Are the Antarctic dipteran, Eretmoptera murphyi, and Arctic collembolan, Megaphorura arctica, vulnerable to rising temperatures?

Polar terrestrial invertebrates are suggested as being vulnerable to temperature change relative to lower latitude species, and hence possibly also to climate warming. Previous studies have shown Antarctic and Arctic Collembola and Acari to possess good heat tolerance and survive temperature exposures above 30 °C. To test this feature further, the heat tolerance and physiological plasticity of heat stress were explored in the Arctic collembolan, Megaphorura arctica, from Svalbard and the Antarctic midge, Eretmoptera murphyi, from Signy Island. The data obtained demonstrate considerable heat tolerance in both species, with upper lethal temperatures ≥35 °C (1 h exposures), and tolerance of exposure to 10 and 15 °C exceeding 56 days. This tolerance is far beyond that required in their current environment. Average microhabitat temperatures in August 2011 ranged between 5.1 and 8.1 °C, and rarely rose above 10 °C, in Ny-Ålesund, Svalbard. Summer soil microhabitat temperatures on Signy Island have previously been shown to range between 0 and 10 °C. There was also evidence to suggest that E. murphyi can recover from high-temperature exposure and that M. arctica is capable of rapid heat hardening. M. arctica and E. murphyi therefore have the physiological capacity to tolerate current environmental conditions, as well as future warming. If the features they express are characteristically more general, such polar terrestrial invertebrates will likely fare well under climate warming scenarios.

The effect of acclimation temperature on thermal activity thresholds in polar terrestrial invertebrates.

In the Maritime Antarctic and High Arctic, soil microhabitat temperatures throughout the year typically range between -10 and +5 °C. However, on occasion, they can exceed 20 °C, and these instances are likely to increase and intensify as a result of climate warming. Remaining active under both cool and warm conditions is therefore important for polar terrestrial invertebrates if they are to forage, reproduce and maximise their fitness. In the current study, lower and upper thermal activity thresholds were investigated in the polar Collembola, Megaphorura arctica and Cryptopygus antarcticus, and the mite, Alaskozetes antarcticus. Specifically, the effect of acclimation on these traits was explored. Sub-zero activity was exhibited in all three species, at temperatures as low as -4.6 °C in A. antarcticus. At high temperatures, all three species had capacity for activity above 30 °C and were most active at 25 °C. This indicates a comparable spread of temperatures across which activity can occur to that seen in temperate and tropical species, but with the activity window shifted towards lower temperatures. In all three species following one month acclimation at -2 °C, chill coma (=the temperature at which movement and activity cease) and the critical thermal minimum (=low temperature at which coordination is no longer shown) occurred at lower temperatures than for individuals maintained at +4 °C (except for the CTmin of M. arctica). Individuals acclimated at +9 °C conversely showed little change in their chill coma or CTmin. A similar trend was demonstrated for the heat coma and critical thermal maximum (CTmax) of all species. Following one month at -2 °C, the heat coma and CTmax were reduced as compared with +4 °C reared individuals, whereas the heat coma and CTmax of individuals acclimated at +9 °C showed little adjustment. The data obtained suggest these invertebrates are able to take maximum advantage of the short growing season and have some capacity, in spite of limited plasticity at high temperatures, to cope with climate change.

Pre-adapted to the maritime Antarctic?--rapid cold hardening of the midge, Eretmoptera murphyi.

During the 1960s, the midge, Eretmoptera murphyi, was transferred from sub-Antarctic South Georgia (55°S 37°W) where it is endemic to a single location on maritime Antarctic Signy Island (60°S 45°W). Its distribution has since expanded considerably, suggesting that it is pre-adapted to the more severe conditions further south. To test one aspect of the level of its pre-adaptation, the rapid cold hardening (RCH) response in this species was investigated. When juvenile (L1-L2) and mature (L3-L4) larvae of E. murphyi were directly exposed to progressively lower temperatures for 8h, they exhibited Discriminating Temperatures (DTemp, temperature at which there is 10-20% survival of exposed individuals) of -11.5 and -12.5°C, respectively. The mean SCP was above -7.5°C in both larval groups, confirming the finding of previous studies that this species is freeze-tolerant. Following gradual cooling (0.2°Cmin(-1)), survival was significantly greater at the DTemp in both larval groups. The response was strong, lowering the lower lethal temperature (LLT) by up to 6.5°C and maintaining survival above 80% for at least 22h at the DTemp. RCH was also exhibited during the cooling phase of an ecologically relevant thermoperiodic cycle (+4°C to -3°C). Mechanistically, the response did not affect freezing, with no alteration in the supercooling point (SCP) found following gradual cooling, and was not induced while the organism was in a frozen state. These results are discussed in light of E. murphyi's pre-adaptation to conditions on Signy Island and its potential to colonize regions further south in the maritime Antarctic.

Insect overwintering in a changing climate.

Insects are highly successful animals inhabiting marine, freshwater and terrestrial habitats from the equator to the poles. As a group, insects have limited ability to regulate their body temperature and have thus required a range of strategies to support life in thermally stressful environments, including behavioural avoidance through migration and seasonal changes in cold tolerance. With respect to overwintering strategies, insects have traditionally been divided into two main groups: freeze tolerant and freeze avoiding, although this simple classification is underpinned by a complex of interacting processes, i.e. synthesis of ice nucleating agents, cryoprotectants, antifreeze proteins and changes in membrane lipid composition. Also, in temperate and colder climates, the overwintering ability of many species is closely linked to the diapause state, which often increases cold tolerance ahead of temperature-induced seasonal acclimatisation. Importantly, even though most species can invoke one or both of these responses, the majority of insects die from the effects of cold rather than freezing. Most studies on the effects of a changing climate on insects have focused on processes that occur predominantly in summer (development, reproduction) and on changes in distributions rather than winter survival per se. For species that routinely experience cold stress, a general hypothesis would be that predicted temperature increases of 1 degree C to 5 degrees C over the next 50-100 years would increase winter survival in some climatic zones. However, this is unlikely to be a universal effect. Negative impacts may occur if climate warming leads to a reduction or loss of winter snow cover in polar and sub-polar areas, resulting in exposure to more severe air temperatures, increasing frequency of freeze-thaw cycles and risks of ice encasement. Likewise, whilst the dominant diapause-inducing cue (photoperiod) will be unaffected by global climate change, higher temperatures may modify normal rates of development, leading to a decoupling of synchrony between diapause-sensitive life-cycle stages and critical photoperiods for diapause induction. In terms of climate warming and potential heat stress, the most recent predictions of summer temperatures in Europe of 40 degrees C or higher in 50-75 years, are close to the current upper lethal limit of some insects. Long-term data sets on insect distributions and the timing of annual migrations provide strong evidence for 'positive' responses to higher winter temperatures over timescales of the past 20-50 years in North America, Europe and Asia.

Temporal expression patterns of diapause-associated genes in flesh fly pupae from the onset of diapause through post-diapause quiescence.

Distinct differences in the temporal expression patterns of genes associated with pupal diapause were noted in the flesh fly, Sarcophaga crassipalpis. The first change observed was a decline in expression of the gene encoding heat shock protein 90 (hsp90) 2 days after pupariation (1 day before the pupa reaches the phanerocephalic stage characteristic of diapause). In contrast, hsp23 and hsp70 transcripts were undetectable in nondiapause samples and d1-d4 diapause-programmed pupae, but were up-regulated just after the start of diapause, 5 days after pupariation. An increase of glycerol content in diapausing pupae was also noted at the start of diapause. The gene encoding proliferating cell nuclear antigen (pcna) was diapause down-regulated, and this occurred in two phases, with the first decline in expression 7 days after pupariation and a second decline in the level of expression on day 14. For pupae held at 20 degrees C for 20 days and transferred to 10 degrees C, diapause ended after 90-100 days at the lower temperature. However, pupae remained in a state of post-diapause quiescence (d100-d150) and sustained diapause-like hsp and pcna expression patterns until adult development was initiated. Glycerol concentrations and survival declined during the post-diapause phase. This study suggests a distinct sequence in the pattern of gene expression at the onset of diapause, but the genes we have monitored do not contribute to the switch to covert developmental potential at the transition from diapause to post-diapause quiescence.

Geographical and diapause-related cold tolerance in the blow fly, Calliphora vicina.

Three geographical strains of the blow fly, Calliphora vicina, were tested for cold tolerance at 0 degrees, -4 degrees and -8 degrees C. Survival to eclosion after 1 to 18 days of cold exposure was greater for diapause-destined larvae than for nondiapause-destined larvae of the two northern strains (Nallikari, Finland 65 degrees N and Edinburgh, Scotland 55 degrees N) but not for the southernmost strain (Barga, Italy 44 degrees N) where no clear differences were apparent. Diapause-destined larvae of the Edinburgh strain were more cold tolerant than those from Nallikari, at both -4 degrees and -8 degrees C, a difference possibly attributable to the long-lasting snow cover in the more northern locality, which might insulate the overwintering soil microclimate. At 0 degrees C, however, Nallikari larvae were more cold tolerant than Edinburgh or Barga. This was also the case for nondiapause-destined larvae, indicating that cold tolerance may occur, in part, independently of the diapause programme. In all three strains diapausing larvae were more cold tolerant than same-age (nondiapausing) pupae. For Nallikari, but not Barga, wandering larvae from short-day exposed flies, therefore initially programmed for diapause, but diverted from the diapause pathway by larval breeding at 19 degrees C, were significantly more cold tolerant than nondiapause larvae from long-day parents, indicating some maternal regulation of larval cold tolerance. There was, however, no evidence for an additional cold hardiness in larvae acclimatised to cold by a gradual reduction of temperature.