Brief Chilling to Subzero Temperature Increases Cold Hardiness in the Hatchling Painted Turtle ( Chrysemys picta )

Rapid cold hardening (RCH) is a type of beneficial phenotypic plasticity that occurs on extremely short time scales (minutes to hours) to enhance insects' ability to cope with cold snaps and diurnal temperature fluctuations. RCH has a well-established role in extending lower lethal limits, but its ability to prevent sublethal cold injury has received less attention. The Antarctic midge, Belgica antarctica, is Antarctica's only endemic insect and has a well-studied RCH response that extends freeze tolerance in laboratory conditions. However, the discriminating temperatures used in previous studies of RCH are far below those ever experienced in the field. Here, we tested the hypothesis that RCH protects against non-lethal freezing injury. Larvae of B. antarctica were exposed to control (2°C), direct freezing (−9°C for 24 h) or RCH (−5°C for 2 h followed by −9°C for 24 h). All larvae survived both freezing treatments, but RCH larvae recovered more quickly from freezing stress and had a significantly higher metabolic rate during recovery. RCH larvae also sustained less damage to fat body and midgut tissue and had lower expression of two heat shock protein transcripts (hsp60 and hsp90), which is consistent with RCH protecting against protein denaturation. The protection afforded by RCH resulted in energy savings; directly frozen larvae experienced a significant depletion in glycogen energy stores that was not observed in RCH larvae. Together, these results provide strong evidence that RCH protects against a variety of sublethal freezing injuries and allows insects to rapidly finetune their performance in thermally variable environments.

Section: Introductionmentioning

confidence: 99%

Rapid cold hardening protects against sublethal freezing injury in an Antarctic insect

Teets

Kawarasaki

Potts

et al. 2019

“…Also, in tadpoles of the neotropical túngara frog Engystomops pustulosus a prior induction of chill coma (see Glossary) by cooling at 1.0°C min −1 slightly depresses CT min during a subsequent trial (Vo and Gridi-Papp, 2017). Similarly, some species of fish (Hazel and Landrey, 1988), salamanders (Layne and Claussen, 1987) and turtles (Muir et al, 2010) exhibit RHC-like responses. Thus, although RCH is less well studied outside of arthropods, it is tempting to speculate that rapid phenotypic plasticity at low temperature is a general feature of ectotherms.…”

Section: Ecological Relevance Of Rch the Rch Response Is Widespread Amentioning

confidence: 99%

Rapid cold hardening: ecological relevance, physiological mechanisms and new perspectives

Teets

Gantz

Kawarasaki

2020

Rapid cold hardening (RCH) is a type of phenotypic plasticity that allows ectotherms to quickly enhance cold tolerance in response to brief chilling (lasting minutes to hours). In this Review, we summarize the current state of knowledge of this important phenotype and provide new directions for research. As one of the fastest adaptive responses to temperature known, RCH allows ectotherms to cope with sudden cold snaps and to optimize their performance during diurnal cooling cycles. RCH and similar phenotypes have been observed across a diversity of ectotherms, including crustaceans, terrestrial arthropods, amphibians, reptiles, and fish. In addition to its well-defined role in enhancing survival to extreme cold, RCH also protects against nonlethal cold injury by preserving essential functions following cold stress, such as locomotion, reproduction, and energy balance. The capacity for RCH varies across species and across genotypes of the same species, indicating that RCH can be shaped by selection and is likely favored in thermally variable environments. Mechanistically, RCH is distinct from other rapid stress responses in that it typically does not involve synthesis of new gene products; rather, the existing cellular machinery regulates RCH through post-translational signaling mechanisms. However, the protective mechanisms that enhance cold hardiness are largely unknown. We provide evidence that RCH can be induced by multiple triggers in addition to low temperature, and that rapidly induced tolerance and cross-tolerance to a variety of environmental stressors may be a general feature of stress responses that requires further investigation.

“…Chilling injury in hatchling C. picta apparently does not reflect widespread membrane damage, but seems restricted to particularly sensitive cells, such as neurons. Muir et al (Muir et al, 2010a) examined brain tissue from cold-shocked turtles (i.e. held supercooled for 24h at -13°C), finding that the cells had sustained direct chilling injury.…”

Section: Supercooling As a Survival Strategymentioning

confidence: 99%

Avoidance and tolerance of freezing in ectothermic vertebrates

Costanzo

Lee

2013

110

111

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...