Temperature acclimation alters cardiac performance in the lobster Homarus americanus

The American lobster is a poikilotherm that inhabits a marine environment where temperature varies over a 25°C range and depends on the winds, the tides and the seasons. To determine how cardiac performance depends on the water temperature to which the lobsters are acclimated we measured lobster heart rates in vivo. The upper limit for cardiac function in lobsters acclimated to 20°C is approximately 29°C, 5°C warmer than that measured in lobsters acclimated to 4°C. Warm acclimation also slows the lobster heart rate within the temperature range from 4 to 12°C. Both effects are apparent after relatively short periods of warm acclimation (3–14 days). However, warm acclimation impairs cardiac function at cold temperatures: following several hours exposure to frigid (<5°C) temperatures heart rates become slow and arrhythmic in warm acclimated, but not cold acclimated, lobsters. Thus, acclimation temperature determines the thermal limits for cardiac function at both extremes of the 25°C temperature range lobsters inhabit in the wild. These observations suggest that regulation of cardiac thermal tolerance by the prevailing environmental temperature protects against the possibility of cardiac failure due to thermal stress.     

Effects of temperature acclimation on cardiorespiratory performance of the Antarctic notothenioid Trematomus bernacchii

Notothenioid fishes of the Southern Ocean have evolved under cold and stable temperatures for millions of years. Due to rising temperatures in the Southern Ocean, investigating thermal limits and the capacities for inducing a temperature acclimation response in notothenioids has become of increasing interest. Here, we investigated effects of temperature acclimation on cardiorespiratory responses and cardiac and skeletal muscle energy metabolism in a benthic Antarctic notothenioid, Trematomus bernacchii. We acclimated specimens to ?1, 2 and 4.5 °C for 14 days and quantified heart rates and ventilation rates during an acute increase in temperature. Ventilation rates showed an effect of acclimation both at initial steady-state acclimation conditions and during an acute temperature increase, suggesting a partial thermal compensatory response. However, acclimation did not affect heart rates at steady-state acclimation conditions and the temperatures at which onset of cardiac arrhythmia occurred, suggesting lack of inducible thermal tolerance in cardiac performance. Citrate synthase (CS), lactate dehydrogenase (LDH) and 3-hydroxyacyl dehydrogenase activities in skeletal muscle tissues suggested acclimation-induced shifts in metabolic fuel preferences, and a marked increase in LDH activity with acclimation to 4.5 °C showed an increase in anaerobic metabolism. In heart tissue, CS and LDH activities decreased with acclimation to 4.5 °C, suggesting reduced cardiac ATP production. Overall, the data suggest a partial acclimatory response to temperature by T. bernacchii and support the hypothesis that reduced cardiac acclimatory capacity may play a role in limiting the thermal plasticity of T. bernacchii.     

Acclimation responses to short‐term temperature treatments during early life stages causes long lasting changes in spontaneous activity of adult Drosophila melanogaster

Ecotherms adjust their physiology to environmental temperatures. Long‐term exposures to heat or cold typically induce acclimation responses that generate directional, but reversible shifts in thermal tolerance and performance. However, less is known about how short exposure in different life stages will affect the adult phenotype. In the present study, we compared the effects of long‐term temperature exposure to 15, 19 and 31 °C with that of brief (16 h) exposure periods at the same temperatures in Drosophila melanogaster eggs, larvae, pupae, or adults, respectively. The acclimation responses are evaluated using activity measurements at 11, 15, 19, 27, 31 and 33 °C and by measuring upper and lower thermal limits (CT_max and CT_min) in 5‐day‐old adult males. As expected, long‐term cold exposure reduces relative CT_min, whereas long‐term heat exposure increases relative CT_max. By contrast, we find little effect on thermal limits when using short‐term exposures at different life stages. Long‐term exposures to 31 and 15 °C both suppressed activity relative to the 19 °C control, suggesting that development at high and low temperatures may lead to reduced activity later in life. Short‐term cold exposure early in development reduces activity in the adult stage, whereas the effects of short‐term heat exposure on behaviour are dependent on life stage and test temperature. Together, our results highlight how the thermal sensitivity of the trait measured determines the ability to detect acclimation responses.     

Can Antarctic lichens acclimatize to changes in temperature?

The Antarctic Peninsula, a tundra biome dominated by lichens and bryophytes, is an ecozone undergoing rapid temperature shifts. Such changes may demand a high physiological plasticity of the local lichen species to maintain their role as key drivers in this pristine habitat. This study examines the response of net photosynthesis and respiration to increasing temperatures for three Antarctic lichen species with different ecological response amplitudes. We hypothesize that negative effects caused by increased temperatures can be mitigated by thermal acclimation of respiration and/or photosynthesis. The fully controlled growth chamber experiment simulated intermediate and extreme temperature increases over the time course of 6 weeks. Results showed that, in contrast to our hypothesis, none of the species was able to down‐regulate temperature‐driven respiratory losses through thermal acclimation of respiration. Instead, severe effects on photobiont vitality demonstrated that temperatures around 15°C mark the upper limit for the two species restricted to the Antarctic, and when mycobiont demands exceeded the photobiont capacity they could not survive within the lichen thallus. In contrast, the widespread lichen species was able to recover its homoeostasis by rapidly increasing net photosynthesis. We conclude that to understand the complete lichen response, acclimation processes of both symbionts, the photo‐ and the mycobiont, have to be evaluated separately. As a result, we postulate that any acclimation processes in lichen are species‐specific. This, together with the high degree of response variability and sensitivity to temperature in different species that co‐occur spatially close, complicates any predictions regarding future community composition in the Antarctic. Nevertheless, our results suggest that species with a broad ecological amplitude may be favoured with on‐going changes in temperature.     

Cold hardiness of diapausing and non-diapausing pupae of the European grapevine moth, Lobesia botrana

Lobesia botrana (Denis & Schiffermüller) (Lepidoptera: Tortricidae) is a key pest of grapes in Europe. It overwinters as a pupa in the bark crevices of the plant. Supercooling point (SCP) and low temperature survival was investigated in the laboratory and was determined using a cool bath and a 1 °C min^?1 cooling rate. Freezing was fatal both to diapausing and non‐diapausing pupae. SCP was significantly lower in diapausing male (?24.8 °C) and female (?24.5 °C) pupae than in non‐diapausing ones (?22.7 and ?22.5 °C, respectively). Sex had no influence on SCP both for diapausing and non‐diapausing pupae. Supercooling was also not affected by acclimation. However, acclimation did improve survival of diapausing pupae at temperatures above the SCP. Survival increased as acclimation period increased and the influence was more profound at the lower temperatures examined. Diapausing pupae could withstand lower temperatures than non‐diapausing ones and lethal temperature was significantly lower than for non‐diapausing pupae. Freezing injury above the SCP has been well documented for both physiological stages of L. botrana pupae. Our findings suggest a diapause‐related cold hardiness for L. botrana and given its cold hardiness ability, winter mortality due to low temperatures is not expected to occur, especially in southern Europe.     

Effect of thermal acclimation on preferred temperatures in two mygalomorph spiders inhabiting contrasting habitats

Variations in the preferred temperatures during the rest periods of Grammostola rosea Walckenaer and Paraphysa parvula Pocock, two mygalomorph spiders occupying different habitats in central Chile, are analyzed. The former inhabits arid and semi‐arid lowland near plant communities, composed of shrubs (evergreens with small leathery leaves) and small trees; the latter is found in the central mountains of the Chilean Andes, above 2000 m.a.s.l. The preferred temperatures of these spiders at different times of day and exposure to cold (15 °C) and warm (25 °C) acclimation temperatures are compared. Body mass does not affect the preferred temperature of the larger spider G. rosea, although P. parvula, a spider with half of the body mass of G. rosea, shows a decrease in preferred temperature with body mass. This can be explained by a higher plasticity and thermal sensitivity of the smaller species as result of increased surface : volume ratio. The preferred temperature increases with the hour of the day under both acclimation conditions in P. parvula and in cold‐acclimated G. rosea, which is likely associated with crepuscular and nocturnal behaviour in both species. Grammostola rosea shows temperature preferences lower than those of P. parvula under both acclimation conditions. The increase of the acclimation temperature from 15 to 25 °C results in an increment of 2–3 °C in the preferred temperature of P. parvula but only 0.2 °C in that of G. rosea. Two contrasting lifestyle strategies are found: a small mygalomorph spider with phenotypic plasticity and adaptation to the fluctuating environment of high altitude, and a large mygalomorph spider with higher thermal inertia adapted to the more stable environment of lowlands.     

Evolution of total net fitness in thermal lines: Drosophila subobscura likes it 'warm'

Fisher's fundamental theorem states that heritable variation for net fitness sets a limit to the rate of response to natural selection. How will temperate (i.e. cold‐tolerant) species cope with contemporary rapid global warming? Using three‐fold replicated lines of Drosophila subobscura that had been allowed to evolve for 4 years (between 32 and 59 generations) at 13 °C (cold), 18 °C (the supposed optimum temperature), and 22 °C (warm) I assess here how net fitness changes according to thermal environments. Net fitness was estimated following the classical approach in population genetics of competing over a number of generation in outbred experimental populations multiple wild‐type O chromosomes (homologous to arm 3R in D. melanogaster) independently derived from each base thermal stock in an otherwise homogeneous genetic background against a balancer chromosome. Warm‐adapted populations (‘warm‐adapted O chromosomes’) performed comparatively well at all tested temperatures. However, net fitness was severely reduced in cold‐adapted populations when transferred to warmer conditions. It seems, therefore, that thermal fitness breath for D. subobscura flies is positively associated to temperature. These findings are discussed in relation to the fast world‐wide clinal shifts in the frequency of genetic markers correlated with current climate change.     

Increased acute thermal tolerance and little change to hematology following acclimation to warm water in juvenile Striped Bass,Morone saxatilis

Striped Bass naturally inhabit a wide range of temperatures, yet little is known about the processes that control their acute and chronic temperature limits. The objective of this study was to determine the effect of temperature acclimation on acute thermal maxima and physiology of juvenile Striped Bass. Juvenile fish were acclimated to 15, 25 or 30 °C for 4 weeks, then split into two sampling groups: post-acclimation and post-critical thermal maximum trials. We found that fish survived in all acclimation temperatures with little change to underlying hematology, and that critical thermal maximum (CT_max) increased with increasing acclimation temperature. At CT_max, fish acclimated to 30 °C had elevated plasma cortisol, lactate and potassium levels. These results suggest that, while 30 °C is likely to be outside their thermal optima, Striped Bass can survive at high temperatures. This ability to cope with warm temperatures may provide an advantage with increasing global temperatures.

     

Acclimation responses to temperature vary with vertical stratification: implications for vulnerability of soil‐dwelling species to extreme temperature events

The occurrence of summer heat waves is predicted to increase in amplitude and frequency in the near future, but the consequences of such extreme events are largely unknown, especially for belowground organisms. Soil organisms usually exhibit strong vertical stratification, resulting in more frequent exposure to extreme temperatures for surface‐dwelling species than for soil‐dwelling species. Therefore soil‐dwelling species are expected to have poor acclimation responses to cope with temperature changes. We used five species of surface‐dwelling and four species of soil‐dwelling Collembola that habituate different depths in the soil. We tested for differences in tolerance to extreme temperatures after acclimation to warm and cold conditions. We also tested for differences in acclimation of the underlying physiology by looking at changes in membrane lipid composition. Chill coma recovery time, heat knockdown time and fatty acid profiles were determined after 1 week of acclimation to either 5 or 20 °C. Our results showed that surface‐dwelling Collembola better maintained increased heat tolerance across acclimation temperatures, but no such response was found for cold tolerance. Concordantly, four of the five surface‐dwelling Collembola showed up to fourfold changes in relative abundance of fatty acids after 1 week of acclimation, whereas none of the soil‐dwelling species showed a significant adjustment in fatty acid composition. Strong physiological responses to temperature fluctuations may have become redundant in soil‐dwelling species due to the relative thermal stability of their subterranean habitat. Based on the results of the four species studied, we expect that unless soil‐dwelling species can temporarily retreat to avoid extreme temperatures, the predicted increase in heat waves under climatic change renders these soil‐dwelling species more vulnerable to extinction than species with better physiological capabilities. Being able to act under a larger thermal range is probably costly and could reduce maximum performance at the optimal temperature.     

Rapid changes in the phospholipid composition of gill membranes during thermal acclimation of the rainbow trout,Salmo gairdneri

Summary The phospholipid composition of gill tissue was determined in rainbow trout (Salmo gairdneri) undergoing thermal acclimation between 5°C and 20°C for a period of up to 28 days. Proportions of phosphatidylethanolamine (PE) and cardiolipin (CL) increased during cold acclimation and decreased during warm acclimation; proportions of phosphatidylcholine (PC) changed in the opposite direction (i.e., decreased during cold acclimation). In contrast, levels of phosphatidylserine,-inositol, and sphingomyelin did not vary significantly. Thermal modulation of headgroup composition occurred rapidly as reflected by changes in the ratio of PC-to-PE, which rose significantly from 2.40±0.09 to 2.92±0.09 within 72 h of transfer from 5 to 20°C; adaptation to 5°C was equally rapid. Proportions of PE changed more rapidly than those of PC during cold adaptation, whereas the opposite was true during warm acclimation. Both the time course and the direction of the observed changes in phospholipid composition suggest that such adjustments may contribute to the homeoviscous regulation of membrane properties, particularly during the initial stages of thermal adaptation.     

Divergence of gastropod life history in contrasting thermal environments in a geothermal lake

Experiments using natural populations have provided mixed support for thermal adaptation models, probably because the conditions are often confounded with additional environmental factors like seasonality. The contrasting geothermal environments within Lake Mývatn, northern Iceland, provide a unique opportunity to evaluate thermal adaptation models using closely located natural populations. We conducted laboratory common garden and field reciprocal transplant experiments to investigate how thermal origin influences the life history of Radix balthica snails originating from stable cold (6 °C), stable warm (23 °C) thermal environments or from areas with seasonal temperature variation. Supporting thermal optimality models, warm‐origin snails survived poorly at 6 °C in the common garden experiment and better than cold‐origin and seasonal‐origin snails in the warm habitat in the reciprocal transplant experiment. Contrary to thermal adaptation models, growth rate in both experiments was highest in the warm populations irrespective of temperature, indicating cogradient variation. The optimal temperatures for growth and reproduction were similar irrespective of origin, but cold‐origin snails always had the lowest performance, and seasonal‐origin snails often performed at an intermediate level compared to snails originating in either stable environment. Our results indicate that central life‐history traits can differ in their mode of evolution, with survival following the predictions of thermal optimality models, whereas ecological constraints have shaped the evolution of growth rates in local populations.     

The effects of temperature acclimation on organ/tissue mass and cytochrome c oxidase activity in juvenile cod (Gadus morhua)

Cod were acclimated to 5 and 15° C (cold and warm acclimation, respectively) for at least 43 days after which tissue-somatic indices, tissue protein, DNA content, and cytochrome c oxidase (CCO) activity were measured. Liver, stomach, intestine, total heart and ventricle-somatic indices were all increased significantly in the cold acclimated animals compared with their warm acclimated counterparts. There were no differences in gill or white muscle-somatic indices between the acclimation temperatures. Tissue protein concentration (mg protein g tissue⁻¹) was generally unaffected by temperature acclimation. Cold acclimation resulted in higher white muscle and lower ventricle CCO specific activities(μmol cytochrome c oxidized min⁻¹· g tissue⁻¹) compared with the respective warm acclimated tissues. No significant differences in CCO specific activity were observed in the remaining tissues (when measured at an intermediate temperature of 10° C). Total tissue CCO activity (measured at an intermediate temperature of 10° C) did not differ significantly between the cold and warm acclimated fish.     

Low temperature tolerance,cold hardening and acclimation in tadpoles of the neotropical túngara frog (Engystomops pustulosus)

Many frogs from temperate climates can tolerate low temperatures and increase their thermal tolerance through hardening and acclimation. Most tropical frogs, on the other hand, fail to acclimate to low temperatures. This lack of acclimation ability is potentially due to lack of selection pressure for acclimation because cold weather is less common in the tropics. We tested the generality of this pattern by characterizing the critical temperature minimum (CTMin), hardening, and acclimation responses of túngara frogs (Engystomops pustulosus). These frogs belong to a family with unknown thermal ecology. They are found in a tropical habitat with a highly constant temperature regime. The CTMin of the tadpoles was on average 12.5 °C. Pre-metamorphic tadpoles hardened by 1.18 °C, while metamorphic tadpoles hardened by 0.36 °C. When raised at 21 °C, tadpoles acclimated expanding their cold tolerance by 1.3 °C in relation to larvae raised at 28 °C. These results indicate that the túngara frog has a greatly reduced cold tolerance when compared to species from temperate climates, but it responds to cold temperatures with hardening and acclimation comparable to those of temperate-zone species. Cold tolerance increased with body length but cold hardening was more extensive in pre-metamorphic tadpoles than in metamorphic ones. This study shows that lack of acclimation ability is not general to the physiology of tropical anurans.     

Effects of acclimation and latitude on the activity thresholds of the aphid Myzus persicae in Europe

Activity thresholds were measured in nine anholocyclic clones of the peach‐potato aphid Myzus persicae collected along a latitudinal cline of its European distribution from Sweden to Spain. The effects of collection origin and intra‐ and intergenerational acclimation on these thresholds were investigated. Low‐temperature (10°C) acclimation for one generation depressed the movement threshold and chill coma temperatures, with the largest reduction in movement threshold recorded for clone UK 1 (8.8–2.5°C) and in chill coma for UK 2 (4.8–2.0°C). High‐temperature (25°C) acclimation for one generation increased the heat movement threshold and heat coma temperature with the largest increase in the movement threshold (40.1–41.1°C) and heat coma (41.4–42.3°C) recorded for clone Swed 1. There was no further intergenerational acclimation over three generations. High‐temperature activity thresholds were less plastic than low‐temperature thresholds, and, consequently, thermal activity ranges were expanded following low‐temperature acclimation. No constant affect of acclimation was observed on chill coma recovery, although clonal differences were observed with Swed 1 and 3 requiring some of the longest complete recovery times. There was no relationship between latitude and activity thresholds with the exception of heat coma data where Scandinavian clones Swed 2 and 3 consistently displayed some of the lowest heat coma temperatures (e.g. 41.3°C for both clones at 20°C) and Mediterranean clones Span 1, 2 and 3 displayed some of the highest (e.g. 42.1, 41.9 and 42.5°C, respectively, at 20°C). These data suggest that clonal mixing could occur over a large scale across Europe, limiting local adaptation to areas where conditions enable long‐term persistence of populations, e.g. adaptation to higher temperatures in the Mediterranean region. It is suggested that aphid thermal tolerance could be governed more by clonal type than the latitudinal origin.     

Winter cold tolerance and the geographic range separation of Bromus tectorum and Bromus rubens,two severe invasive species in North America

The invasive grasses Bromus rubens and Bromus tectorum are responsible for widespread damage to semiarid biomes of western North America. Bromus. tectorum dominates higher and more northern landscapes than its sister species B. rubens, which is a severe invader in the Mojave desert region of the American Southwest. To assess climate thresholds controlling their distinct geographic ranges, we evaluated the winter cold tolerance of B. tectorum and B. rubens. Freezing tolerance thresholds were determined using electrolyte leakage and whole‐plant mortality. The responses of the two species to winter cold and artificial freezing treatments were similar in 2007–2008 and 2009–2010. When grown at minimum temperatures of 10 °C, plants of both species had cold tolerance thresholds near ?10 °C, while plants acclimated to a daily minimum of ?10 to ?30 °C survived temperatures down to ?31 °C. In the winter of 2010–2011, a sudden severe cold event on December 9, 2010 killed all B. rubens populations, while B. tectorum was not harmed; all tested plants were 7–8 weeks old. Controlled acclimation experiments demonstrated that 8‐week‐old plants of B. rubens had a slower acclimation rate to subzero temperatures than B. tectorum and could not survive a rapid temperature drop from 1 to ?14 °C. Four‐month‐old B. rubens populations were as cold tolerant as B. tectorum. Our results show that severe and sudden freeze events in late autumn can kill young plants of B. rubens but not B. tectorum. Such events could exclude B. rubens from the relatively cold, Intermountain steppe biome of western North America where B. tectorum predominates.     

Temporal heterogeneity of cold acclimation phenotypes in Arabidopsis leaves

To predict the effects of temperature changes on plant growth and performance, it is crucial to understand the impact of thermal history on leaf morphology, anatomy and physiology. Here, we document a comprehensive range of leaf phenotypes in 25/20 °C‐grown Arabidopsis thaliana plants that were shifted to 5 °C for up to 2 months. When warm‐grown, pre‐existing (PE) leaves were exposed to cold, leaf thickness increased due to an increase in mesophyll cell size. Leaves that were entirely cold‐developed (CD) were twice as thick (eight cell layers) as their warm‐developed (WD) counterparts (six layers), and also had higher epidermal and stomatal cell densities. After 4 d of cold, PE leaves accumulated high levels of total non‐structural carbohydrates (TNC). However, glucose and starch levels declined thereafter, and after 45 d in the cold, PE leaves exhibited similar TNC to CD leaves. A similar phenomenon was observed in δ¹³C and a range of photosynthetic parameters. In cold‐treated PE leaves, an increase in respiration (R_dark) with cold exposure time was evident when measured at 25 °C but not 5 °C. Cold acclimation was associated with a large increase in the ratio of leaf R_dark to photosynthesis. The data highlight the importance of understanding developmental thermal history in determining individual phenotypic traits.