Survival and energetic costs of repeated cold exposure in the Antarctic midge, <i>Belgica antarctica</i>: a comparison between frozen and supercooled larvae

Self Cite

SUMMARYDuring the austral summer, larvae of the terrestrial midge Belgica antarctica (Diptera: Chironomidae) experience highly variable and often unpredictable thermal conditions. In addition to remaining freeze tolerant year-round, larvae are capable of swiftly increasing their cold tolerance through the rapid cold-hardening (RCH) response. The present study compared the induction of RCH in frozen versus supercooled larvae. At the same induction temperature, RCH occurred more rapidly and conferred a greater level of cryoprotection in frozen versus supercooled larvae. Furthermore, RCH in frozen larvae could be induced at temperatures as low as -12°C, which is the lowest temperature reported to induce RCH. Remarkably, as little as 15min at -5°C significantly enhanced larval cold tolerance. Not only is protection from RCH acquired swiftly, but it is also quickly lost after thawing for 2h at 2°C. Because the primary difference between frozen and supercooled larvae is cellular dehydration caused by freeze concentration of body fluids, we also compared the effects of acclimation in dehydrated versus frozen larvae. Because slow dehydration without chilling significantly increased larval survival to a subsequent cold exposure, we hypothesize that cellular dehydration caused by freeze concentration promotes the rapid acquisition of cold tolerance in frozen larvae.

Section: Experimental Conditions For Assessing Larval Cold Tolerancementioning

confidence: 99%

“…Whether larvae of B. antarctica freeze inoculatively by contact with environmental ice or remain supercooled during an acute exposure to cold likely depends on hydric conditions of their microhabitat Teets et al, 2011). The primary purpose of our study was to compare the RCH response in frozen versus supercooled larvae.…”

Section: Introductionmentioning

confidence: 99%

The protective effect of rapid cold-hardening develops more quickly in frozen versus supercooled larvae of the Antarctic midge, Belgica antarctica

Kawarasaki

Teets

Denlinger

et al. 2013

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“…Many stressors generate oxidative stress in animals including: low and/or high temperature (Storey and Storey, 2010;An and Choi, 2010), freezing (Joanisse and Storey, 1998;Hermes-Lima and Storey, 1993;Hermes-Lima et al, 1998), dehydration (Franca et al, 2007;Clark et al, 2009;López-Martínez et al, 2009;Benoit, 2010;Rizzo et al, 2010), ultraviolet (López-Martínez et al, 2008;Meng et al, 2010) and gamma irradiation (Peng et al, 1986;Datkhile et al, 2009), anoxia-reperfusion (Hermes-Lima andStorey, 1996;Hermes-Lima et al, 1998;HermesLima et al, 2001) and hypoxia-reperfusion (Jamieson et al, 1986;Hermes-Lima et al, 2001). Stress from the accumulation of reactive oxygen species (ROS) and the resulting oxidative damage can have long-lasting effects on organismal performance, and organisms experience multiple bouts of oxidative stress throughout their lifetime, with some of these bouts involving simultaneous combinations of multiple stressors (Metcalfe and Alonso-Alvarez, 2010; Benoit et al, 2010;Teets et al, 2011;Marshall and Sinclair, 2011). Thus, an inducible and strong antioxidant response is crucial for organismal performance across many contexts, and organisms employ a suite of biologically active molecules that breakdown ROS.…”

Section: Introductionmentioning

confidence: 99%

Short-term anoxic conditioning hormesis boosts antioxidant defenses, lowers oxidative damage following irradiation and enhances male sexual performance in the Caribbean fruit fly, Anastrepha suspensa

López‐Martínez

Hahn

2012

SUMMARYMost organisms are repeatedly exposed to oxidative stress from multiple sources throughout their lifetimes, potentially affecting all aspects of organismal performance. Here we test whether exposure to a conditioning bout of anoxia early in adulthood induces a hormetic response that confers resistance to oxidative stress and enhances male sexual performance later in life in the Caribbean fruit fly, Anastrepha suspensa. Anoxic conditioning of adults prior to emergence led to an increase in antioxidant capacity driven by mitochondrial superoxide dismutase and glutathione peroxidase. When exposed to gamma irradiation, a strong oxidative stressor, males that received anoxic conditioning had lower lipid and protein oxidative damage at sexual maturity. Anoxia conditioning led to greater male sexual competitiveness compared with unconditioned males when both were irradiated, although there was no effect of anoxia conditioning on mating competitiveness in unirradiated males. Anoxia also led to higher adult emergence rates and greater flight ability in irradiation-stressed flies while preserving sterility. Thus, hormetic treatments that increased antioxidant enzyme activity also improved male performance after irradiation, suggesting that antioxidant enzymes play an important role in mediating the relationship between oxidative stress and sexual selection. Furthermore, our work has important applied implications for the sterile insect technique (SIT), an environmentally friendly method of insect pest control where males are sterilized by irradiation and deployed in the field to disrupt pest populations via mating. We suggest that hormetic treatments specifically designed to enhance antioxidant activity may produce more sexually competitive sterile males, thus improving the efficacy and economy of SIT programs. Supplementary material available online at

“…Some studies measured the actual cost of freezing during the freezing and thawing process, whereas others simply measured the effects of previous freezing on the MR of thawed animals. In invertebrates, Teets et al (Teets et al, 2011) found a decrease in energy stores when Belgica antarctica was exposed to repeated freezing, while Marshall and Sinclair (Marshall and Sinclair, 2011) did not find any change in MR or energy reserves after exposing P. isabella to repeated freezing. In frogs, the thawing process has been shown to be more energetically costly than the freezing process (Layne, 2000;Voituron et al, 2009;Sinclair et al, 2013).…”

Section: Energetic Costs Of Constant Freezing and Repeated Freezingmentioning

confidence: 96%

“…Churchill and Storey, 1989;Sinclair et al, 2004;Sinclair and Chown, 2005;Marshall and Sinclair, 2011;Teets et al, 2011;Sinclair et al, 2013). Some studies measured the actual cost of freezing during the freezing and thawing process, whereas others simply measured the effects of previous freezing on the MR of thawed animals.…”

Section: Energetic Costs Of Constant Freezing and Repeated Freezingmentioning

confidence: 99%

Effect of repeated freeze-thaw cycles on geographically different populations of the freeze tolerant wormEnchytraeus albidus(Oligochaeta)

Fisker

Holmstrup

Malte

et al. 2014

Freeze-tolerant organisms survive internal ice formation; however, the adaptations to repeated freeze-thaw cycles are often not well investigated. Here we report how three geographically different populations of Enchytraeus albidus (Germany, Iceland and Svalbard) respond to three temperature treatments -constant thawed (0°C), constant freezing (−5°C) and fluctuating temperature (0 to −5°C) -over a period of 42 days. Survival varied between treatments and populations such that enchytraeids from arctic locations had a higher survival following prolonged freeze periods compared with temperate populations. However, enchytraeids from temperate locations had the same survival rate as arctic populations when exposed to repeated freeze-thaw events. Across all populations, metabolic rate decreased markedly in frozen animals (−5°C) compared with thawed controls (0°C). This decrease is likely due to the lower temperature of frozen animals, but also to the transition to the frozen state per se. Animals exposed to repeated freeze-thaw events had an intermediate metabolic rate and freeze-thaw events were not associated with pronounced excess energetic costs. Overwintering under either condition was not associated with a decrease in lipid content; however, during exposure to constant freezing and repeated freeze-thaw events there was a noticeable decrease in carbohydrate stores over time. Thus, animals exposed to constant freezing showed a decrease in glycogen stores, while both glucose and glycogen content decreased over time when the organisms were exposed to repeated freezing. The results therefore suggest that carbohydrate resources are important as a fuel for E. albidus during freezing whereas lipid resources are of marginal importance.