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Evolutionary and acclimation-induced variation in the thermal limits of heart function in congeneric marine snails (genus Tegula): implications for vertical zonation.

We analyzed the thermal limits of heart function for congeneric species of the marine snail Tegula that have different patterns of vertical zonation. T. funebralis is found in the low to mid-intertidal zone, and T. brunnea and T. montereyi live in the low-intertidal or subtidally. As indices of thermal limits of heart function, we used the temperature at which heart rate initially decreased rapidly during heating (the Arrhenius break temperature, or ABT) and the temperature at which heart ceased to beat with either heating or cooling (the flatline temperature, or FLT(hot) or FLT(cold), respectively). These three indices provide an estimate of the thermal range within which Tegula heart function is maintained. For field-acclimatized specimens, the thermal range of the high-intertidal T. funebralis was greater than those of its two lower-occurring congeners (higher ABT, higher FLT(hot), lower FLT(cold)). We also demonstrated the effects of constant thermal acclimation on the heart rate response to heat stress. Acclimation to 14 degrees C and 22 degrees C resulted in increases in ABT and FLT(hot), with the largest changes in T. brunnea and T. montereyi. Although T. funebralis is more heat tolerant and eurythermal than its two lower-occurring congeners, it can encounter field body temperatures that exceed ABT, indicating that T. funebralis faces a larger threat from heat stress, in situ. These findings are consistent with recent studies on other taxa of marine invertebrates that have shown, somewhat paradoxically, that warm-adapted, eurythermal intertidal species may be more impacted by global warming than congeneric subtidal species that are less heat tolerant.

Acclimatization↗

Thermogenic side effects to migratory predisposition in shorebirds.

In the calidrine sandpiper red knot (Calidris canutus), the weeks preceding takeoff for long-distance migration are characterized by a rapid increase in body mass, largely made up of fat but also including a significant proportion of lean tissue. Before takeoff, the pectoral muscles are known to hypertrophy in preparation for endurance flight without any specific training. Because birds facing cold environments counterbalance heat loss through shivering thermogenesis, and since pectoral muscles represent a large proportion of avian body mass, we asked the question whether muscle hypertrophy in preparation for long-distance endurance flight would induce improvements in thermogenic capacity. We acclimated red knots to different controlled thermal environments: 26 degrees C, 5 degrees C, and variable conditions tracking outdoor temperatures. We then studied within-individual variations in body mass, pectoral muscle size (measured by ultrasound), and metabolic parameters [basal metabolic rate (BMR) and summit metabolic rate (M(sum))] throughout a 3-mo period enclosing the migratory gain and loss of mass. The gain in body mass during the fattening period was associated with increases in pectoral muscle thickness and thermogenic capacity independent of thermal acclimation. Regardless of their thermal treatment, birds showing the largest increases in body mass also exhibited the largest increases in M(sum). We conclude that migratory fattening is accompanied by thermoregulatory side effects. The gain of body mass and muscle hypertrophy improve thermogenic capacity independent of thermal acclimation in this species. Whether this represents an ecological advantage depends on the ambient temperature at the time of fattening.

Acclimatization↗

The effects of acclimation on thermal tolerance, desiccation resistance and metabolic rate in Chirodica chalcoptera (Coleoptera: Chrysomelidae).

Despite much focus on species responses to environmental variation through space and time, many higher taxa and geographic areas remain poorly studied. We report the effects of temperature acclimation on thermal tolerance, desiccation rate and metabolic rate for adult Chirodica chalcoptera (Coleoptera: Chrysomelidae) collected from Protea nerifolia inflorescences in the Fynbos Biome in South Africa. After 7 days of acclimation at 12, 19 and 25 degrees C, critical thermal maxima (mean+/-s.e.: 41.8+/-0.2 degrees C in field-fresh beetles) showed less response (<1 degrees C change) to temperature acclimation than did the onset of the critical thermal minima (0.1+/-0.2, 1.0+/-0.2 and 2.3+/-0.2 degrees C, respectively). Freezing was lethal in C. chalcoptera (field-fresh SCP -14.6 degrees C) and these beetles also showed pre-freeze mortality. Survival of 2 h at -10.1 degrees C increased from 20% to 76% after a 2 h pre-exposure to -2 degrees C, indicating rapid cold hardening. Metabolic rate, measured at 25 degrees C and adjusted by ANCOVA for mass variation, did not differ between males and females (2.772+/-0.471 and 2.517+/-0.560 ml CO2 h(-1), respectively), but was higher in 25 degrees C-acclimated beetles relative to the field-fresh and 12 degrees C-acclimated beetles. Body water content and desiccation rate did not differ between males and females and did not respond significantly to acclimation. We place these data in the context of measured inflorescence and ambient temperatures, and predict that climate change for the region could have effects on this species, in turn possibly affecting local ecosystem functioning.

Acclimatization↗

Temperature acclimation: effects on membrane physiology of an identified snail neuron.

The neuronal basis for thermal acclimation was examined by comparing the short- and long-term effects of temperature change on the physiological properties of an identified neuron in the isolated ganglion of Hexis aspersa. Using intracellular electrophysiological techniques, we found that the frequency of spontaneous action potentials and excitability of neurons from warm-acclimated animals was depressed by abruptly cooling from 20 to 5 degrees C. After a 2-wk period of acclimation to 5 degrees C, the levels of spontaneous activity and excitability were comparable to those of warm-acclimated neurons at 20 degrees C. Conversely, abrupt warming of neurons from cold-acclimated animals greatly increased the frequency of spontaneous activity, but after acclimation to 20 degrees C the frequency decreased. Although the duration of the action potential and the cell's electrogenic Na-K pump were temperature sensitive, thermal acclimation had no obvious effects on these parameters. Membrane permeability to Na and PNa/PK decreased with cooling, whereas PRb/PK and PCs/PK increased. Warming had the opposite effect on the relative alkali cation permeability (PX/PK). With acclimation PX/PK underwent compensatory changes.

Action Potentials↗

Temperature-related changes in the erythrocytic carbonic anhydrase (acetazolamide-sensitive esterase) activity of goldfish, Carassius auratus.

1. Carbonic anhydrase activity in 'membrane' and 'cytosol' fractions of goldfish erythrocytes was assayed by the p-nitrophenyl acetate procedure following thermal acclimation. 2. The thermal sensitivity of "membrane"-associated activity was apparently unaltered by acclimation. "Cytosol" activity in warm-acclimated specimens was somewhat more thermosensitive than that animals maintained at low temperature. 3. Significant increases in specific activity, and activity per unit volume of packed cells and blood were observed at higher temperatures when assays were conducted at the temperatures at which the system actually functions in the fish. By contrast, when determinations were carried out at a standard temperature (41 degrees C) corresponding to the upper incipient lethal for this species, activity was either unaffected, or declined as acclimation temperatures increased. 4. Changes in carbonic anhydrase activity following acclimation are consistent with the hypothesis that this system is implicated in the maintenance of stable plasma chloride levels, and the suggestion that alternations in red cell chloride levels with temperature are, in part at least, attributable to concomitant variations in enzyme activity.

Adaptation, Physiological↗

Cold acclimation increases carnitine palmitoyltransferase I activity in oxidative muscle of striped bass.

The effect of thermal acclimation on the activity of carnitine palmitoyltransferase I (CPT I), the rate-limiting enzyme for beta-oxidation of long-chain fatty acids, was determined in oxidative red muscle of striped bass (Morone saxatilis) acclimated at 5 or 25 degrees C. As observed in mammalian tissues, malonyl-CoA potently inhibited CPT I activity of mitochondria. Inhibition by malonyl-CoA required inclusions of both bovine serum albumin (BSA) and palmitoyl-CoA in the reaction media. Because BSA binds long-chain fatty acyl-CoAs, this observation suggests that free fatty acyl-CoAs may disrupt mitochondrial membranes and affect the CPT I protein. Cold acclimation increased citrate synthase activity 1.6-fold and total CPT activity 2-fold in homogenates of red muscle; free carnitine increased 62%, and specific activity of CPT I in mitochondria increased 2-fold. No differences were observed between cold- and warm-acclimated fish in substrate-binding properties of CPT I at an assay temperature of 15 degrees C, as judged by the Michaelis constant (Km) for carnitine (0.11 +/- 0.02 vs. 0.13 +/- 0.02 mM) or inhibition of CPT I, as determined by the half-maximal inhibition concentration (IC50) for malonyl-CoA (0.14 +/- 0.05 vs. 0.09 +/- 0.03 microM). Thermal sensitivity of CPT I (Q10 = 2.91 +/- 0.12 vs. 3.02 +/- 0.20) and preference of CPT I for different long-chain fatty acyl-CoA substrates (16:1-CoA = 16:0-CoA > 18:1-CoA) were not altered by thermal acclimation.(ABSTRACT TRUNCATED AT 250 WORDS)

Acclimatization↗

Investigation of a requirement for the PsbP-like protein in Synechocystis sp. PCC 6803.

The sll1418 gene encodes a PsbP-like protein in Synechocystis sp. PCC 6803. Expression of sll1418 was similar in BG-11 and in Cl- - or Ca2+ -limiting media, and inactivation of sll1418 did not prevent photoautotrophic growth in normal or nutrient-limiting conditions. Also the wild-type and DeltaPsbP strains exhibited similar oxygen evolution and assembly of Photosystem II (PS II) centers. Inactivation of sll1418 in the DeltaPsbO: DeltaPsbP, DeltaPsbQ:DeltaPsbP, DeltaPsbU:DeltaPsbP and DeltaPsbV:DeltaPsbP mutants did not prevent photoautotrophy or alter PS II assembly and oxygen evolution in these strains. Moreover, the absence of PsbP did not affect the ability of alkaline pH to restore photoautotrophic growth in the DeltaPsbO:DeltaPsbU strain. The PsbO, PsbU and PsbV proteins are required for thermostability of PS II and thermal acclimation in Synechocystis sp. PCC 6803 [Kimura et al. (2002) Plant Cell Physiol 43: 932-938]. However, thermostability and thermal acclimation in DeltaPsbP cells were similar to wild type. These results are consistent with the conclusion that PsbP is associated with approximately 3 of PS II centers, and may play a regulatory role in PS II [Thornton et al. (2004) Plant Cell 16: 2164-2175].

Amino Acid Sequence↗

Tolerance of photosynthesis to high temperature in desert plants.

Winter- and summertime-active desert annual species were grown at different temperatures to assess their capacity for photosynthetic acclimation. Thermal stability of photosynthesis was determined from responses of chlorophyll fluorescence to increased temperature. Photosynthesis in winter ephemerals grown at 28 degrees C/21 degrees C became unstable close to 41 degrees C in contrast to the summer annuals which were stable up to about 46 degrees C. Growth at higher temperature (43 degrees C/32 degrees C) resulted in increases in thermal stability of 5 to 7 degrees C for the winter annuals and 3 to 4 degrees C for the summer annuals, showing that temperature can provide the primary stimulus for acclimation of the photosynthetic apparatus. The magnitude of these changes was very similar to the range of field values observed for the respective floras, indicating that the thermal acclimation response under field conditions was qualitatively similar to that occurring under controlled growth conditions. Perennial species, co-existing with these annuals in the desert, were on average more thermostable. The cacti were exceptionally heat stable, the threshold for fluorescence increase averaging 55 degrees C.

Journal Article↗

Thermal behaviour of crustaceans.

Specific thermoreceptors or putative multimodal thermoreceptors are not known in Crustacea. However, behavioural studies on thermal avoidance and preference and on the effects of temperature on motor activity indicate that the thermosensitivity of crustaceans may be in the range 0.2-2 degrees C. Work on planktonic crustaceans suggests that they respond particularly to changes in temperature by klinokinesis and orthokinesis. The thermal behaviour of crustaceans is modified by thermal acclimation among other factors. The acclimation of the critical maximum temperature is an example of resistance acclimation, while the acclimation of preference behaviour may be classified as capacity acclimation of some other function. In crustaceans, the use of the concepts stenothermy and eurythermy at the species level is questionable, and it is not possible to divide crustacean species into thermal guilds as suggested for fishes. Thermal preference behaviour contributes to fitness in different ways in different species, often by maximising the aerobic metabolic scope for activity. In crustaceans the peripheral nervous system seems to have retained the capacity for thermosensitivity and thermal acclimation independently of the central nervous system control of behaviour.

Acclimatization↗

Temperature adaptation of biological membranes: differential homoeoviscous responses in brush-border and basolateral membranes of carp intestinal mucosa.

The effects of temperature acclimation of carp upon the hydrocarbon order of intestinal membranes has been determined. A fractionation technique has been developed for the simultaneous purification of brush-border and basolateral membrane fractions from the intestinal mucosa. The specific activity of alkaline phosphatase in the brush-border fraction was enhanced 6.4-fold over that of the initial homogenate, whilst the (Na(+)-K+)-stimulated ATPase was enhanced 5.8-fold in the basolateral fraction. The specific activities of NADPH-cytochrome-c reductase, succinate-cytochrome-c reductase and acid phosphatase were not increased in these two fractions. Membrane hydrocarbon order in membranes from 10 and 30 degrees C-acclimated carp has been compared by measuring the steady-state fluorescence polarization of 1,6-diphenyl-1,3,5-hexatriene over a range of temperatures. In the brush-border fraction, polarization was identical in both cold- and warm-acclimated groups, whilst large differences were observed in the basolateral fraction sufficient to offset approx. 75% of the temperature-induced ordering effects of cold. The fatty acid composition of the major phosphoglyceride fractions in the brush-border fraction was also largely unaffected by thermal acclimation, whilst the basolateral fraction showed significant increases in the proportion of unsaturated fatty acids in the cold. It is concluded that whilst the basolateral membrane of intestinal mucosa displays a large homoeoviscous response that correlates with a shift in lipid composition, the brush-border membrane does not. These findings are consistent with evidence of functional adaptations of the basolateral membrane during thermal acclimation (Gibson, J.S., Ellory, J.C. and Cossins, A.R. (1985) J. Exp. Biol. 114, 355-364).

Adaptation, Physiological↗

Effects of temperature, food deprivation and salinity on growth, RNA/DNA ratio and certain enzyme activities in rainbow trout (Salmo gairdneri Richardson).

1. The connection between feeding regime (food deprivation and restricted diet) and thermal acclimation (1-2, 6, 11 and 16 degrees C) was studied in rainbow trout held in diluted seawater (20% S). 2. At 1 degree C, food deprivation effects on all parameters are slight, and on RNA and certain enzymes they are masked by thermal acclimation effects. 3. At a salinity of 20% rainbow trout on a restricted diet and held at 11 degrees C have the highest growth rate. 4. Owing to increasing RNA levels, the RNA/DNA quotient is significantly higher than normal in rainbow trout held at 1 degree C although the fishes do not grow at this temperature. 5. Temperature and feeding both affect the enzymes we studied (liver: G1DH, AspT, arginase, G6PDH, and 6PGDH; kidney: G1DH, AspT, arginase, and Na/K-ATPase; white muscle: AspT and A1T; gill: Na/K-ATPase) differently. Interactions between these two factors also occur in some cases.

Alanine Transaminase↗

The effect of acclimation temperature on enzyme activity in Drosophila melanogaster.

1. The response to thermal acclimation of five key rate-limiting enzymes of intermediary metabolism and of six degradative enzymes was measured in tissue extracts of adult Drosophila melanogaster which had been acclimated for 4 days to 15, 25 or 30 degrees C. 2. Three enzymes of intermediary metabolism (HK, alpha-GPDH and CO) showed positive thermal compensation, which is the type of response characteristic of the enzymes involved in energy metabolism in vertebrate ectotherms. 3. The data obtained for CS and G6PDH showed no evidence for increased activity of TCA cycle nor of the pentose phosphate pathway upon cold acclimation in D. melanogaster. 4. Two degradative enzymes, ADH and non-specific esterase, showed inverse thermal compensation which is the type of response characteristic of degradative enzymes in vertebrate ectotherms. 5. In contrast to the situation in vertebrate ectotherms, catalase and the three lysosomal enzymes assayed (APH, acid DNase and acid RNase) displayed positive rather than inverse compensation. 6. The results presented here extend the data on the range of D. melanogaster enzymes which show compensation upon thermal acclimation and on the type of acclimation response which occurs.

Acclimatization↗

Characterization of gill Na/K-ATPase activity and ouabain binding in Antarctic and New Zealand nototheniid fishes.

The effects of thermal acclimation in two Nototheniid species, the stenothermal Antarctic Trematomous bernacchii and the eurythermal New Zealand Notothenia angustata, were investigated. Serum osmolality, gill Na/K-ATPase activity, sodium pump density and ouabain affinity were determined. Both fish were acclimated at their upper and lower viable thermal temperatures. Warm acclimation (+4 degrees C) of the T. bernacchii significantly decreased their serum osmolality from 550 to 450 mOsm/kg compared to cold-acclimation (-1.5 degrees C) and this was accompanied by a two-fold increase in gill Na/K-ATPase activity. Warm-acclimation (+14 degrees C) of N. angustata did not significantly change their serum osmolality from 330 mOsm/kg or gill Na/K-ATPase activity compared to the cold-acclimated (+4 degrees C) N. angustata. Using [(3)H]ouabain binding techniques, the B(max) and K(d) values of gill Na/K-ATPase enzymes were determined. No difference in the B(max) or K(d) of the warm-acclimated T. bernacchii accounted for the increase in Na/K-ATPase activity. We conclude that the change in gill Na/K-ATPase activity in the warm-acclimated T. bernacchii is not mediated by an increase in the number of enzyme sites and is not reflected in a change in ouabain affinity for Na/K-ATPase.

Acclimatization↗

Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography.

Heat stress sufficient to cause cellular damage triggers the heat-shock response, the enhanced expression of a group of molecular chaperones called heat-shock proteins (hsps). We compared the heat-shock responses of four species of marine snails of the genus Tegula that occupy thermal niches differing in absolute temperature and range of temperature. We examined the effects of short-term heat stress and thermal acclimation on the synthesis of hsps of size classes 90, 77, 70 and 38 kDa by measuring incorporation of (35)S-labeled methionine and cysteine into newly synthesized proteins in gill tissue. Temperatures at which enhanced synthesis of hsps first occurred (T(on)), temperatures of maximal induction of hsp synthesis (T(peak)) and temperatures at which hsp synthesis was heat-inactivated (T(off)) were lowest in two low-intertidal to subtidal species from the temperate zone, T. brunnea and T. montereyi, intermediate in a mid- to low-intertidal species of the temperate zone, T. funebralis, and highest in a subtropical intertidal species from the Gulf of California, T. rugosa. Synthesis of hsps and other classes of protein by T. brunnea and T. montereyi was heat-inactivated at temperatures commonly encountered by T. funebralis during low tides on warm days. In turn, protein synthesis by T. funebralis was blocked at the upper temperatures of the habitat of T. rugosa. Acclimation of snails to 13 degrees C, 18 degrees C and 23 degrees C shifted T(on) and T(peak) for certain hsps, but did not affect T(off). The heat-shock responses of field-acclimatized snails were generally reduced in comparison with those of laboratory-acclimated snails. Overall, despite the occurrence of acclimatory plasticity in their heat-shock responses, genetically fixed differences in T(on), T(peak) and T(off) appear to exist that reflect the separate evolutionary histories of these species and may play important roles in setting their thermal tolerance limits and, thereby, their biogeographic distribution patterns.

Journal Article↗

High temperature acclimation of C4 photosynthesis is linked to changes in photosynthetic biochemistry.

With average global temperatures predicted to increase over the next century, it is important to understand the extent and mechanisms of C4 photosynthetic acclimation to modest increases in growth temperature. To this end, we compared the photosynthetic responses of two C4 grasses (Panicum coloratum and Cenchrus ciliaris) and one C4 dicot (Flaveria bidentis) to growth at moderate (25/20 degrees C, day/night) or high (35/30 degrees C, day/night) temperatures. In all three C4 species, CO2 assimilation rates (A) underwent significant thermal acclimation, such that when compared at growth temperatures, A increased less than what would be expected given the strong response of A to short-term changes in leaf temperature. Thermal photosynthetic acclimation was further manifested by an increase in the temperature optima of A, and a decrease in leaf nitrogen content and leaf mass per area in the high- relative to the moderate-temperature-grown plants. Reduced photosynthetic capacity at the higher growth temperature was underpinned by selective changes in photosynthetic components. Plants grown at the higher temperature had lower amounts of ribulose-1,5-bisphosphate carboxylase/oxygenase and cytochrome f and activity of carbonic anhydrase. The activities of photosystem II (PSII) and phosphoenolpyruvate carboxylase were not affected by growth temperature. Chlorophyll fluorescence measurements of F. bidentis showed a corresponding decrease in the quantum yield of PSII (phi(PSII)) and an increase in non-photochemical quenching (phi(NPQ)). It is concluded that through these biochemical changes, C4 plants maintain the balance between the various photosynthetic components at each growth temperature, despite the differing temperature dependence of each process. As such, at higher temperatures photosynthetic nitrogen use efficiency increases more than A. Our results suggest C4 plants will show only modest changes in photosynthetic rates in response to changes in growth temperature, such as those expected within or between seasons, or the warming anticipated as a result of global climate change.

Adaptation, Physiological↗

Differential effects of temperature on macrophages of ectothermic vertebrates.

The role of macrophages in vertebrate defense reactions is especially important at low temperatures, which commonly affect representatives of ectothermic species. The aim of this work was to compare the effects of in vivo thermal acclimation and in vitro assay temperatures on peritoneal macrophages (PMs) from fish (carp and goldfish) and amphibians (salamanders and toads). The substratum adherence of PMs was undisturbed over the wide range of temperatures experienced by animals in nature. Dehydrogenases and endocytosis were sensitive to temperature fluctuations in a species-specific manner, more or less dependent on the previous thermal history of animals. The MTT reduction, inhibited by low assay temperatures, was slightly improved in PMs from cold-acclimated amphibians but not fishes. Endocytosis by the amphibian PMs, very efficient over the wide range of assay temperatures, was additionally improved by previous in vivo cold exposure. Contrasting effects of thermal acclimation were most evident in the case of endocytic properties of fish PMs; endocytosis by PMs from cold-acclimated fishes was extraordinarily efficient at a temperature just above zero, which almost completely inhibited cells from fishes adapted to warmth.

Animals↗