Survival strategies of freshwater insects in cold environments

J. Limnol., 63(Suppl. 1): 45-55, 2004 Survival strategies of freshwater insects in cold environments Valeria LENCIONI Section of Invertebrate Zoology and Hydrobiology, Museo Tridentino di Scienze Naturali, Via Calepina 14, I-38100 Trento, Italy e-mail address: ABSTRACT At high latitudes and altitudes, ice formation is a major variable affecting survival of freshwater fauna and hence the abundance and composition of invertebrate communities. Freezing, but also desiccation and anoxia, are lethal threats to all life stages of aquatic insects, from the eggs to the adults. During cold periods, the aquatic stages commonly remain in or move to a portion of the water body that will not freeze or dry (e.g., deep waters of lakes, springs and hyporheic zone) where they can remain active. Less frequently they migrate to habitats that will freeze at the onset of winter. Insects have developed a complex of strategies to survive at their physiological temperature minimum, comprising (a) morphological (melanism, reduction in size, hairiness/pubescence, brachyptery and aptery), (b) behavioural (basking in the sun, changes in feeding and mating habit, parthenogenesis, polyploidy, ovoviviparity, habitat selection and cocoon building), (c) ecological (extension of development to several years by quiescence or diapause and reduction of the number of generations per year), (d) physiological and biochemical (freezing tolerance and freezing avoidance) adaptations. Most species develop a combination of these survival strategies that can be different in the aquatic and terrestrial phase. Freezing avoidance and freezing tolerance may be accompanied by diapause. Both cold hardiness and diapause manifest during the unfavourable season and: (i) involve storage of food resources (commonly glycogen and lipids); (ii) are under hormonal control (ecdysone and juvenile hormone); (iii) involve a depression or suppression of the oxidative metabolism with mitochondrial degradation. However, where the growing season is reduced to a few weeks, insects may develop cold hardiness without entering diapause, maintaining in the haemolymph a high concentration of Thermal Hysteris Proteins (THPs) for the entire year and a slow but continuous growth. A synthesis of literature regarding adaptation strategies in aquatic insects is presented, highlighting the scarcity of information on freshwater insects from Alpine regions. Most references are on Diptera Chironomidae from North America and North Europe. Some recent findings on aquatic insects from Italian Alpine streams are also presented. Key words: freshwater insects, Chironomidae, temperature, diapause, hibernation, supercooling 1. INTRODUCTION "Insect cold hardiness: to freeze or not to freeze" (Lee 1989), "Insect cold hardiness: a matter of life and death" (Bale 1996) and "Life on the edge: insect ecology in arctic environments" (Strathdee & Bale 1998), are some of the most effective titles to highlight the difficulty of withstanding the rigors of winter in habitats that freeze, at high latitudes and altitudes. The ability of insects to face winter in a frozen state was first investigated in the 1930s, and has since been well documented for many taxa, mainly terrestrial, and by many researchers, mostly from North America (e.g., Downes 1965; Block 1980; Andrews & Rigler 1985; Lee & Denlinger 1991; Moore & Lee 1991; Irons et al. 1993; Danks 2000a). The interest of ecologists, zoologists, physiologists and biochemists in understanding the strategies adopted by insects to survive in cold environments has many reasons. Firstly, it was supposed that the evolution of most aquatic insects (e.g., Chironomidae, Empididae and Plecoptera) started in cold and running headwaters several hundred million years ago and the conquest of all the other habitats was secondary (Danks 1971a; Danks & Oliver 1972a). Their physiological adaptations may have been forged in their early evolutionary history and biogeographic patterns in taxonomic diversity (i.e. latitudinal and altitudinal gradients) could thus be related to the ability to survive subzero temperatures (Oswood et al. 1991; Rossaro 1991). Secondly, winter mortality is a major factor determining population dynamics of aquatic and terrestrial insects in polar and alpine regions (Oswood et al. 1991). Furthermore, investigation of the ecology and physiology of cold tolerance in insects has practical applications in understanding the overwinter survival of pest species in agriculture and forestry (Block 1990). Similarities were found between physiological and/or biochemical processes that determine resistance to cold, anoxia, desiccation and to chemical products as pesticides. These different resistance forms resulted to produce and accumulate the same or similar substances (i.e. the "stress" or "shock proteins"). Finally, the studies on insect cold hardiness find application in cryobiology (Block 1990). This paper aims to synthetize existing information on cold adaptations in freshwater insects living at high latitude and altitude, with some recent findings for the Italian Alps. 46 2. ENVIRONMENTAL CONSTRAINTS AT HIGH LATITUDE AND ALTITUDE Regions at high altitude and latitude share similar "extreme" environmental conditions, characterised by a high degree of harshness due to a combination of severity, seasonality, unpredictability and variability (Mani 1962; Danks 1999a). The limiting factors of these habitats are: extended period of snow/ice cover (from 6 to 10 months a year); short growing season (concentrated in the period free from ice/snow cover); reduced quantity and quality of food; high risk of drought; low precipitation; poor quality of the soil; strong winds and very low temperature with ample daily and seasonal excursions, especially in exposed terrestrial microhabitats, shallow ponds and small streams. In both terrestrial and water habitats, temperature is near the physiological minimum of insect life, and few species are able to adjust their metabolism to be active in these conditions and complete their life cycle. In the Arctic, air temperature may range from -50/-70 °C in winter to +10/+15 °C in summer, and that of temporary water bodies from -20 °C in winter to +20 °C in summer (Downes 1964, 1965; Oliver 1968; Danks et al. 1994; Strathdee & Bale 1998). A decrease in species richness and diversity occurs with increasing latitude and altitude, due to growing environmental harshness and isolation condition, to which low rates of colonisation, speciation and generally high extinction rate are also associated (Mani 1968; Ward & Stanford 1982; Downes 1988; Danks 1990; Stevens 1992; Ward 1994; Strathdee & Bale 1998; Füreder 1999). Freshwaters at high latitudes (Downes 1964, 1965) and altitudes (Brittain & Milner 2001; Lods-Crozet et al. 2001a; Maiolini & Lencioni 2001) are colonised mainly by Diptera Chironomidae for which adaptations to a variety of environmental rigors such as desiccation, anoxia, extremely high (...truncated)