The impacts of repeated cold exposure on insects

Abstract

SummaryInsects experience repeated cold exposure (RCE) on multiple time scales in natural environments, yet the majority of studies of the effects of cold on insects involve only a single exposure. Three broad groups of experimental designs have been employed to examine the effects of RCE on insect physiology and fitness, defined by the control treatments: ʻRCE vs coldʼ, which compares RCE with constant cold conditions; ʻRCE vs warmʼ, which compares RCE with constant warm conditions; and ʻRCE vs matched coldʼ which compares RCE with a prolonged period of cold matched by time to the RCE condition. RCE are generally beneficial to immediate survival, and increase cold hardiness relative to insects receiving a single prolonged cold exposure. However, the effects of RCE depend on the study design, and RCE vs warm studies cannot differentiate between the effects of cold exposure in general vs RCE in particular. Recent studies of gene transcription, immune function, feeding and reproductive output show that the responses of insects to RCE are distinct from the responses to single cold exposures. We suggest that future research should attempt to elucidate the mechanistic link between physiological responses and fitness parameters. We also recommend that future RCE experiments match the time spent at the stressful low temperature in all experimental groups, include age controls where appropriate, incorporate a pilot study to determine time and intensity of exposure, and measure sub-lethal impacts on fitness.Supplementary material available online at

Survival of rapidly fluctuating natural low winter temperatures by High Arctic soil invertebrates

“…This insulation can allow the survival of species not capable of tolerating the minima experienced in unprotected habitats (Convey and Block 1996;Danks, 2007;Ávila-Jiménez et al, 2010;Bale and Hayward, 2010;Hågvar and Hågvar, 2011;Marshall and Sinclair, 2012;Legault and Weis, 2013), and is a feature of the richer and more diverse Svalbard habitats. A reduction in snow cover, for example associated with elevated winter evaporation rates, winter thaws, or increased storminess and wind redistribution, will result in reduced soil temperatures and potentially increased frequency of repeated cold events that are appreciated to be stressful for the underlying ecosystems and their component species (Groffman et al, 2001;Isard et al, 2007;Kreyling and Henry, 2011;Marshall and Sinclair, 2012;Pauli et al, 2013). However, it is unclear how invertebrates, which are fundamental to soil processes including organic soil formation, decomposition and nutrient recycling (Bardgett, 2005;Brussard et al, 2007;Brussard, 2012) will respond to such changes.…”

“…However, while these techniques provide much useful and consistent information about the cold tolerance of the studied animals, placing this in the context of true field conditions is often difficult as the parameters investigated -in particular relating to rate of temperature manipulation, frequency of repeated cold events, duration of cold exposure, and survival -often differ greatly from the natural situation (e.g. Coulson and Bale, 1996;Convey and Worland, 2000;Worland and Convey, 2001;Marshall and Sinclair, 2012).…”

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

“…To our knowledge, this is the first study that has directly tested for population differences in response to freezing and thawing cycles, although some previous studies have focused on variation in population responses to fluctuating temperatures on species that do not freeze (Ragland and Kingsolver, 2008;Kingsolver et al, 2009;Cooper et al, 2012;Marshall and Sinclair, 2012a). As reviewed by Marshall and Sinclair (Marshall and Sinclair, 2012a), the interpretation of the results of repeated cold exposure is often dependent on experimental design and therefore often difficult to compare across studies.…”

“…As reviewed by Marshall and Sinclair (Marshall and Sinclair, 2012a), the interpretation of the results of repeated cold exposure is often dependent on experimental design and therefore often difficult to compare across studies. This is also the case for comparisons across populations with regard to repeated cold exposure.…”

“…Despite an impressive array of adaptations to overcome freezing, freeze-tolerant organisms may still experience physical damage during freezing (particularly if freezing is severe, rapid or prolonged) (Bale, 2002;Lee, 2010;Marshall and Sinclair, 2012a). Furthermore, in some freeze-tolerant animals it has been found that the freeze-thaw events carry energetic costs associated with reestablishment of osmotic and ionic gradients, and re-synthesis of damaged proteins and cryoprotectants (Churchill and Storey, 1989;Marshall and Sinclair, 2011;Sinclair et al, 2013).…”