Physiological responses in a variable environment: relationships between metabolism, hsp and thermotolerance in an intertidal-subtidal species

Physiological responses to temperature reflect the evolutionary adaptations of organisms to their thermal environment and the capability of animals to tolerate thermal stress. Contrary to conventional metabolism theory, increasing environmental temperatures have been shown to reduce metabolic rate in rocky-eulittoral-fringe species inhabiting highly variable environments, possibly as a strategy for energy conservation. To study the physiological adaptations of an intertidal-subtidal species to the extreme and unpredictable heat stress of the intertidal zone, oxygen consumption rate and heat shock protein expression were quantified in the sea cucumber Apostichopus japonicus. Using simulate natural temperatures, the relationship between temperature, physiological performance (oxygen consumption and heat shock proteins) and thermotolerance were assessed. Depression of oxygen consumption rate and upregulation of heat shock protein genes (hsps) occurred in sequence when ambient temperature was increased from 24 to 30°C. Large-scale mortality of the sea cucumber occurred when temperatures rose beyond 30°C, suggesting that the upregulation of heat shock proteins and mortality are closely related to the depression of aerobic metabolism, a phenomenon that is in line with the concept of oxygen- and capacity-limited thermal tolerance (OCLTT). The physiologically-related thermotolerance of this sea cucumber should be an adaptation to its local environment.     

Antioxidant responses of Atlantic Forest native tree species as indicators of increasing tolerance to oxidative stress when they are exposed to air pollutants and seasonal tropical climate

Tropical forest ecosystems may be subjected to climate-origin oxidative stress as it is observed in Southeast Brazil. The region is characterized by seasonal climate with well-defined wet and dry periods. Anthropogenic air pollutants are additional oxidative stress sources in these ecosystems. However, the tolerance of Brazilian tree species to oxidative stress is still unknown. Thus, the current field study aims to comparatively establish the range of antioxidant responses of ascorbate-glutathione cycle in Astronium graveolens, Croton floribundus and Piptadenia gonoacantha adult trees exposed to air pollutants and seasonal tropical climate as indicators of their increasing tolerance to oxidative stress. These are the most abundant species in the semideciduous Atlantic Forest, in Southeast Brazil. Variations in biochemical leaf traits (antioxidant defenses: ascorbate peroxidase, catalase, superoxide dismutase, glutathione reductase, ascorbate and glutathione; pigments: chlorophyll a, b and carotenoid; oxidative damage indicators: hydrogen peroxide and lipid peroxidation indicator) were determined. The native Brazilian tree species revealed distinct biochemical patterns in response to environmental oxidative stress during the wet and dry seasons. Biochemical leaf traits changed mainly in response to photoxidative stress, during the wet season. This variation was stimulated by better climate conditions to photosynthesis and plant growth, such as high light energy, water availability and temperatures. Catalase seemed to be the biochemical leaf tolerance indicator in all species during the wet season. The environmental conditions during the dry season, either of natural or anthropogenic origin, were stressful to the Brazilian tree species. They induced several changes in their biochemical leaf traits. Such changes were indicated by multilinear regression analyses. Oxidative/antioxidative imbalances, such as increased lipid peroxidation and decreased glutathione as well as the chlorophyll contents, were the most appropriate oxidative stress indicators during the dry season. C. floribundus was the most efficient species in terms of oxidative stress tolerance and it was followed by A. graveolens and P. gonoacantha.     

Adjustment of metabolite composition in the haemolymph to seasonal variations in the land snail <Emphasis Type="Italic">Helix pomatia</Emphasis>

In temperate regions, land snails are subjected to subzero temperatures in winter and hot temperatures often associated to drought in summer. The response to these environmental factors is usually a state of inactivity, hibernation and aestivation, respectively, in a temperature and humidity buffered refuge, accompanied by physiological adjustments to resist cold or heat stress. We investigated how environmental factors in the microhabitat and body condition influence the metabolite composition of haemolymph of the endangered species Helix pomatia. We used UPLC and GC–MS techniques and analyzed annual biochemical variations in a multivariate model. Hibernation and activity months differed in metabolite composition. Snails used photoperiod as cue for seasonal climatic variations to initiate a physiological state and were also highly sensitive to temperature variations, therefore constantly adjusting their physiological processes. Galactose levels gave evidence for the persistence of metabolic activity with energy expenditure during hibernation and for high reproductive activity in June. Triglycerides accumulated prior to hibernation might act as cryoprotectants or energy reserves. During the last month of hibernation snails activated physiological processes related to arousal. During activity, protein metabolism was reflected by high amino acid level. An exceptional aestivation period was observed in April giving evidence for heat stress responses, like the protection of cells from dehydration by polyols and saccharides, the membrane stabilization by cholesterol and enhanced metabolism using the anaerobic succinic acid pathway to sustain costly stress responses. In conclusion, physiological adjustments to environmental variations in Helix pomatia involve water loss regulation, cryoprotectant or heatprotectant accumulation.     

Respiratory metabolism in pacifastacus leniusculus (Dana) (crustacea: decapoda) as related to its ecology

Summary Respiratory metabolism in the high-altitude crayfish, Pacifastacus leniusculus from Lake Tahoe (California-Nevada, U.S.A.) was investigated in a series of laboratory experiments. In general, oxygen consumption was found to be directly proportional to size when expressed per individual, and inversely proportional to size when expressed per ash-free gram dry weight per unit time. No significant variations in respiratory rates were observed between males and females. There was little variation in uptake over a temperature range of 5°C to 12.5°C, while the lowest and highest uptake values were observed at 0°C and 15°C respectively. An increase in temperature above 15°C, however, resulted in a decrease in respiratory activity. These results closely correlate with patterns of ventilatory activity, oxygen extraction efficiency, and seasonal feeding and reproductive activity in Pacifastacus as related to the annual temperature profile for their Lake Tahoe habitat. These results, as well as the extremely low tolerance of this species for low oxygen levels, suggest temperature as the possible critical environmental factor in the determination of the nature of seasonal metabolic cycles. It is concluded that Pacifastacus shows little tolerance for fluctuations in environmental oxygen and temperature and is well adapted to the narrow range of condition present in its Lake Tahoe habitat.     

Ecological relevance of laboratory determined temperature limits: colonization potential,biogeography and resilience of Antarctic invertebrates to environmental change

The relevance of laboratory experiments in predicting effects of climate change has been questioned, especially in Antarctica where sea temperatures are remarkably stable. Laboratory studies of Southern Ocean marine animal capacities to survive increasing temperature mainly utilize rapid temperature elevations, 100 ×–10 000 × faster than sea temperature is predicted to rise. However, due to small‐scale temperature fluctuations these studies may be crucial for understanding colonization patterns and predicting survival particularly through interactions between thermal tolerance and migration. The colonization of disjunct shelves around Antarctica by larvae or adult drift requires crossing or exposure to, rapid temperature changes of up to 2–4 °C over days to weeks. Analyses of responses to warming at varying rates of temperature change in the laboratory allow better predictions of the potential species have for colonizing disjunct shelf areas (such as the Scotia Arc). Inhabiting greater diversities of localities increases the geographic and thermal range species experience. We suggest a strong link between short‐term temperature tolerance, environmental range and prospects for surviving changing environments.     

Is there a trade-off between peak performance and performance breadth across temperatures for aerobic scope in teleost fishes?

The physiology and behaviour of ectotherms are strongly influenced by environmental temperature. A general hypothesis is that for performance traits, such as those related to growth, metabolism or locomotion, species face a trade-off between being a thermal specialist or a thermal generalist, implying a negative correlation between peak performance and performance breadth across a range of temperatures. Focusing on teleost fishes, we performed a phylogenetically informed comparative analysis of the relationship between performance peak and breadth for aerobic scope (AS), which represents whole-animal capacity available to carry out simultaneous oxygen-demanding processes (e.g. growth, locomotion, reproduction) above maintenance. Literature data for 28 species indicate that peak aerobic capacity is not linked to thermal performance breadth and that other physiological factors affecting thermal tolerance may prevent such a trade-off from emerging. The results therefore suggest that functional links between peak and thermal breadth for AS may not constrain evolutionary responses to environmental changes such as climate warming.     

Does cold tolerance plasticity correlate with the thermal environment and metabolic profiles of a parasitoid wasp?

Tolerance of ectotherm species to cold stress is highly plastic according to thermal conditions experienced prior to cold stress. In this study, we investigated how cold tolerance varies with developmental temperature (at 17, 25 and 30 °C) and whether developmental temperature induces different metabolic profiles. Experiments were conducted on the two populations of the parasitoid wasp, Venturia canescens, undergoing contrasting thermal regimes in their respective preferential habitat (thermally variable vs. buffered). We predicted the following: i) development at low temperatures improves the cold tolerance of parasitoid wasps, ii) the shape of the cold tolerance reaction norm differs between the two populations, and iii) these phenotypic variations are correlated with their metabolic profiles. Our results showed that habitat origin and developmental acclimation interact to determine cold tolerance and metabolic profiles of the parasitoid wasps. Cold tolerance was promoted when developmental temperatures declined and population originating from variable habitat presented a higher cold tolerance. Cold tolerance increases through the accumulation of metabolites with an assumed cryoprotective function and the depression of metabolites involved in energy metabolism. Our data provide an original example of how intraspecific cold acclimation variations correlate with metabolic response to developmental temperature.     

Cold stress and acclimation – what is important for metabolic adjustment?

As sessile organisms, plants are unable to escape from the many abiotic and biotic factors that cause a departure from optimal conditions of growth and development. Low temperature represents one of the most harmful abiotic stresses affecting temperate plants. These species have adapted to seasonal variations in temperature by adjusting their metabolism during autumn, increasing their content of a range of cryo‐protective compounds to maximise their cold tolerance. Some of these molecules are synthesised de novo. The down‐regulation of some gene products represents an additional important regulatory mechanism. Ways in which plants cope with cold stress are described, and the current state of the art with respect to both the model plant Arabidopsis thaliana and crop plants in the area of gene expression and metabolic pathways during low‐temperature stress are discussed.     

Seasonal changes in thermal environment and metabolic enzyme activity in the diamondback terrapin (Malaclemys terrapin)

Diamondback terrapins experience broad fluctuations in temperature on both a daily and seasonal basis in their estuarine environment. We measured metabolic enzyme activity in terrapin muscle tissue to assess thermal dependence and the role of temperature in seasonal metabolic downregulation in this species. Activity of lactate dehydrogenase (LDH), pyruvate kinase (PK), citrate synthase (CS), and cytochrome c oxidase (CCO) was assayed at 10, 20, 30, and 40 °C for tissue collected during summer and winter. The Q(10) for enzyme activity varied between 1.31 and 2.11 within the temperature range at which terrapins were active (20-40 °C). The Q(10) for LDH, CS, and CCO varied between 1.39 and 1.76 and between 10 and 20 °C, but PK exhibited heightened thermal sensitivity within this lower temperature range, with a Q(10) of 2.90 for summer-collected tissue and 5.55 for winter-collected tissue. There was no significant effect of season on activity of LDH or PK, but activity of CS and CCO was significantly lower in winter-collected tissue compared with summer-collected tissue. Results indicate that temperature effects contribute to seasonal metabolic downregulation and dormancy in terrapins, but other environmental factors (i.e. oxygen availability), as well as seasonal shifts in blood biochemistry and circulating hormones may also play an important role.     

Intestinal barrier function of Atlantic salmon (<Emphasis Type="Italic">Salmo salar</Emphasis> L.) post smolts is reduced by common sea cage environments and suggested as a possible physiological welfare indicator

Background  

Fish farmed under high intensity aquaculture conditions are subjected to unnatural environments that may cause stress. Therefore awareness of how to maintain good health and welfare of farmed fish is important. For Atlantic salmon held in sea cages, water flow, dissolved oxygen (DO) levels and temperature will fluctuate over time and the fish can at times be exposed to detrimentally low DO levels and high temperatures. This experimental study investigates primary and secondary stress responses of Atlantic salmon post smolts to long-term exposure to reduced and fluctuating DO levels and high water temperatures, mimicking situations in the sea cages. Plasma cortisol levels and cortisol release to the water were assessed as indicators of the primary stress response and intestinal barrier integrity and physiological functions as indicators of secondary responses to changes in environmental conditions.     

What do warming waters mean for fish physiology and fisheries?

Environmental signals act primarily on physiological systems, which then influence higher-level functions such as movement patterns and population dynamics. Increases in average temperature and temperature variability associated with global climate change are likely to have strong effects on fish physiology and thereby on populations and fisheries. Here we review the principal mechanisms that transduce temperature signals and the physiological responses to those signals in fish. Temperature has a direct, thermodynamic effect on biochemical reaction rates. Nonetheless, plastic responses to longer-term thermal signals mean that fishes can modulate their acute thermal responses to compensate at least partially for thermodynamic effects. Energetics are particularly relevant for growth and movement, and therefore for fisheries, and temperature can have pronounced effects on energy metabolism. All energy (ATP) production is ultimately linked to mitochondria, and temperature has pronounced effects on mitochondrial efficiency and maximal capacities. Mitochondria are dependent on oxygen as the ultimate electron acceptor so that cardiovascular function and oxygen delivery link environmental inputs with energy metabolism. Growth efficiency, that is the conversion of food into tissue, changes with temperature, and there are indications that warmer water leads to decreased conversion efficiencies. Moreover, movement and migration of fish relies on muscle function, which is partially dependent on ATP production but also on intracellular calcium cycling within the myocyte. Neuroendocrine processes link environmental signals to regulated responses at the level of different tissues, including muscle. These physiological processes within individuals can scale up to population responses to climate change. A mechanistic understanding of thermal responses is essential to predict the vulnerability of species and populations to climate change.     

Phenotypic plasticity in temperature stress resistance is triggered by photoperiod in a fly

Temperature variation poses a substantial challenge for individual survival and reproductive success, warranting effective means to counter negative effects of temperature extremes. Phenotypic plasticity offers a particularly powerful mechanism to cope with short-time temperature fluctuations. While temperature-induced plasticity in thermal tolerance has been widely explored, effects of other environmental factors have received much less attention. Using a full-factorial design we here show that variation in temperature stress resistance can be triggered by photoperiod (and temperature) in the fly Protophormia terraenovae, with shorter day lengths inducing more cold- and longer day lengths more heat-tolerant phenotypes. Such plastic changes were not related to different developmental pathways (reproductive activity or reproductive diapause), and can be induced during development but also in the adult stage (at least for cold tolerance). We suggest that short-term, photoperiod-mediated changes in insect thermal tolerance represent a mechanism of adaptive seasonal plasticity. Photoperiod further affected development time and body size, the significance of which is currently unclear.     

THERMAL ECOPHYSIOLOGY OF LAURENCIA PACIFICA AND LAURENCIA NIDIFICA (CERAMIALES,RHODOPHYTA) FROM TROPICAL AND WARM‐TEMPERATE REGIONS1

Laurencia is a globally distributed genus with about 80 species (order Ceramiales) that inhabit tropical, subtropical, and warm‐temperate regions of both sides of the Atlantic and Indo‐Pacific oceans. This study investigated how two species of Laurencia distributed in different thermal environments (California and Hawaii) varied in their photosynthetic responses to temperature. The thermal ecophysiology of both species was investigated at different temporal scales (short‐term responses and seasonal acclimatization) using oxygen evolution and pulse‐amplitude‐modulated (PAM) fluorometry. Our results indicated that seasonal acclimatization of both species of Laurencia influenced the short‐term photosynthetic response at both locations. Greater seasonal differences in the photosynthetic performance were observed for L. pacifica Kylin, which reflects the ability of this species to acclimatize to local environmental conditions characterized by short‐term fluctuations and a broader annual temperature range. Photosynthetic performance of L. nidifica J. Agardh was consistent with the less variable local environment (no short‐term fluctuations and a narrower temperature range). These results suggest that acclimatization to temperature variability in the environment can influence the degree of flexibility of physiological responses of species in this genus.     

Effect of the rate of temperature increase of the dynamic method on the heat tolerance of fishes

Heat tolerance is commonly determined by exposing organisms to increasing temperatures until they show symptoms of thermal stress or death. Here we carried out an experiment on a blenny species (Acantemblemaria hancocki; Pisces: Chaenopsidae) and reviewed the literature to evaluate the extent to which variations in the rate at which temperature is increased in experimental trials affects thermal tolerance of fishes. For the blenny species, we found that thermal tolerance decreases significantly from an intermediate heating rate of ∼1 °C/h towards quicker and slower heating rates. In the literature we found very few comparisons of thermal tolerance among heating rates (i.e. eight fish species) and although such comparisons were done over narrow ranges of heating rates, overall they appear to follow the pattern described for the blenny species. We discuss a variety of factors including variations in the levels of acclimation, energy use and body quality among heating rates as the causes for this pattern. However, available data are still limited and further research will be necessary to determine the generality and causes of the pattern we found here. Nevertheless, our results indicate the need for caution in the extrapolation of thermal tolerance data when assessing the tolerance of organisms to environmental phenomena that vary in their rates of warming.     

Multigenerational analysis of temperature and salinity variability affects on metabolic rate,generation time,and acute thermal and salinity tolerance in Daphnia pulex

Climate change, sea level rise, and human freshwater demands are predicted to result in elevated temperature and salinity variability in upper estuarine ecosystems. Increasing levels of environmental stresses are known to induce the cellular stress response (CSR). Energy for the CSR may be provided by an elevated overall metabolic rate. However, if metabolic rate is constant or lower under elevated stress, energy for the CSR is taken from other physiological processes, such as growth or reproduction. This study investigated the examined energetic responses to the combination of temperature and salinity variability during a multigenerational exposure of partheogenetically reproducing Daphnia pulex. We raised D. pulex in an orthogonal combination of daily fluctuations in temperature (15, 15–25, 15–30 °C) and salinity (0, 0–2, 0–5). Initially metabolic rates were lower under all variable temperature and variable salinity treatments. By the 6th generation there was little metabolic variation among low and intermediate temperature and salinity treatments, but metabolic suppression persisted at the most extreme salinity. When grown in the control condition for the 6th generation, metabolic suppression was only observed in D. pulex from the most extreme condition (15–30 °C, 0–5 salinity). Generation time was influenced by acclimation temperature but not salinity and was quickest in specimens reared at 15–25 °C, likely due to Q₁₀ effects at temperatures closer to the optima for D. pulex, and slowest in specimens reared at 15–30 °C, which may have reflected elevated CSR. Acute tolerance to temperature (LT₅₀) and salinity (LC₅₀) were both highest in D. pulex acclimated to 15–30 °C and salinity 0. LT₅₀ and LC₅₀ increased with increasing salinity in specimens raised at 15 °C and 15–25 °C, but decreased with increasing salinity in specimens raised at 15–30 °C. Thus, increasing temperature confers cross-tolerance to salinity stress, but the directionality of synergistic effects of temperature and salinity depend on the degree of environmental variability. Overall, the results of our study suggest that temperature is a stronger determinant of metabolism, growth, and tolerance thresholds, and assessment of the ecological impacts of environmental change requires explicit information regarding the degree of environmental variability.     

The role of environmental factors in the induction of oxidative stress in zebra mussel (<Emphasis Type="Italic">Dreissena polymorpha</Emphasis>)

The aim of this study was to investigate the influence of specific environmental factors, such as temperature, pH, oxygen concentration, and phosphate, nitrate, chloride, sodium, potassium, sulphate, magnesium and calcium ions concentration, as well as microcystins, on the seasonal variations in the activity of the antioxidant system of the zebra mussel. We examined changes in lipid peroxidation (LPO) levels, glutathione content and the catalase activity of mussels inhabiting the two ecosystems, which differ due to their trophic structure and the presence of toxic cyanobacteria. The results show a relationship between the activity of the antioxidant system of zebra mussels and the seasonal fluctuations of environmental parameters: the symptoms of oxidative stress were generally the highest during spring and the lowest during summer in both ecosystems. Our study also revealed that regardless of the study area the most important factors determining the activity of the antioxidant defences of mussels were the mineral composition (particularly magnesium and calcium ions concentrations) and physical parameters of the water (oxygen concentration and pH). However, factors resulting from the trophic status of studied ecosystems, such as limitations in food resources or high concentration of microcystins during cyanobacterial blooms, were periodically responsible for increased level of LPO in the tissues of zebra mussel. These findings may indicate a limited tolerance of the zebra mussel to the local environmental conditions.     

Influences of body mass,temperature, oxygen tension,and salinity on respiratory oxygen consumption of cyprinodontoid fishes of three families

This review evaluates the current state of knowledge of influences of body mass, ambient temperature, P_O2, and salinity on routine metabolic rates of members of three families, Fundulidae, Cyprinodontidae, and Poeciliidae, belonging to the order Cyprinodontiformes. The study was motivated by Winberg’s (Fisheries Research Board of Canada, Translation Series No. 194. Distributed by the Fisheries Research Board of Canada Biological Station, Nanaimo, BC, 1960) conclusion that the Cyprinodontiformes (Winberg included only live-bearing poeciliids) generally have lower metabolic rates that do other fishes. Based on available information Winberg’s conclusion was borne out that live-bearing freshwater poeciliids show lower than average routine metabolic rates compared to other freshwater fish groups. This is also true of poeciliids from saline waters, and of both freshwater and saline-water members of the related families Fundulidae and Cyprinodontidae. However, considerable variation in metabolic patterns was noted within and among these three families. There were geographic variations between subspecies of some species. Some island groups/species showed lower routine metabolic rates than did allied mainland groups/species. Thermal responses (Q₁₀ values) in routine metabolic rates of these fishes showed variations with geographic location, P_O2, salinity and size. Values of P_O2crit were altered among species by temperature, body size/age, and possibly salinity. Influences of ambient salinity on routine metabolic rates of these cyprinodontoid fishes also showed variations with temperature and size/age of individuals. The patterns of metabolic responses in these cyprinodontoid fishes to environmental conditions were generally similar to those of other species. Unfortunately, the available information on these fishes lacks the uniformity that would allow for critical and quantitative comparisons between and among the cyprinodontoids and with other species.