MODES OF SEASONAL ADAPTATION IN THE INSECTS: I. WINTER SURVIVAL

Abstract Factors affecting the winter survival of temperate-zone insects are reviewed. Certain species suffer high winter mortality especially in cold years, or in years with below normal amounts of insulating snow. Survival depends on the choice of winter microhabitat and on cold-hardiness, but also on biological features that have not previously been emphasized. These include behaviour that results in placement of overwintering eggs in less severe sites and manufacture of cocoons or other structures that retard inoculation by ice, or desiccation. The possible role of habitat heterogeneity in facilitating population survival is stressed. Microhabitats are characterized mainly with respect to temperature. They differ markedly among geographic areas and not only in midwinter conditions (including the extent of variation), but also in the time at which entry to the microhabitat in fall is necessary to avoid the risk of frost. The cues that govern entry into these microhabitats include negative phototaxis in many species but have not been subjected to quantitative analysis. Deeper layers are warmer in winter but warm up more slowly in spring and therefore some species, especially in arctic habitats where rapid vernal development is advantageous because the season is short, overwinter in superficial or insolated sites. Supposed mechanisms of cold- and freezing-injury and its avoidance are reviewed. There are several theories of freezing-injury: many modem theories focus on damage to the cell membrane, apparently caused by changes in cell volume induced during freezing. Injury is avoided by suppression of haemolymph nucleators (enhancing supercooling); or by a variety of methods, especially those involving solutes, minimising damage to frozen tissues. Among these solutes, the prevalence of glycerol in overwintering insects is not unexpected since glycerol is a normal metabolite in animals and can play several possible roles in cryoprotection. Cold-hardiness is metabolically costly because of these solute adjustments. The cold-hardiness of a taxon depends partly on climatic history during its evolution. Faunal composition at the highest latitudes reflects this dependence. The winter survival of many high-latitude insects varies rather widely from year to year; but the many detailed studies on cold-hardiness that have been made in the laboratory have seldom been related to natural mortality. The overwintering stage depends partly on the taxon. It is often fixed within a genus, but less closely within higher taxa. Proportionately more species overwinter as larvae at higher latitudes, especially when the life cycle lasts more than one year. Habitat also influences the overwintering stage: aquatic species generally overwinter as larvae, although species of temporary pools frequently overwinter as eggs. Overwintering in more than one stage is not common. This review suggests that winter survival of a group depends on latitude (or its climatic equivalent), habitat, and evolutionary history. It might therefore be especially useful to compare cold-hardiness, developmental rates, control of the life cycle and other features among species at the same latitude from each extreme of a series, that contrasts cold-hardy groups in stable habitats (such as Chironomidae) with aerial or vegetation dwelling groups that are not cold-hardy (such as Orthoptera). Future study of winter survival also demands more ecological data (overwintering stage, microhabitat, and conditions experienced there) for a larger sample of the fauna, and the simultaneous measurement of cold-hardiness.