DIAPAUSE IN DEVELOPMENTAL STAGES
AND THE IMAGO of Arthropods
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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).
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?
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