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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. |