Avoidance and tolerance of freezing in ectothermic vertebrates

Abstract

Ectothermic vertebrates have successfully colonized virtually every available ecological niche on Earth, some thriving in seasonally or continuously cold habitats at high latitudes and altitudes. In this commentary we briefly discuss adaptations of these animals to survive exposure to subzero temperatures and, in certain cases, the freezing of their body fluids.Excepting certain polar fishes, which swim in ice-laden waters, most aquatic species occupy habitats that are relatively warm. Accordingly, we here focus on terrestrial species whose body temperature (T b ) may fall appreciably below the equilibrium freezing/melting point (T Feq ) of their body fluids. Some of the key tenets of cold hardiness are best illustrated from invertebrates, which are more extensively researched than higher taxa. However, we liberally reference two of the best-studied and most cold-hardy vertebrates. The wood frog (Rana sylvatica), the most northerly distributed of North American amphibians, occurs within the Arctic Circle. Throughout its range, this species overwinters beneath forest duff where it encounters subzero cold but nevertheless survives the freezing of its tissues. The painted turtle (Chrysemys picta) is a cold-adapted reptile that ranges to within 7° latitude of the Arctic Circle. Hatchlings of this species commonly overwinter within the natal nest, only 5-10cm below the ground surface, but can survive chilling to temperatures as low as −4°C in the frozen state or −15°C by avoiding freezing. Winter thermal environmentAmong cold-hardy organisms, capacity for cold tolerance is tuned to the temperatures and exposure durations that a given species encounters within its habitat (Addo-Bediako et al., 2000). Thermal conditions in winter refugia vary markedly, the intensity and frequency of chilling excursions increasing with altitude and latitude, and decreasing with any insulation afforded by the microenvironment. In temperate regions, frogs overwintering on the forest floor may encounter minima of −5 or −7°C (MacArthur and Dandy, 1982;Schmid, 1982), although more severe chilling can occur in northerly regions. Temperatures ranging between −1 and −4°C were recorded in grass tussocks harboring European common lizards, Lacerta vivipara, during particularly cold periods with little snow cover (Grenot et al., 2000). Where snow cover is routinely sparse and winters severe, temperatures can be, but are not necessarily, extreme. At a given study site, thermal minima within C. picta nests can vary by 10°C or more, reflecting differences in nest depth, slope, aspect, patchiness of snow cover, and other physiognomic factors (Costanzo et al., 2004;Weisrock and Janzen, 1999). A common but erroneous perception is that all hibernators must endure a single, winter-long bout of extreme cold. The more accurate scenario, especially for animals using wellinsulated refugia, is for the temperature to hover near 0°C for extended periods that may (or may not) be punctuated by brief (i.e. hours to days) excursions to slightly lower temperatures be...

Hibernation physiology, freezing adaptation and extreme freeze tolerance in a northern population of the wood frog

“…Within their hibernacula, indigenous frogs are commonly exposed to -10°C or below (Middle and Barnes, 2000), consistent with conditions within subnivean habitats of Interior Alaska (Barnes et al, 1996). In contrast, R. sylvatica endemic to the Great Lakes Region in North America encounter more modest hibernal temperatures and tolerate freezing only to -3 to -6°C (Costanzo and Lee, 2013). Discovering the physiological basis of this variation could provide important clues to the evolution of the freeze-tolerance adaptation.…”

“…Glucose mobilized with freezing is cleared from most tissues, returned to the liver and reconverted to glycogen usually within 24-48h of thawing (Costanzo and Lee, 2013;Storey and Storey, 2004). Expectedly, glucose levels in blood and organs of Ohioan frogs returned to near-basal values within 5days after thawing began.…”

“…Throughout its range, R. sylvatica overwinters in relatively exposed sites on the forest floor, where it potentially encounters subzero temperatures but nevertheless survives the freezing of up to two-thirds of its body water (Costanzo and Lee, 2013;Storey and Storey, 2004). Freezing adaptation in northern populations of this species has not been thoroughly examined, although preliminary findings indicate that frogs collected near Fairbanks, Alaska, USA, tolerate profound freezing, with many surviving exposure to temperatures below -18°C (Middle and Barnes, 2001).…”

“…Two osmolytes paramount in freezing survival of R. sylvatica are urea, which accumulates during fall and early winter, and glucose, which is quickly and copiously mobilized from hepatic glycogen reserves in direct response to freezing. Both agents limit freezing injury by colligatively lowering the equilibrium freezing/melting point (FP eq ) of body fluids (and, hence, limiting ice formation), and by preserving the integrity of membranes and macromolecules (Costanzo and Lee, 2013;Storey and Storey, 2004). Cryoprotection is also conferred by a redistribution of water and its sequestration as ice within coelomic and lymphatic compartments, a process that limits intra-organ ice formation that could physically damage cells and tissues .…”

Host‐mediated shift in the cold tolerance of an invasive insect

“…Passionate discussion has surrounded the importance of gradients within and between these strategies, and how responses to cold could be further delineated (e.g., Bale, 1996; Chown, Sørensen, & Sinclair, 2008; Nedvěd, 2000; Sinclair, 1999). Broadly, though, evolutionary and geographic relationships distinguish groups that withstand freezing and those that do not (Addo‐Bediako, Chown, & Gaston, 2000; Sinclair, Addo‐Bediako, & Chown, 2003), with most evidence supporting freeze tolerance as a derived state from freeze avoidance (Costanzo & Lee, 2013; Vernon & Vannier, 2002; but see also Chown & Sinclair, 2010). …”