Ent. Res. 37:
95-7. Simmonds, F. J. 1947.
Some factors influencing diapause. Canad. Ent. 89: 226-32. Simmonds, F. J. 1948.
The influence of maternal physiology on the incidence of diapause. Philo.
Trans. Roy. Soc. London, Ser. B, 233(603): 385-414. Sullivan, C. R. &
D. R. Wallace. 1967. Interaction of temperature and photoperiod in the
induction of prolonged diapause in Neodiprion
sertifer. Canad. Ent. 99: 834-50. Tauber,
M. J. & C. A. Tauber. 1976. Insect
seasonality: diapause maintenance, termination and post diapause development.
Ann. Rev. Ent. 21: 81-107. Walker, I. & D.
Pimentel. 1966. Correlation between longevity and incidence of diapause in Nasonia vitripennis Walker
(Hymenoptera, Pteromalidae). Gerontologia 12: 89-98. |