Thermal limits of survival and reproduction depend on stress duration: A case study of Drosophila suzukii.

Studies of ectotherm responses to heat extremes often rely on assessing absolute critical limits for heat coma or death (CT), however, such single parameter metrics ignore the importance of stress exposure duration. Furthermore, population persistence may be affected at temperatures considerably below CT through decreased reproductive output. Here we investigate the relationship between tolerance duration and severity of heat stress across three ecologically relevant life-history traits (productivity, coma and mortality) using the global agricultural pest Drosophila suzukii.

Cold comfort: metabolic rate and tolerance to low temperatures predict latitudinal distribution in ants.

Metabolic compensation has been proposed as a mean for ectotherms to cope with colder climates. For example, under the metabolic cold adaptation and the metabolic homeostasis hypotheses (MCA and MHH), it has been formulated that cold-adapted ectotherms should display both higher (MCA) and more thermally sensitive (MHH) metabolic rates (MRs) at lower temperatures. However, whether such compensation can truly be associated with distribution, and whether it interplays with cold tolerance to predict species' climatic niches, remains largely unclear despite broad ecological implications thereof.

Locust gut epithelia do not become more permeable to fluorescent dextran and bacteria in the cold.

The insect gut, which plays a role in ion and water balance, has been shown to leak solutes in the cold. Cold stress can also activate insect immune systems, but it is unknown whether the leak of the gut microbiome is a possible immune trigger in the cold. We developed a novel feeding protocol to load the gut of locusts (Locusta migratoria) with fluorescent bacteria before exposing them to -2°C for up to 48 h.

Chilled, starved or frozen: insect mitochondrial adaptations to overcome the cold.

Physiological adaptations to tackle cold exposure are crucial for insects living in temperate and arctic environments and here we review how cold adaptation is manifested in terms of mitochondrial function. Cold challenges are diverse, and different insect species have evolved metabolic and mitochondrial adaptations to i) energize homeostatic regulation at low temperatures ii) stretch energy reserves during prolonged cold exposure, and iii) preserve the structural organization of organelles following extracellular freezing. While the literature is still sparse, our review suggests that cold-adapted insects preserve ATP production at low temperatures by maintaining preferred mitochondrial substrate oxidation, which is otherwise challenged in cold-sensitive species.

Interspecific differences in thermal tolerance landscape explain aphid community abundance under climate change.

A single critical thermal limit is often used to explain and infer the impact of climate change on geographic range and population abundance. However, it has limited application in describing the temporal dynamic and cumulative impacts of extreme temperatures. Here, we used a thermal tolerance landscape approach to address the impacts of extreme thermal events on the survival of co-existing aphid species (Metopolophium dirhodum, Sitobion avenae and Rhopalosiphum padi).

Balanced mitochondrial function at low temperature is linked to cold adaptation in Drosophila species.

The ability of ectothermic animals to live in different thermal environments is closely associated with their capacity to maintain physiological homeostasis across diurnal and seasonal temperature fluctuations. For chill-susceptible insects, such as Drosophila, cold tolerance is tightly linked to ion and water homeostasis obtained through a regulated balance of active and passive transport. Active transport at low temperature requires a constant delivery of ATP and we therefore hypothesize that cold-adapted Drosophila are characterized by superior mitochondrial capacity at low temperature relative to cold-sensitive species.

Extreme escalation of heat failure rates in ectotherms with global warming.

Temperature affects the rate of all biochemical processes in ectotherms and is therefore critical for determining their current and future distribution under global climate change. Here we show that the rate of biological processes maintaining growth, homeostasis and ageing in the permissive temperature range increases by 7% per degree Celsius (median activation energy E = 0.48 eV from 1,351 rates across 314 species).

Phylogenetic and environmental patterns of sex differentiation in physiological traits across Drosophila species.

Sex-based differences in physiological traits may be influenced by both evolutionary and environmental factors. Here we used male and female flies from >80 Drosophila species reared under common conditions to examine variance in a number of physiological traits including size, starvation, desiccation and thermal tolerance. Sex-based differences for desiccation and starvation resistance were comparable in magnitude to those for size, with females tending to be relatively more resistant than males.

Finding the right thermal limit: a framework to reconcile ecological, physiological and methodological aspects of CTmax in ectotherms.

Upper thermal limits (CTmax) are frequently used to parameterize the fundamental niche of ectothermic animals and to infer biogeographical distribution limits under current and future climate scenarios. However, there is considerable debate associated with the methodological, ecological and physiological definitions of CTmax. The recent (re)introduction of the thermal death time (TDT) model has reconciled some of these issues and now offers a solid mathematical foundation to model CTmax by considering both intensity and duration of thermal stress.

Acclimation, duration and intensity of cold exposure determine the rate of cold stress accumulation and mortality in Drosophila suzukii.

The spotted wing drosophila (SWD), Drosophila suzukii, is a major invasive fruit pest. There is strong consensus that low temperature is among the main drivers of SWD population distribution, and the invasion success of SWD is also linked to its thermal plasticity. Most studies on ectotherm cold tolerance focus on exposure to a single stressful temperature but here we investigated how cold stress intensity affected survival duration across a broad range of low temperatures (-7 to +3 °C).

A unifying model to estimate thermal tolerance limits in ectotherms across static, dynamic and fluctuating exposures to thermal stress.

Temperature tolerance is critical for defining the fundamental niche of ectotherms and researchers classically use either static (exposure to a constant temperature) or dynamic (ramping temperature) assays to assess tolerance. The use of different methods complicates comparison between studies and here we present a mathematical model (and R-scripts) to reconcile thermal tolerance measures obtained from static and dynamic assays. Our model uses input data from several static or dynamic experiments and is based on the well-supported assumption that thermal injury accumulation rate increases exponentially with temperature (known as a thermal death time curve).

Osmoregulatory capacity at low temperature is critical for insect cold tolerance.

At low temperature many insects lose extracellular ion homeostasis and the capacity to mitigate homeostatic imbalance determines their cold tolerance. Extracellular homeostasis is ensured by the osmoregulatory organs and recent research has emphasized key roles for the Malpighian tubules and hindgut in modulating insect cold tolerance. Here, we review the effects of low temperature on transport capacity of osmoregulatory organs and outline physiological processes leading from cold exposure to disruption of ion homeostasis and cold-injury in insects.

Dramatic changes in mitochondrial substrate use at critically high temperatures: a comparative study using .

Ectotherm thermal tolerance is critical to species distribution, but at present the physiological underpinnings of heat tolerance remain poorly understood. Mitochondrial function is perturbed at critically high temperatures in some ectotherms, including insects, suggesting that heat tolerance of these animals is linked to failure of oxidative phosphorylation (OXPHOS) and/or ATP production. To test this hypothesis, we measured mitochondrial oxygen consumption rate in six species with different heat tolerance using high-resolution respirometry.

Cold acclimation preserves hindgut reabsorption capacity at low temperature in a chill-susceptible insect, Locusta migratoria.

Cold acclimation increases cold tolerance of chill-susceptible insects and the acclimation response often involves improved organismal ion balance and osmoregulatory function at low temperature. However, the physiological mechanisms underlying plasticity of ion regulatory capacity are largely unresolved. Here we used Ussing chambers to explore the effects of cold exposure on hindgut KCl reabsorption in cold- (11 °C) and warm-acclimated (30 °C) Locusta migratoria.

Cold acclimation increases depolarization resistance and tolerance in muscle fibers from a chill-susceptible insect, .

Cold exposure depolarizes cells in insects due to a reduced electrogenic ion transport and a gradual increase in extracellular K concentration ([K]). Cold-induced depolarization is linked to cold injury in chill-susceptible insects, and the locust, , has been shown to improve cold tolerance following cold acclimation through depolarization resistance. Here we investigate how cold acclimation influences depolarization resistance and how this resistance relates to improved cold tolerance.

Comparison of Static and Dynamic Assays When Quantifying Thermal Plasticity of Drosophilids.

Numerous assays are used to quantify thermal tolerance of arthropods including dynamic ramping and static knockdown assays. The dynamic assay measures a critical temperature while the animal is gradually heated, whereas the static assay measures the time to knockdown at a constant temperature. Previous studies indicate that heat tolerance measured by both assays can be reconciled using the time × temperature interaction from "thermal tolerance landscapes" (TTLs) in unhardened animals.

Neural dysfunction correlates with heat coma and CT in but does not set the boundaries for heat stress survival.

When heated, insects lose coordinated movement followed by the onset of heat coma (critical thermal maximum, CT). These traits are popular measures to quantify interspecific and intraspecific differences in insect heat tolerance, and CT correlates well with current species distributions of insects, including Here, we examined the function of the central nervous system (CNS) in five species of with different heat tolerances, while they were exposed to either constant high temperature or a gradually increasing temperature (ramp). Tolerant species were able to preserve CNS function at higher temperatures and for longer durations than sensitive species, and similar differences were found for the behavioural indices (loss of coordination and onset of heat coma).

Maintenance of hindgut reabsorption during cold exposure is a key adaptation for cold tolerance.

Maintaining extracellular osmotic and ionic homeostasis is crucial for organismal function. In insects, hemolymph volume and ion content is regulated by the secretory Malpighian tubules and reabsorptive hindgut. When exposed to stressful cold, homeostasis is gradually disrupted, characterized by a debilitating increase in extracellular K concentration (hyperkalemia).

Temperature preference across life stages and acclimation temperatures investigated in four species of Drosophila.

Ectotherms can use microclimatic variation and behavioral thermoregulation to cope with unfavorable environmental temperatures. However, relatively little is known about how and if thermoregulatory behavior is used across life stages in small ectothermic insects. Here we investigate differences between three specialized Drosophila species from temperate, tropical or desert habitats and one cosmopolitan species by estimating the preferred temperature (T) and the breadth (T) of the distribution of adults, adult egg-laying, and larvae in thermal gradients.

Evolution and plasticity of thermal performance: an analysis of variation in thermal tolerance and fitness in 22 Drosophila species.

The thermal biology of ectotherms is often used to infer species' responses to changes in temperature. It is often proposed that temperate species are more cold-tolerant, less heat-tolerant, more plastic, have broader thermal performance curves (TPCs) and lower optimal temperatures when compared to tropical species. However, relatively little empirical work has provided support for this using large interspecific studies.

The central nervous system and muscular system play different roles for chill coma onset and recovery in insects.

When insects are cooled, they initially lose their ability to perform coordinated movements at their critical thermal minima (CT). At a slightly lower temperature, they enter a state of complete paralysis (chill coma onset temperature - CCO) and if they are returned to permissive temperatures they regain function after a recovery period which is termed chill coma recovery time (CCRT). These three phenotypes (CT, CCO, and CCRT) are all popular measures of insect cold tolerance and it is therefore important to characterize the physiological processes that are responsible for these phenotypes.

Cold acclimation modulates voltage gated Ca channel currents and fiber excitability in skeletal muscles of Locusta migratoria.

Cold exposure is known to induce stressful imbalances in chill susceptible insects, including loss of hemolymph water, hyperkalemia and cell depolarization. Cold induced depolarization induces uncontrolled Ca influx and accumulation of injury through necrosis/apoptosis. Conversely cold induced Ca influx has been shown to induce rapid cold hardening and therefore also play a role to reduce cold injury.

Effects of anoxia on ATP, water, ion and pH balance in an insect ().

When exposed to anoxia, insects rapidly go into a hypometabolic coma from which they can recover when exposed to normoxia again. However, prolonged anoxic bouts eventually lead to death in most insects, although some species are surprisingly tolerant. Anoxia challenges ATP, ion, pH and water homeostasis, but it is not clear how fast and to what degree each of these parameters is disrupted during anoxia, nor how quickly they recover.

Fluctuating thermal regime preserves physiological homeostasis and reproductive capacity in Drosophila suzukii.

Drosophila suzukii, an invasive species recently introduced in Europe, lays eggs in thin-skinned fruits and causes huge financial losses to fruit growers. One potential way to control this pest is the sterile insect technique (SIT) which demands a large stock of reproductive females to produce millions of sterile males to be released on demand. Unfortunately, Drosophila stocks age quickly, show declining fecundity when maintained at warm temperatures and conversely, they die from chill injury if they are maintained at constant low temperature.