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Insect Cold-Hardiness: to Freeze Or Not to Freeze Richard E. Lee, Jr. Bioscience, Vol. 39, No. 5

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Insect Cold-Hardiness: to Freeze Or Not to Freeze Richard E. Lee, Jr. Bioscience, Vol. 39, No. 5 Insect Cold-Hardiness: To Freeze or Not to Freeze Richard E. Lee, Jr. BioScience, Vol. 39, No. 5. (May, 1989), pp. 308-313. Stable URL: http://links.jstor.org/sici?sici=0006-3568%28198905%2939%3A5%3C308%3AICTFON%3E2.0.CO%3B2-8 BioScience is currently published by American Institute of Biological Sciences. Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/about/terms.html. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/journals/aibs.html. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. The JSTOR Archive is a trusted digital repository providing for long-term preservation and access to leading academic journals and scholarly literature from around the world. The Archive is supported by libraries, scholarly societies, publishers, and foundations. It is an initiative of JSTOR, a not-for-profit organization with a mission to help the scholarly community take advantage of advances in technology. For more information regarding JSTOR, please contact [email protected]. http://www.jstor.org Tue Jan 8 14:40:48 2008 Insect Cold-hardiness: To Freeze or Not to Freeze How insects survive low temperatures by Richard E. Lee, Jr. n temperate regions, few insects process of winter cold-hardening re- are able to avoid exposure to low The capacity to quires at least several weeks to com- I environmental temperatures dur- plete. ing the winter. Notable exceptions cold-harden is required include the monarch butterfly, which Two strategies. Overwintering insects for overwintering mav, migrateu more than 1000-milesto appear to use two major strategies, warmer climates, and the honeybee, depending on whether they can sur- which maintains constant hive tem- vive the freezing" of their bodv water. peratures near 35" C by behavioral Freeze-susceptible insects must avoid and physiological activities of the col- to survive long-term or short-term freezing; freeze-tolerant insects can ony (Heinrich 1981, Southwick and exposure to low temperature. This survive extracellular ice formation Heldmaier 1987). Other species avoid capacity varies as a function of the within their tissues. low-temperature extremes by vertical specific developmental stage, season FREEZE-SUSCEPTIBLEINSECTS. migration into the soil or the selection of the year, nutritional status, and the Freeze-susceptible (or freeze-intol- of protected hibernacula. However, duration of exposure. Physiological erant) species take advantage of su- for the many insects unable to avoid and biochemical processes that en- percooling. Small volumes of water, exposure to low temperatures, the hance low-temperature tolerance re- whether in organisms or not, can of- capacity to cold-harden is required sult in cold-hardening. ten be cooled many degrees below the for overwintering survival. The study of insect cold-hardiness melting point before spontaneous nu- Although many overwintering in- is a comparatively new one. Based on cleation. For example, 5-microliter sects seek protected overwintering his publications in the 1950s and samples of tap water commonly can sites in leaf litter or beneath the bark 1960s, R. W. Salt is generally credited be cooled to -18" C or lower. The of trees, the most cold-tolerant spe- as the first to examine rigorously on capacity to supercool decreases as cies are those that overwinter in biochemical and physiological levels volume increases and as the duration exposed sites, such as the Arctic cat- the nature of low-temperature toler- of exposure to subzero temperatures erpillar (Gynaephora), which over- ance in insects (Salt 1961, 1969). In- increases. Therefore. it should not be winters on rocky surfaces, or fly lar- terest in this area has grown steadily, surprising that insects, being essen- vae in plant galls that extend above as evidenced by the number of publi- tially small bags of water, have the the snowline, thus exposing their in- cations listed in two recent bibliogra- capacity to supercool extensively. In- habitants to the extremes of fluctua- phies on this subject (Baust et al. sects can sometimes avoid freezing tion in ambient temperatures (Ring 1982, Lee et al. 1986). This article until their temperature has fallen and Tesar 1981). provides a brief introduction to insect many degrees below the melting point Cold-hardiness or cold tolerance cold-hardiness with emphasis on of the body fluids (Figure 1). refers to the capacity of an organism some recent findings, including the The supercooling point is the tem- description of an extremely rapid perature at which spontaneous nucle- cold-hardening response protective ation occurs and the ice lattice begins Richard E. Lee, Jr., is an associate profes- against short exposures to cold. to grow. Even for small insects or sor in the Department of Zoology at " Miami University, Hamilton, Ohio their eggs, this value is easily mea- 45011. His cryobiological research fo- Overwintering cold-hardiness sured by using thermocouples to de- cuses on mechanisms of freeze tolerance tect the release of the heat of crystal- and low-temperature adaptation in insects To prepare for the cold of winter, lization. The heat usuallv dissi~ates and frogs. O 1989 American Institute of insects undergo a variety of physio- within a few minutes, and their body Biological Sciences. logical and biochemical changes. The temperatures decrease to the ambient 308 BioScience Vol. 39 No. 5 temperatures. INSECT RESPONSE TO LOW TEMPERATURE In preparation for overwintering, freeze-susceptible species, such as ladybugs and springtails (Collem- bola), commonly decrease their su- BODY TEMPERATU percooling point, thereby increasing the chance of winter survival (Figure 1). For this group, supercooling points often range in winter between -15" and -3.5" C (Sarmme 1982), al- MELTING POINT though some species from the interior OF BODY FLUIDS of Alaska supercool to approximately -60" C (Miller 1982). Evacuation of the gut, resulting in the removal of potential ice-nucleating agents, is be- lieved to be one mechanism of en- hancing supercooling capacity (Cannon and Block 1988). Also, endogenous ice-nucleating agents lo- cated in the tissues may be inactivated or masked during cold-hardening (Baust and Zachariassen 1983). In other species, water balance and des- iccation appear to influence the super- cooling point (Cannon et al. 1985). The insects also accumulate certain . chemicals, called cryoprotectants. FREEZE-TOLERANTINSECTS. Other insects are able to survive extensive extracellular ice formation within . body tissues and organs when tem- . peratures may fall as low as -70" C -60 (Miller 1982, Storey and Storey 1988). These freeze-tolerant insects, TIME such as the goldenrod gall fly (Eu- rosta solidaginis), commonly synthe- Figure 1. Responses of insects cooled to subzero temperatures. Insect body tempera- size ice-nucleating agents during win- tures (heavy line) in relation to the melting point, the supercooling point, and the ter cold-hardening. These unique nucleation of ice in body fluids. Although the bars on the right convey general ranges proteins or lipoproteins serve as cata- of insect response to low temperatures, the top of the bar for the range of freeze tolerance and the bottom of the bar for freeze avoidance correspond to the supercooling lysts for the extracellular nucleation point value illustrated in the center of the figure. However, a number of freeze-tolerant of ice in body fluids at temperatures insects have supercooling points in the range of -8" to -10" C, whereas some of -5" to -10" C (Duman et al. freeze-susceptible species supercool extensively, to -60" C or below. 1985). By limiting the amount of su- percooling, these proteins apparently serve to avoid lethal intracellular decrease in the size of unfrozen chan- concentrations corresponding to 25% freezing. nels in the extracellular space (Mazur of its body weight (Salt 1961). In Freeze tolerance refers to a specific 1984). some species, combinations of two or temperature range in which tissue more of these compounds are accu- freezing is tolerated; cooling below Cryoprotectants. One of the most re- mulated during cold-hardening. In that range may result in mortality markable characteristics of overwin- freeze-intolerant species, the tradi- from excessive cellular dehydration tering insects is their capacity to pro- tional view held that these antifreezes (Figure 1). Because only water mole- duce both sim~lecom~ounds and functioned primarily in a colligative cules join the ice lattice as it grows in proteins that act as antifreeze. Insects fashion (i.e., based on the number of the extracellular space, the remaining can accumulate large amounts of solute particles in solution), causing a extracellular solute becomes more glycerol, sorbitol, trehalose, or other depression in both the hernolymph concentrated. This process results in low-molecular-weight carbohydrates freezing point and the supercooling an osmotic gradient that removes wa- or polyols. These compounds, made point (Salt 1961, Zachariassen 1985). ter from the cells. Injury due to freez- by both freeze-susceptible and freeze- One of the most significant ad- ing results from excessive concentra- tolerant s~ecies. are referred to as vances in the last few years is the tion of solutes and cell shrinkage, and low-molecular-weight antifreezes or realization that low-molecular-weight more recently it has been suggested cryoprotectants. One larval wasp, polyols and sugars can protect biolog- that damage may be a function of the Bracon cephi, produces 5-M glycerol ical molecules and systems via non- May 1989 309 colligative mechanisms (Crowe et al.
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