ELENA B. VINOGRADOVA 2007
DIAPAUSE IN AQUATIC INSECTS, WITH EMPHASIS ON MOSQUITOES

V. R. Alekseev et al. (eds.), Diapause in Aquatic Invertebrates, 83–113. © 2007 Springer.

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Diapause is the primary factor synchronizing insect life cycles with seasonal changes in the environment. Diapause is the major factor regulating the timing of growth, development, and reproduction, both before and after the period of dormancy. Many definitions of diapause may be found in the literature. Tauber et al. (1986) define diapause as “a neurohormonally mediated, dynamic state of low metabolic activity. Associated with this is a reduced morphogenesis, increased resistance to environmental extremes, and altered or reduced behavior activity. Diapause occurs during genetically determined stage(s) of metamorphosis, and its full expression develops in a species-specific manner, usually in response to a number of environmental stimuli that precede unfavourable conditions. Once diapause has begun, metabolic activity is suppressed even if conditions favorable for development prevail.” Aquatic insects are represented in many orders including the Diptera (Culicidae, Chironomidae, Simuliidae, Ceratopogonidae, Chaoboridae, Dixinae), Coleoptera, (Dytiscidae, Hydrophylidae), and Heteroptera (about 20 families); some orders such as Odonata, Ephemeroptera, and Trichoptera are exclusively aquatic. In most cases only immature stages of insects are true water inhabitants whereas the adults are terrestrial. Hibernation, diapausing stages, and induction and termination of diapause are studied in the mentioned insect groups to varying degrees. Among the aquatic insects, the most voluminous literature is devoted to the mosquitoes because of their medical and veterinary importance, thus the mosquitoes were selected as a model group for this discussion of diapause and controlling environmental factors. Diapause in other aquatic insects will be reviewed briefly at the end of this chapter. Though aquatic insects occur in specific habitats that cool more slowly in autumn, metamorphosis appears to be controlled by cues similar to those used by terrestrial insects. The photoperiod and temperature responses of aquatic insects are as broad as the range found in terrestrial species, though there may be greater flexibility in overwintering instars (Danks 1978). In mosquitoes the environmental control of diapause has been investigated from the early 1960s coinciding with the beginning of intensive studies in the field of seasonality, diapause, and photoperiodism in insects. The main ideas on this problem were reviewed by Lees (1955), Danilevsky (1961), Tauber et al. (1986), and Danks (1987). Mosquito diapause and its environmental control has been reviewed in monographs by Vinogradova (1969, 2000) and Mitchell (1988). The study of this topic in mosquitoes was additionally stimulated by the great applied importance of this taxa as active bloodsuckers and vectors of many agents 83  of medical and veterinary significance such as malaria, filariasis, and many arbovirus infections (yellow fever, Western equine, St. Louis, Japanese, and West Nile encephalitis). Phenological studies, which ascertain the dates of onset and termination of diapause, the period of reproductive activity, and number of generations provide predictive capabilities that are important for developing control tactics for mosquitoes. Data on the winter survival of mosquito females provide insights on the mechanism of arbovirus circulation and maintenance in nature. The study of diapause and its environmental control in mosquitoes, like other insects, is usually based both on the field observations and laboratory experiments, which require the use of laboratory colonies. It is important to note that only a few mosquito species, not more than 20 stenogamic species, are willing to mate in cages. The role of data concerning diapause and its regulation may be illustrated by the next examples. Progress with the elimination of malaria in the former USSR in the 1960s was possible only because many years (15–30 years) of observations had been devoted to the patterns of seasonal development of the Anopheles maculipennis complex in different climatic zones during autumn (Shipitsina 1957a, b). Aedes albopictus is another example. This species is a daytime biting mosquito known as a vector of dengue and haemorrhoidalis fever, and also a potential vector of a number of arboviruses, which it can transmit vertically or transversely, thereby providing a means for arbovirus maintenance and transmission. This native Asian mosquito occurs in China, the Pacific, and on islands of the Indian Ocean. A. albopictus has been rapidly spreading across all continents for the last decade: it is now established in North and South Americas, Africa, Oceania, and Europe (Knudsen 1995; Moore 1999). The international shipment of used tire provides A. albopictus with an ideal mechanism of dispersal, and tire stocks throughout much of the world constitute an extremely productive ecological niche for this mosquito to inhabit. It can breed in many different habitats within urban and suburban environments, as well as in perirural areas. The great applied importance of this species increases the interests of its biology and especially on the seasonal adaptations, which are responsible for its successful invasion into new regions. Temperate populations of A. albopictus overwinter as diapausing eggs, but tropical populations lack the ability to diapause, therefore they will not succeed when introduced into temperate zone. Currently about 2,500 mosquito species are known worldwide, and most inhabit tropical and subtropical regions, with the rest occurring in the temperate zones. Clearly diapause as an adaptation for hibernation is common in mosquitoes from northern and temperate latitudes. In mosquitoes three of the four known types of diapauses occur: diapause during the egg, larval, and adult stages. In northern regions including the USA, Canada, Europe, nontropical Asia including Japan, North Africa, and the Middle East, fewer than 300 species have been recorded, but hibernating stages are known only for a small number of these species. For instance, among mosquitoes distributed in North America and the former USSR with neighboring countries (Matheson 1944; Gutsevich et al. 1970), the majority of mosquito species enter an overwintering diapause as eggs (55 species), as adults (about 30 species), and as larvae (16 species). The seasonality of the rest (about 80 species) has not been studied. Some trends in the relationship between the diapausing stage and systematic position of mosquitoes are evident. Egg stage diapause is typical for Ochlerotatus, Aedes, and Psorophora; adult diapause occurs mainly in Anopheles, Culex, and Culiseta; larval diapause is encountered in distinct representatives of many genera such as Anopheles, Ochlerotatus, Culiseta, Mansonia, Orthopodomyia, Topomyia, Tripteroides, Armigeres, Wyeomyia, and Toxorhynchites. Only one diapausing stage is typical of most mosquito species, but a few may overwinter in two different stages in different parts of their distribution range. Egg and larval diapauses are encountered in O. togoi (Galka & Brust 1987a, b), O. triseriatus (Vinogradova 1967), O. caspius (Vinogradova 1975; Abdel-Rahman et al. 1985), and O. geniculatus (Sims & Munstermann 1983). An interesting case is O. sierrensis: in Oregon, USA, a single individual undergoes egg diapause in summer and larval diapause later, in winter (Jordan 1980a, b). In this chapter the terms “facultative” and “obligate” diapauses are used despite
their debatable character and difficulties in knowing for certain which type of diapause is occurring (Tauber et al. 1986; Danks 1987). These terms reflect variations in seasonal cycles of insects ranging from almost complete reliance upon environmental factors (monovoltinism or multivoltinism with environmental determinate facultative diapause) to genetic predominance (multivoltinism without any diapause) at one extreme, and monovoltinism with obligate diapause in each generation at the other extreme. 
In this chapter a new classification will be employed for the composite genus Aedes with elevation of the subgenus Ochlerotatus to generic rank (Reinert 2000; Snow & Ramsdale 2003; Darsie & Ward 2005).