No full-text available
To read the full-text of this research,
you can request a copy directly from the authors.
Slow heating rates increase thermal tolerance and alter mRNA HSP expression in juvenile white sturgeon (Acipenser transmontanus)
Abstract
Freshwater fish such as white sturgeon (Acipenser transmontanus) are particularly vulnerable to the effects of anthropogenically induced global warming. Critical thermal maximum tests (CTmax) are often conducted to provide insight into the impacts of changing temperatures; however, little is known about how the rate of temperature increase in these assays affects thermal tolerance. To assess the effect of heating rate (0.3 °C/min, 0.03 °C/min, 0.003 °C/min) we measured thermal tolerance, somatic indices, and gill Hsp mRNA expression. Contrary to what has been observed in most other fish species, white sturgeon thermal tolerance was highest at the slowest heating rate of 0.003 °C/min (34.2 °C, and CTmax of 31.3 and 29.2 °C, for rates 0.03 and 0.3 °C/min, respectively) suggesting an ability to rapidly acclimate to slowly increasing temperatures. Hepatosomatic index decreased in all heating rates relative to control fish, indicative of the metabolic costs of thermal stress. At the transcriptional level, slower heating rates resulted in higher gill mRNA expression of Hsp90a, Hsp90b, and Hsp70. Hsp70 mRNA expression was increased in all heating rates relative to controls, whereas expression of Hsp90a and Hsp90b mRNA only increased in the two slower trials. Together these data indicate that white sturgeon have a very plastic thermal response, which is likely energetically costly to induce. Acute temperature changes may be more detrimental to sturgeon as they struggle to acclimate to rapid changes in their environment, however under slower warming rates they demonstrate strong thermal plasticity to warming.
... Trials were run by increasing temperature 0.3 • C·min −1 with immersed titanium heater sticks (finnex TITANIUM 300+) until the larvae lost equilibrium (LOE) and were unable to right themselves after a disturbance (i.e. touching their caudal tail with a blunted probe; Bard and Kieffer, 2019;Yoon et al., 2019;Bugg et al., 2020;Penman et al., 2023). Air saturation was maintained >95% throughout the trial through bubbling air through air stones. ...
... There were a few genes that were affected by CTmax (Fig. 7) as determined by ANOVA, including hsp70, hsp90b, g6p and pepck-c (P-values are reported in S1). Interestingly, the only gene that increased expression in all temperature groups after CTmax was hsp70; in older white sturgeon, we typically observe an increase in additional hsps after acute thermal stress (Earhart et al., Unpublished data;Penman et al., 2023). ...
... The ARRs reported here, 1.4 (between 14 and 18 • C) and 0.9 (between 18 and 21 • C), are twice as high compared with other fishes (Morley et al., 2019) and thus highlights the outstanding ability of larval white sturgeon to accrue thermal tolerance through acclimation. In fact, across North American sturgeon species, there are reports of impressive increases in thermal tolerance as demonstrated by relative (Wilkes, 2011;Zhang and Kieffer, 2014;Bard and Kieffer, 2019;Rodgers et al., 2019;Bugg et al., 2020;Penman et al., 2023;Earhart et al., Unpublished data). This large acclimatory capacity of sturgeons compared with other fishes may be a result of having large genomes regulating their thermal plasticity, and this would greatly benefit an ancient, long-lived species (Fontana et al., 2004;Ellis et al., 2014;Bugg et al., 2020). ...
Climate change-induced warming effects are already evident in river ecosystems, and projected increases in temperature will continue to amplify stress on fish communities. In addition, many rivers globally are impacted by dams, which have many negative effects on fishes by altering flow, blocking fish passage, and changing sediment composition. However, in some systems, dams present an opportunity to manage river temperature through regulated releases of cooler water. For example, there is a government mandate for Kenney dam operators in the Nechako river, British Columbia, Canada, to maintain river temperature <20°C in July and August to protect migrating sockeye salmon (Oncorhynchus nerka). However, there is another endangered fish species inhabiting the same river, Nechako white sturgeon (Acipenser transmontanus), and it is unclear if these current temperature regulations, or timing of the regulations, are suitable for spawning and developing sturgeon. In this study, we aimed to identify upper thermal thresholds in white sturgeon embryos and larvae to investigate if exposure to current river temperatures are playing a role in recruitment failure. We incubated embryos and yolk-sac larvae in three environmentally relevant temperatures (14, 18 and 21°C) throughout development to identify thermal thresholds across different levels of biological organization. Our results demonstrate upper thermal thresholds at 21°C across physiological measurements in embryo and yolk-sac larvae white sturgeon. Before hatch, both embryo survival and metabolic rate were reduced at 21°C. After hatch, sublethal consequences continued at 21°C because larval sturgeon had decreased thermal plasticity and a dampened transcriptional response during development. In recent years, the Nechako river has reached 21°C by the end of June, and at this temperature, a decrease in sturgeon performance is evident in most of the traits measured. As such, the thermal thresholds identified here suggest current temperature regulations may not be suitable for developing white sturgeon and future recruitment.
... As aforementioned, yolk-sac larvae White Sturgeon recently demonstrated one of the highest ARRs reported thus far (1.4) when acclimated to 14 and 18 • C (Earhart et al., 2023a). This ARR decreased to 0.9 between 18 and 21 • C (Earhart et al., 2023a), and it is thought that for northern species of sturgeon, plasticity decreases as acclimation temperatures approach 20 • C (Zhang and Kieffer, 2014;Bugg et al., 2020;Bugg et al., 2023;Penman et al., 2023). While we do not see a plateauing effect with upper thermal limits in the YOY southern White Sturgeon examined here, ARR is lower between subsequent acclimation temperatures and thermal safety margins (the difference between upper thermal limit and acclimation temperature) decrease from 15.4 • C for 14 • C-acclimated fish to 12.1 • C for 22 • C-acclimated fish. ...
... Though effect sizes of temperature were large for warm-acclimated fish, the confidence intervals calculated with Cohen's d suggest that this declining pattern is not significant for HSI or SSI. This is inconsistent with previous studies of sturgeon and other fishes, where HSI significantly decreases with warmer temperature and may indicate increased mobilization of energy stores with increased energetic costs (Rossi et al., 2017;Bugg et al., 2020;Penman et al., 2023). Instead, warmacclimated White Sturgeon demonstrated significantly lower RVM. ...
Assessing how at-risk species respond to co-occurring stressors is critical for predicting climate change vulnerability. In this study, we characterized how young-of-the-year White Sturgeon (Acipenser transmontanus) cope with warming and low oxygen (hypoxia) and investigated whether prior exposure to one stressor may improve the tolerance to a subsequent stressor through “cross-tolerance”. Fish were acclimated to five temperatures within their natural range (14-22°C) for one month prior to assessment of thermal tolerance (critical thermal maxima, CTmax) and hypoxia tolerance (incipient lethal oxygen saturation, ILOS; tested at 20°C). White Sturgeon showed a high capacity for thermal acclimation, linearly increasing thermal tolerance with increasing acclimation temperature (slope = 0.55, adjusted R2 = 0.79), and an overall acclimation response ratio (ARR) of 0.58, from 14°C (CTmax = 29.4 ± 0.2°C, mean ± S.E.M.) to 22°C (CTmax = 34.1 ± 0.2°C). Acute warming most negatively impacted hypoxia tolerance in 14°C-acclimated fish (ILOS = 15.79 ± 0.74% air saturation), but prior acclimation to 20°C conferred the greatest hypoxia tolerance at this temperature (ILOS = 2.60 ± 1.74% air saturation). Interestingly, individuals that had been previously tested for thermal tolerance had lower hypoxia tolerance than naïve fish that had no prior testing. This was particularly apparent for hypoxia-tolerant 20°C-acclimated fish, whereas naïve fish persisted the entire 15-h duration of the hypoxia trial and did not lose equilibrium at air saturation levels below 20%. Warm-acclimated fish demonstrated significantly smaller relative ventricular mass, indicating potential changes to tissue oxygen delivery, but no other changes to red blood cell characteristics and somatic indices. These data suggest young-of-the-year White Sturgeon are resilient to warming and hypoxia, but the order in which these stressors are experienced and whether exposures are acute or chronic may have important effects on phenotype.
... Moreover, the use of different methods or protocols might impact the estimation of thermal traits (Chown et al., 2009;Pottier, Burke, Drobniak, et al., 2022;Rohr et al., 2018;Terblanche et al., 2007; but not . For example, acclimation duration (i.e., how long organisms were held at an acclimation temperature before being exposed to the test temperature; Rohr et al., 2018;Ruthsatz, Dausmann, et al., 2022) and ramping protocol (i.e., heating or cooling rate in thermal tolerance trials; Illing et al., 2020;Penman et al., 2023) have been suggested to influence measurements of acclimation capacity, as the underlying physiological processes occur over certain time periods. ...
... The estimates are sensitive to differences in the methods. For example, faster ramping (heating) rates tend to yield higher thermal tolerance estimates compared to slower ramping rates (Kovacevic et al., 2019;Moyano et al., 2017;Penman et al., 2023). ...
Amphibians and fishes play a central role in shaping the structure and function of freshwater environments. These organisms have a limited capacity to disperse across different habitats and the thermal buffer offered by freshwater systems is small. Understanding determinants and patterns of their physiological sensitivity across life history is, therefore, imperative to predicting the impacts of climate change in freshwater systems. Based on a systematic literature review including 345 experiments with 998 estimates on 96 amphibian (Anura/Caudata) and 93 freshwater fish species (Teleostei), we conducted a quantitative synthesis to explore phylogenetic, ontogenetic, and biogeographic (thermal adaptation) patterns in upper thermal tolerance (CT max ) and thermal acclimation capacity (acclimation response ratio, ARR) as well as the influence of the methodology used to assess these thermal traits using a conditional inference tree analysis. We found globally consistent patterns in CT max and ARR, with phylogeny (taxa/order), experimental methodology, climatic origin, and life stage as significant determinants of thermal traits. The analysis demonstrated that CT max does not primarily depend on the climatic origin but on experimental acclimation temperature and duration, and life stage. Higher acclimation temperatures and longer acclimation times led to higher CT max values, whereby Anuran larvae revealed a higher CT max than older life stages. The ARR of freshwater fishes was more than twice that of amphibians. Differences in ARR between life stages were not significant. In addition to phylogenetic differences, we found that ARR also depended on acclimation duration, ramping rate, and adaptation to local temperature variability. However, the amount of data on early life stages is too small, methodologically inconsistent, and phylogenetically unbalanced to identify potential life cycle bottlenecks in thermal traits. We, therefore, propose methods to improve the robustness and comparability of CT max /ARR data across species and life stages, which is crucial for the conservation of freshwater biodiversity under climate change.
... Also, there may be inaccuracies in the magnitude of the sturgeons' thermal exposure because of the daily timestep temperature outputs of the model. Sturgeons are known to have a high degree of thermal plasticity (Bugg et al., 2020;Penman, 2021;Penman et al., 2023), where thermal tolerance increases with acclimation temperature. This could only be nested in our integrative approach with an hourly time-step hydrological model. ...
Water temperature plays a crucial role in the physiology of aquatic species, particularly in their survival and development. Thus, resource programs are commonly used to manage water quality conditions for endemic species. In a river system like the Nechako River system, central British Columbia, a water management program was established in the 1980s to alter water release in the summer months to prevent water temperatures from exceeding a 20 °C threshold downstream during the spawning season of Sockeye salmon (Oncorhynchus nerka). Such a management regime could have consequences for other resident species like the white sturgeon (Acipenser transmontanus). Here, we use a hydrothermal model and white sturgeon life stage-specific experimental thermal tolerance data to evaluate water releases and potential hydrothermal impacts based on the Nechako water management plan (1980-2019). Our analysis focused mainly on the warmest five-month period of the year (May to September), which includes the water release management period (July-August). Our results show that the thermal exposure risk, an index that measures temperature impact on species physiology of Nechako white sturgeon across all early life stages (embryo, yolk-sac larvae, larvae, and juvenile) has increased substantially, especially in the 2010s relative to the management program implementations' first decade (the 1980s). The embryonic life stage was the most impacted, with a continuous increase in potential adverse thermal exposure in all months examined in the study. We also recorded major impacts of increased thermal exposure on the critical habitats necessary for Nechako white sturgeon recovery. Our study highlights the importance of a holistic management program with consideration for all species of the Nechako River system and the merit of possibly reviewing the current management plan, particularly with the current concerns about climate change impacts on the Nechako River.
Climate change is impacting river ecosystems, underlining the need for water management strategies to protect native species within these ecosystems. Here, we evaluate the impact of climate change and water management on the physiology of white sturgeon (Acipenser transmontanus) in the Nechako River, British Columbia (Canada). Using the CEQUEAU hydrological–thermal model, we simulated daily water temperatures from 1980 to 2099 under two climate scenarios (SSP2-4.5 and SSP5-8.5). We assessed thermal exposure risk (Te) for different developmental stages of white sturgeon, focusing on the warmest 6-month period. Our findings show that embryos and yolk-sac larvae exhibit resilience, with Te values consistently <1 under both scenarios, signifying low thermal stress. In contrast, feeding larvae and juveniles experience elevated Te values, indicating significant future thermal stress. For feeding larvae, Te values exceeded 1 under both scenarios, reaching up to 1.5 by the mid-century (2050s) and up to 1.8 by the end of the century (2090s) under SSP5-8.5. Juvenile white sturgeon also faced increased thermal risks, with Te values rising >1 during July and August, reaching 1.4 and 1.8 by the 2050s and 1.8 and 2.0 by the 2090s under SSP5-8.5, compared to the 1980s. These results underscore the need to evaluate the existing water management programme to better accommodate the projected changes in thermal conditions associated with climate change. Additionally, regulated river discharge, which can both increase and decrease downstream temperatures, offers a strategic opportunity to mitigate some climate impacts through strategic dam discharge management.
Critical thermal limits, commonly quantified as CTmax (maximum) or CTmin (minimum), are core metrics in the thermal biology of aquatic ectotherms. CTmax, in particular, has recently surged in popularity due to its various applications, including understanding and predicting the responses of animals to climate warming. Despite its growing popularity, there is a limited literature aimed at establishing best practices for designing, running, and reporting CTmax experiments. This lack of standardisation and insufficiently detailed reporting in the literature creates challenges when designing CTmax studies or comparing results across studies. Here, we provide a comprehensive, practical guide for designing and conducting experiments to measure critical thermal limits, with an emphasis on CTmax. Our recommendations cover 12 topic areas including apparatus design, masking (blinding), warming rates, endpoints, replication, and reporting. We include diagrams and photos for designing and building critical thermal limit arenas for field or lab applications. We also provide a reporting checklist as a reference for researchers when carrying out experiments and preparing manuscripts. Future studies incorporating critical thermal limits would benefit from transparent reporting of warming/cooling rates (raw data, supplementary graphs) and photo/video evidence showing arena designs and critical thermal limit endpoints. We also provide directions for empirical research that will help further inform the measurement of critical thermal limits, including on biotic factors like stress and digestion, warming/cooling rates, the effects of body mass on heat transfer, and the physiological mechanisms underlying thermal tolerance.
The Amazon basin contains more than 15% of the world’s freshwater fishes, many of ecological and economical importance. Unfortunately, research suggests that tropical species, which have adapted to a thermally stable environment, are most at risk with a long-term increase above current temperatures, which is worrisome when the Amazon could experience an increase in air temperature of up to +6.5 °C within the next century. In this chapter, we review the thermal limits of Amazonian fishes and their capacity to acclimate to warm temperatures. Furthermore, we explore how this thermal tolerance data may be incorporated into prediction models to evaluate Amazonian fish’s vulnerability to thermal stress and highlight the research that is needed to better understand their capacity to acclimate to a warming world.
Understanding how ectotherms may fare with rising global temperatures and more frequent heatwaves is especially concerning for species already considered at‐risk, such as long‐lived, late‐maturing sturgeon. There have been concerted efforts to collect data on the movement behavior and thermal physiology of North American sturgeon to enhance conservation efforts; thus, we sought to synthesize these data to understand how sturgeon respond to thermal stress and what capacity they have to acclimate and adapt to warming. Here, we combined a systematic literature review and meta‐analysis, integrating field‐based observations (distribution and spawning) and laboratory‐based experiments (survival, activity, growth, metabolism, and upper thermal limits) for large‐scale insights to understand the vulnerability of North American sturgeon to rising global temperatures. We summarized the preferred thermal habitat and thermal limits of sturgeon in their natural environment and using meta‐analytical techniques, quantified the effect of prolonged temperature change on sturgeon whole‐animal physiology and acute upper thermal limits. While acclimation did not have significant effects on physiological rates or survival overall, there were positive trends of activity and metabolism in young‐of‐the‐year sturgeons, likely offset by negative trends of survival in early life. Notably, North American sturgeon have a greater capacity for thermal tolerance plasticity than other fishes, increasing upper thermal limits by 0.56°C per 1°C change in acclimation temperature. But with limited laboratory‐based studies, more research is needed to understand if this is a sturgeon trait, or perhaps that of basal fishes in general. Importantly, with these data gaps, the fate of sturgeon remains uncertain as climate change intensifies, and physiological impacts across life stages likely limit ecological success.
Sturgeon aquaculture has grown in recent years, driven by increasing global demand for its highly valued products. Russian sturgeon (Acipenser gueldenstaedtii), recognised as one of the most valuable species for caviar production, is farmed in several warm-temperate regions. However, the substantial temperature increase due to global warming represents a challenge for developing sturgeon aquaculture. Previously we demonstrated that Russian sturgeon under chronic heat stress (CHS) exhibited a liver metabolic reprogramming to meet energy demands, weakening their innate defences and leading to increased mortality and economic losses. Here, we used RNA-seq technology to analyse regulated genes in the spleen of Russian sturgeons exposed to CHS and challenged with Aeromonas hydrophila. The assembly gave 253,415 unigenes, with 13.7 % having at least one reliable functional annotation. We found that CHS caused mild splenitis and upregulated genes related to protein folding, heat shock response, apoptosis and autophagy while downregulated genes associated with the cell cycle. The cell cycle arrest was maintained upon A. hydrophila challenge in heat-stressed fish, potentially inducing cell senescence. Surprisingly, immunoglobulin heavy and light chains were upregulated in the spleen of stressed sturgeons but not in those maintained at tolerable temperatures; however, no changes in IgM serum levels were observed in any condition. Our findings indicate that long-term exposure to non-tolerable temperatures induced a heat shock response and activated apoptosis and autophagy processes in the spleen. These mechanisms may enable the control of tissue damage and facilitate the recycling of cell components in a condition where the nutrient supply by the liver might be insufficient. Stressed sturgeons challenged with A. hydrophila maintain these mechanisms, which could culminate in cellular senescence.
Your personalized Share Link:
https://authors.elsevier.com/c/1k6Cq,dg1asf5t
Wild ectotherms are exposed to multiple stressors, including parasites, that can affect their responses to environmental change. Simultaneously, unprecedented warm temperatures are being recorded worldwide, increasing both the average and maximum temperatures experienced in nature. Understanding how ectotherms, such as fishes, will react to the combined stress of parasites and higher average temperatures can help predict the impact of extreme events such as heat waves on populations. The critical thermal method (CTM), which assesses upper (CTmax) and lower (CTmin) thermal tolerance, is often used in acclimated ectotherms to help predict their tolerance to various temperature scenarios. Despite the widespread use of the CTM across taxa, few studies have characterized the response of naturally infected fish to extreme temperature events or how acute thermal stress affects subsequent survival. We acclimated naturally infected pumpkinseed sunfish (Lepomis gibbosus) to four ecologically relevant temperatures (10, 15, 20 and 25°C) and one future warming scenario (30°C) for 3 weeks before measuring CTmax and CTmin. We also assessed individual survival the week following CTmax. Parasites were counted and identified following trials to relate infection intensity to thermal tolerance and survival. Interestingly, trematode parasites causing black spot disease were negatively related to CTmax, suggesting that heavily infected fish are less tolerant to acute warming. Moreover, fish infected with yellow grub parasites showed decreased survival in the days following CTmax implying that the infection load has negative survival consequences on sunfish during extreme warming events. Our findings indicate that, when combined, parasite infection and high prolonged average temperatures can affect fish thermal tolerance and survival, emphasizing the need to better understand the concomitant effects of stressors on health outcomes in wild populations. This is especially true given that some parasite species are expected to thrive in warming waters making host fish species especially at risk.
Rising mean and variance in temperatures elevates threats to endangered freshwater species such as lake sturgeon, Acipenser fulvescens. Previous research demonstrated that higher temperatures during development result in physiological consequences for lake sturgeon populations throughout Manitoba, Canada, with alteration of metabolic rate, thermal tolerance, transcriptional responses, growth and mortality. We acclimated lake sturgeon (30-60 days post fertilization, a period of high mortality) from northern and southern populations (56°02'46.5″N, 96°54'18.6″W and 50°17'52″N, 95°32'51″W, respectively, separated by approximately 650 km) within Manitoba to current (summer highs of 20-23°C) and future projected (+2-3°C) environmental temperatures of 16, 20 and 24°C for 30 days, and we measured gill transcriptional responses using RNAseq. Transcripts revealed SNPs consistent with genetically distinct populations and transcriptional responses altered by acclimation temperature. There were a higher number of differentially expressed transcripts observed in the southern, compared to the northern, population as temperatures increased, indicating enhanced transcriptional plasticity. Both lake sturgeon populations responded to elevated acclimation temperatures by downregulating the transcription of genes involved in protein synthesis and energy production. Furthermore, there were population-specific thresholds for the downregulation of processes promoting transcriptional plasticity as well as mitochondrial function as the northern population showed decreases at 20°C, while this capacity was not diminished until 24°C in the southern population. These transcriptional responses highlight the molecular impacts of increasing temperatures for divergent lake sturgeon populations during vulnerable developmental periods and the critical influence of transcriptome plasticity on acclimation capacity.
Understanding the physiological mechanisms that limit animal thermal tolerance is crucial in predicting how animals will respond to increasingly severe heat waves. Despite their importance for understanding climate change impacts, these mechanisms underlying the upper thermal tolerance limits of animals are largely unknown. It has been hypothesized that the upper thermal tolerance in fish is limited by the thermal tolerance of the brain and is ultimately caused by a global brain depolarization. In this study, we developed methods for measuring the upper thermal limit (CT max ) in larval zebrafish ( Danio rerio ) with simultaneous recordings of brain activity using GCaMP6s calcium imaging in both free-swimming and agar-embedded fish. We discovered that during warming, CT max precedes, and is therefore not caused by, a global brain depolarization. Instead, the CT max coincides with a decline in spontaneous neural activity and a loss of neural response to visual stimuli. By manipulating water oxygen levels both up and down, we found that oxygen availability during heating affects locomotor-related neural activity, the neural response to visual stimuli, and CT max . Our results suggest that the mechanism limiting the upper thermal tolerance in zebrafish larvae is insufficient oxygen availability causing impaired brain function.
The capacity of fishes to cope with environmental variation is considered to be a main determinant of their fitness and is partly determined by their stress physiology. By 2100, global ocean temperature is expected to rise by 1–4°C, with potential consequences for stress physiology. Global warming is affecting animal populations worldwide through chronic temperature increases and an increase in the frequency of extreme heatwave events. As ectotherms, fishes are expected to be particularly vulnerable to global warming. Although little information is available about the effects of global warming on stress physiology in nature, multiple studies describe the consequences of temperature increases on stress physiology in controlled laboratory conditions, providing insight into what can be expected in the wild. Chronic temperature increase constitutes a physiological load that can alter the ability of fishes to cope with additional stressors, which might compromise their fitness. In addition, rapid temperature increases are known to induce acute stress responses in fishes and might be of ecological relevance in particular situations. This review summarizes knowledge about effects of temperature increases on the stress physiology of fishes and discusses these in the context of global warming.
Global warming is predicted to increase both acute and prolonged thermal challenges for aquatic ectotherms. Severe short and medium-term thermal stress over hours to days may cause mortality, while longer sub-lethal thermal challenges may cause performance declines. The interrelationship between the responses to short, medium and longer thermal challenges is unresolved. We asked if the same individuals are tolerant to both rapid and slow warming challenges, a question which has so far received little attention. Additionally, we investigated the possibility of a thermal syndrome where individuals in a population are distributed along a warm-type to cold-type axis. We tested whether different thermal traits correlate across individuals by acclimating 200 juvenile zebrafish (Danio rerio) to sub- or supra- optimal temperatures for growth (22 and 34°C) for 40 days and measured growth and thermal tolerance at two different warming rates. We found that tolerance to rapid warming correlated with tolerance to slow warming, in the 22°C treatment. However, individual tolerance to neither rapid nor slow warming correlated with growth at the supra-optimal temperature. We thus find some support for a syndrome-like organisation of thermal traits, but the lack of connection between tolerance and growth-performance indicates a restricted generality of a thermal syndrome. The results suggest that tolerance to rapid warming may share underlying physiological mechanisms with tolerance to slower heating, and indicate that the relevance of acute critical thermal tolerance extends beyond the rapid ramping rates used to measure them.
Temperature is one of the most important abiotic factors regulating development and biological processes in ectotherms.
By 2050, climate change may result in temperature increases of 2.1–3.4◦C in Manitoba, Canada. Lake sturgeon, Acipenser
fulvescens, from both northern and southern populations in Manitoba were acclimated to 16, 20 and 24◦C for 30 days, after
which critical thermal maximum (CTmax) trials were conducted to investigate their thermal plasticity. We also examined the
effects of temperature on morphological and physiological indices. Acclimation temperature significantly influenced the
CTmax, body mass, hepatosomatic index, metabolic rate and the mRNA expression of transcripts involved in the cellular
response to heat shock and hypoxia (HSP70, HSP90a, HSP90b, HIF-1α) in the gill of lake sturgeon. Population significantly
affected the above phenotypes, as well as the mRNA expression of Na+/K+ ATPase-α1 and the hepatic glutathione peroxidase
enzyme activity. The southern population had an average CTmax thatwas 0.71 and 0.45◦C higher than the northern population
at 20 and 24◦C, respectively. Immediately following CTmax trials, mRNA expression of HSP90a and HIF-1α was positively
correlatedwith individualCTmax of lake sturgeon across acclimation treatments and populations (r=0.7, r=0.62, respectively;
P<0.0001). Lake sturgeon acclimated to 20 and 24◦C had decreased hepatosomatic indices (93 and 244% reduction, respectively;
P<0.0001) and metabolic suppression (27.7 and 42.1% reduction, respectively; P<0.05) when compared to sturgeon
acclimated to 16◦C, regardless of population. Glutathione peroxidase activity and mRNA expression Na+/K+ ATPase-α1 were
elevated in the northern relative to the southern population. Acclimation to 24◦C also induced mortality in both populations
when compared to sturgeon acclimated to 16 and 20◦C. Thus, increased temperatures have wide-ranging population-specific
physiological consequences for lake sturgeon across biological levels of organization.
Exposure to high temperatures can lead to thermotolerance in fish, which is hypothesized to potentially improve post-release survival in species under restocking programs, like Atlantic sturgeon. The aim of this study was to determine whether Atlantic sturgeon juveniles exposed to a 4-week temperature treatment respond differently to a subsequent heat shock than juveniles exposed to heat shock for the first time (naive fish). Response to heat shock was assessed by mapping the liver transcriptome. In total, 838 unique contigs were differentially expressed between the trained and the control group (592 downregulated, 261 upregulated, and 15 down- or upregulated, depending on the condition), corresponding to genes involved in the response to heat, tissue damage, proteolysis, and metabolism. Temperature-trained fish showed 2–4-fold fewer dysregulated contigs than naive fish, indicating their ability to maintain and recover homeostasis faster. During heat shock, hspc1 was upregulated in both experimental groups, while hspa1 and dnaja4 were exclusively upregulated in the control. Overall, compensatory mechanisms were observed in addition to the heat shock response. Only two genes, fgg and apnl, were upregulated at nearly all timepoints in both groups. Peptidases were more strongly downregulated in control fish, which also showed a reduction in lipid metabolism during recovery. Keratins, pck1, gadd45ga, and gadd45gb were differentially expressed between trained and control fish, and due to their roles in tissue protection and ER stress reduction, they might be responsible for the maintenance of the transcriptional homeostasis observed in trained fish.
The upper thermal tolerance of brook trout Salvelinus fontinalis was estimated using critical thermal maxima (CTmax) experiments on fish acclimated to temperatures that span the species' thermal range (5–25°C). The CTmax increased with acclimation temperature but plateaued in fish acclimated to 20, 23 and 25°C. Plasma lactate was highest, and the hepato‐somatic index (IH) was lowest at 23 and 25°C, which suggests additional metabolic costs at those acclimation temperatures. The results suggest that there is a sub‐lethal threshold between 20 and 23°C, beyond which the fish experience reduced physiological performance.
Critical thermal limits (CTLs) show much variation associated with the experimental rate of temperature change used in their estimation. Understanding the full range of variation in rate effects on CTLs and their underlying basis is thus essential if methodological noise is not to overwhelm or bias the ecological signal. We consider the effects of rate variation from multiple intraspecific assessments and provide a comprehensive empirical analysis of the rate effects on both the critical thermal maximum (CTmax) and critical thermal minimum (CTmin) for 47 species of ectotherms, exploring which of the available theoretical models best explains this variation. We find substantial interspecific variation in rate effects, which takes four different forms (increase, decline, no change, mixed), with phylogenetic signal in effects on CTmax, but not CTmin. Exponential and zero exponential failure rate models best explain the rate effects on CTmax. The majority of the empirical rate variation in CTmin could not be explained by the failure rate models. Our work demonstrates that rate effects cannot be ignored in comparative analyses, and suggests that incorporation of the failure rate models into such analyses is a useful further avenue for exploration of the fundamental basis and implications of such variation.
Background:
Pacific salmon (Oncorhynchus spp.) serve as good biological indicators of the breadth of climate warming effects on fish because their anadromous life cycle exposes them to environmental challenges in both marine and freshwater environments. Our study sought to mine the extensive functional genomic studies in fishes to identify robust thermally-responsive biomarkers that could monitor molecular physiological signatures of chronic thermal stress in fish using non-lethal sampling of gill tissue.
Results:
Candidate thermal stress biomarkers for gill tissue were identified using comparisons among microarray datasets produced in the Molecular Genetics Laboratory, Pacific Biological Station, Nanaimo, BC, six external, published microarray studies on chronic and acute temperature stress in salmon, and a comparison of significant genes across published studies in multiple fishes using deep literature mining. Eighty-two microarray features related to 39 unique gene IDs were selected as candidate chronic thermal stress biomarkers. Most of these genes were identified both in the meta-analysis of salmon microarray data and in the literature mining for thermal stress markers in salmonids and other fishes. Quantitative reverse transcription PCR (qRT-PCR) assays for 32 unique genes with good efficiencies across salmon species were developed, and their activity in response to thermally challenged sockeye salmon (O. nerka) and Chinook salmon (O. tshawytscha) (cool, 13–14 °C and warm temperatures 18–19 °C) over 5–7 days was assessed. Eight genes, including two transcripts of each SERPINH1 and HSP90AA1, FKBP10, MAP3K14, SFRS2, and EEF2 showed strong and robust chronic temperature stress response consistently in the discovery analysis and both sockeye and Chinook salmon validation studies.
Conclusions:
The results of both discovery analysis and gene expression showed that a panel of genes involved in chaperoning and protein rescue, oxidative stress, and protein biosynthesis were differentially activated in gill tissue of Pacific salmon in response to elevated temperatures. While individually, some of these biomarkers may also respond to other stressors or biological processes, when expressed in concert, we argue that a biomarker panel comprised of some or all of these genes could provide a reliable means to specifically detect thermal stress in field-caught salmon.
Heat shock proteins (HSP) play important role in maintenance of cellular homeostasis. These proteins constitute around 5–10% total proteins of all normal cells and mediate the correct assembly of proteins and intracellular localization. In unstressed cells, HSP play various constitutive functions; however, when cells face stressed condition, multifold increase in the synthesis of HSP is observed. Fish is an important animal in aquatic ecosystem and the health of fish reflects the health status of its environment. Moreover, fish is a health food and fisheries and aquaculture is one of the the fastest growing food production sectors. Fishes are poikilothermic animals and confront a wide range of biotic and abiotic stressors, and like other
animals and plants, in fish also HSP play important role in combating and/or withstanding the stress. So the HSP have potential applications in monitoring and management of stress in fish. The present chapter discusses the different types of HSP that have been reported in fish and their potential applications in monitoring and
management of fish health under biotic and abiotic stress; further, the knowledge from the lower vertebrates could be useful in health and disease management in higher vertebrates including humans.
PurposeThis study evaluated whether glycogen-associated water is a protected entity not subject to normal osmotic homeostasis. An investigation into practical and theoretical aspects of the functionality of this water as a determinant of osmolality, dehydration, and glycogen concentration was undertaken. Methods
In vitro experiments were conducted to determine the intrinsic osmolality of glycogen–potassium phosphate mixtures as would be found intra-cellularly at glycogen concentrations of 2% for muscle and 5 and 10% for liver. Protected water would not be available to ionic and osmotic considerations, whereas free water would obey normal osmotic constraints. In addition, the impact of 2 L of sweat loss in situations of muscle glycogen repletion and depletion was computed to establish whether water associated with glycogen is of practical benefit (e.g., to increase “available total body water”). ResultsThe osmolality of glycogen–potassium phosphate mixtures is predictable at 2% glycogen concentration (predicted 267, measured 265.0 ± 4.7 mOsmol kg−1) indicating that glycogen-associated water is completely available to all ions and is likely part of the greater osmotic system of the body. At higher glycogen concentrations (5 and 10%), there was a small amount of glycogen water (~ 10–20%) that could be considered protected. However, the majority of the glycogen-associated water behaved to normal osmotic considerations. The theoretical exercise of selective dehydration (2 L) indicated a marginal advantage to components of total body water such as plasma volume (1.57% or 55 mL) when starting exercise glycogen replete. Conclusion
Glycogen-associated water does not appear to be a separate reservoir and is not able to uniquely replete water loss during dehydration.
Thermoregulation in ectothermic animals is influenced by the ability to effectively respond to thermal variations. While it is known that ectotherms are affected by thermal changes, it remains unknown whether physiological and/or metabolic traits are impacted by modifications to the thermal environment. Our research provides key evidence that fish ectotherms are highly influenced by thermal variability during development, which leads to important modifications at several metabolic levels (e.g., growth trajectories, microstructural alterations, muscle injuries, and molecular mechanisms). In Atlantic salmon (Salmo salar), a wide thermal range (ΔT 6.4°C) during development (posthatch larvae to juveniles) was associated with increases in key thermal performance measures for survival and growth trajectory. Other metabolic traits were also significantly influenced, such as size, muscle cellularity, and molecular growth regulators possibly affected by adaptive processes. In contrast, a restricted thermal range (ΔT 1.4°C) was detrimental to growth, survival, and cellular microstructure as muscle growth could not keep pace with increased metabolic demands. These findings provide a possible basic explanation for the effects of thermal environment during growth. In conclusion, our results highlight the key role of thermal range amplitude on survival and on interactions with major metabolism-regulating processes that have positive adaptive effects for organisms.
The qualitative composition of the Caspian Sea sturgeon has been studied on the basis of multiyear factual material. The relationship between the length, weight and age, marked a slowdown of growth the sturgeon. At present, the size of the population of Russian sturgeon and other major sturgeon species as beluga and stellate sturgeon have fallen sharply in the last 10-15 years (2000-2016), almost the recruitment absent, both, from the natural and of aquaculture. The findings suggest that the anthropogenic factor, over the past 40 years, has a negative impact on the biological productivity of fishery water bodies (Caspian Sea and adjacent rivers) and have an impact on fishes, their biological and physiological state. Evaluation of morphophysiological transformations in sturgeons based on the use of a variety of morphophysiological and biochemical parameters gives us grounds to speak about a certain deterioration of the physiological conditions of these fishes over time, in the sea and river periods of their life.
Heat shock genes are the most evolutionarily ancient among the systems responsible for adaptation of organisms to a harsh environment. The encoded proteins (heat shock proteins, Hsps) represent the most important factors of adaptation to adverse environmental conditions. They serve as molecular chaperones, providing protein folding and preventing aggregation of damaged cellular proteins. Structural analysis of the heat shock genes in individuals from both phylogenetically close and very distant taxa made it possible to reveal the basic trends of the heat shock gene organization in the context of adaptation to extreme conditions. Using different model objects and nonmodel species from natural populations, it was demonstrated that modulation of the Hsps expression during adaptation to different environmental conditions could be achieved by changing the number and structural organization of heat shock genes in the genome, as well as the structure of their promoters. It was demonstrated that thermotolerant species were usually characterized by elevated levels of Hsps under normal temperature or by the increase in the synthesis of these proteins in response to heat shock. Analysis of the heat shock genes in phylogenetically distant organisms is of great interest because, on one hand, it contributes to the understanding of the molecular mechanisms of evolution of adaptogenes and, on the other hand, sheds the light on the role of different Hsps families in the development of thermotolerance and the resistance to other stress factors.
The heat shock response (HSR) refers to the rapid production of heat shock proteins (hsps) in response to a sudden increase in temperature. Its regulation by heat shock factors is a good example of how gene expression is transcriptionally regulated by environmental stresses. In contrast, little is known about post-transcriptional regulation of the response. The heat shock response is often used to characterize the temperature tolerance of species with the rationale that whenever the response sets on, a species is approaching its lethal temperature. It has commonly been considered that an increase in hsp mRNA gives an accurate indication that the same happens to the protein level, but this need not be the case. With climate change, understanding the effects of temperature on gene expression of especially polar organisms has become imperative to evaluate how both biodiversity and commercially important species respond, since temperature increases are expected to be largest in polar areas. Here we studied the HSR of two phylogenetically related Arctic species, which differ in their temperature tolerance with Arctic charr having lower maximally tolerated temperature than Atlantic salmon. Arctic charr acclimated to 15°C and exposed to 7°C temperature increase for 30 min showed both an increase in hsp70 mRNA and hsp70 whereas in salmon only hsp70 mRNA increased. Our results indicate that the temperature for transcriptional induction of hsp can be different from the one required for a measurable change in inducible hsp level. The species with lower temperature tolerance, Arctic charr, are experiencing temperature stress already at the higher acclimation temperature, 15°C, as their hsp70 mRNA and hsp70 levels were higher, and they grow less than fish at 8°C (whereas for salmon the opposite is true). Consequently, charr experience more drastic heat shock than salmon. Although further studies are needed to establish the temperature range and length of exposure where hsp mRNA and hsp level are disconnected, the observation suggests that by measuring both hsp mRNA and hsp level, one can evaluate if a species is approaching the higher end of its temperature tolerance, and thus evaluate the vulnerability of an organism to the challenges imposed by elevated water temperature.
Global warming is widely predicted to reduce the biomass production of top predators, or even result in species loss. Several exceptions to this expectation have been identified, however, and it is vital that we understand the underlying mechanisms if we are to improve our ability to predict future trends. Here, we used a natural warming experiment in Iceland and quantitative theoretical predictions to investigate the success of brown trout as top predators across a stream temperature gradient (4-25 °C). Brown trout are at the northern limit of their geographic distribution in this system, with ambient stream temperatures below their optimum for maximal growth, and above it in the warmest streams. A five-month mark-recapture study revealed that population abundance, biomass, growth rate, and production of trout all increased with stream temperature. We identified two mechanisms that contributed to these responses: (1) trout became more selective in their diet as stream temperature increased, feeding higher in the food web and increasing in trophic position; and (2) trophic transfer through the food web was more efficient in the warmer streams. We found little evidence to support a third potential mechanism: that external subsidies would play a more important role in the diet of trout with increasing stream temperature. Resource availability was also amplified through the trophic levels with warming, as predicted by metabolic theory in nutrient-replete systems. These results highlight circumstances in which top predators can thrive in warmer environments and contribute to our knowledge of warming impacts on natural communities and ecosystem functioning.
Background:
Gene-expression analysis is increasingly important in biological research, with real-time reverse transcription PCR (RT-PCR) becoming the method of choice for high-throughput and accurate expression profiling of selected genes. Given the increased sensitivity, reproducibility and large dynamic range of this methodology, the requirements for a proper internal control gene for normalization have become increasingly stringent. Although housekeeping gene expression has been reported to vary considerably, no systematic survey has properly determined the errors related to the common practice of using only one control gene, nor presented an adequate way of working around this problem.
Results:
We outline a robust and innovative strategy to identify the most stably expressed control genes in a given set of tissues, and to determine the minimum number of genes required to calculate a reliable normalization factor. We have evaluated ten housekeeping genes from different abundance and functional classes in various human tissues, and demonstrated that the conventional use of a single gene for normalization leads to relatively large errors in a significant proportion of samples tested. The geometric mean of multiple carefully selected housekeeping genes was validated as an accurate normalization factor by analyzing publicly available microarray data.
Conclusions:
The normalization strategy presented here is a prerequisite for accurate RT-PCR expression profiling, which, among other things, opens up the possibility of studying the biological relevance of small expression differences.
Seasonal change in temperature has a profound effect on reproduction in fish. Increasing temperatures cue reproductive development in spring-spawning species, and falling temperatures stimulate reproduction in autumn-spawners. Elevated temperatures truncate spring spawning, and delay autumn spawning. Temperature increases will affect reproduction, but the nature of these effects will depend on the period and amplitude of the increase and range from phase-shifting of spawning to complete inhibition of reproduction. This latter effect will be most marked in species that are constrained in their capacity to shift geographic range. Studies from a range of taxa, habitats and temperature ranges all show inhibitory effects of elevated temperature albeit about different environmental set points. The effects are generated through the endocrine system, particularly through the inhibition of ovarian oestrogen production. Larval fishes are usually more sensitive than adults to environmental fluctuations, and might be especially vulnerable to climate change. In addition to direct effects on embryonic duration and egg survival, temperature also influences size at hatching, developmental rate, pelagic larval duration and survival. A companion effect of marine climate change is ocean acidification, which may pose a significant threat through its capacity to alter larval behaviour and impair sensory capabilities. This in turn impacts on population replenishment and connectivity patterns of marine fishes.
Trends in Canada’s climate are analyzed using recently updated data to provide a comprehensive view of climate variability and long-term changes over the period of instrumental record. Trends in surface air temperature, precipitation, snowcover, and streamflowindices are examined alongwith the potential impact of lowfrequency variability related to large-scale atmospheric and oceanic oscillations on these trends. The results
show that temperature has increased significantly inmost regions ofCanada over the period 1948–2012,with the largestwarming occurring inwinter and spring. Precipitation has also increased, especially in the north.Changes in other climate and hydroclimatic variables, including a decrease in the amount of precipitation falling as snow in the south, fewer days with snow cover, an earlier start of the spring high-flow season, and an increase inApril
streamflow, are consistent with the observed warming and precipitation trends. For the period 1900–2012, there are sufficient temperature and precipitation data for trend analysis for southern Canada (south of 608N) only. During this period, temperature has increased significantly across the region, precipitation has increased, and the amount of precipitation falling as snowhas decreased inmany areas south of 558N. The results also showthat modes of low-frequency variability modulate the spatial distribution and strength of the trends; however, they alone cannot explain the observed long-term trends in these climate variables.
How thermal tolerance estimated in the laboratory can be extrapolated to natural settings remains a contentious subject. Here, we argue that the general premise that a single temperature can accurately describe upper or lower tolerance limits is incorrect.
Survival probability is determined by both the intensity and the duration of a thermal stress, and the association between these variables can be adequately conveyed by a thermal tolerance landscape. Employing this framework, we demonstrate that the temperature range that an organism can tolerate is expected to narrow down with the duration of the thermal challenge.
Analyses suggest that a trade‐off exists between tolerances to acute and chronic exposition to thermal stress, and that changes in temperature means or extremes may result in drastically different selective pressures and subsequent evolutionary responses.
After controlling for the duration of the thermal challenge, we also uncover latitudinal effects on upper lethal temperatures in insects that remained unnoticed in previous broad‐scale comparative analyses.
Ultimately, critical thermal limits have been adopted in the ecological literature for logistic reasons and are inadequate descriptors of thermal tolerance on conceptual grounds. We consider that tolerance landscapes provide a more suitable framework to study temperature tolerance and its potential impact in ecological settings.
This study investigates the responses of white sturgeon larvae (Acipenser transmontanus) to starvation and thermal stress, through the measurement of nutritional status (i.e. growth performances) and cellular biomarkers: heat shock proteins (Hsp) 70 and 90. White sturgeon larvae (25 day post hatch; initial weight 179.0 ± 5.1 mg) were fed (20% body weight per day) or starved for 24, 48 or 72 hrs. Every 24 hrs, five larvae from each of the starved or fed treatment replicates were exposed to heat shock resulting from an increase in water temperature from 19°C to 26°C, at a rate of 1°C per 15 min, and maintained at 26°C for 4 hrs. No mortality was observed in this study. Starvation significantly (p < 0.05) decreased the body weight and body contents of energy, protein, and lipid of the experimental larvae, compared to the fed larvae. Heat shock induced the expressions of Hsp70 and Hsp90 in both the fed and starved group; however, starvation reduced the induction at all sampling points. The current study demonstrates that poor larval nutritional status, assessed by the aforementioned parameters, reduced heat shock responses to thermal stress, as measured by heat shock protein levels. Furthermore, Hsp70 and 90 are more sensitive to heat shock and starvation, respectively. This may be, in part, a result of the different functioning of the heat shock proteins in cellular stress response and warrants further study.
SYNOPSIS. This paper reviews the generalized stress response in fish at the cellular and neuroendocrine levels. The focus of this review is to examine the possible relationships between the stress responses at these two levels in fish. It focuses primarily on the heat shock protein 70 (hsp70). Thus, the descriptions of the en- docrine and the cellular stress responses are followed by a discussion of how hsps may be related to the stress hormones adrenaline and cortisol. Preliminary evi- dence shows that adrenaline causes an increase in hsp70 in primary cultures of rainbow trout hepatocytes. Cortisol does not directly affect hsp70 levels in fish tissues; however, in primary cultures of trout hepatocytes, cortisol decreased the stressor-induced increase in hsp 70. A wide range of abiotic and biological stressors have been shown to induce hsp induction in many types of fish cells, including cell lines, primary cell cultures, and in tissues from whole animals. Heat shock proteins has been implicated in the protection of sulphate transport in the renal epithelium of the flounder against the damaging effects of heat stress. Heat shock proteins likely confer thermotolerance in fish, as well as tolerance to cytotoxic effects of environmental contaminants and other non-thermal stressors.
We use elasticity analyses for three sturgeon species, the shortnose sturgeon Acipenser brevirostrum, Atlantic sturgeon A. oxyrinchus, and white sturgeon A. transmontanus, to calculate the potential to increase population growth rate, l, by improving survival and fecundity. Elasticity analysis is a means of assessing changes to l resulting from conserva- tion initiatives. The elasticity of l to survival has a characteristic profile that includes a pla- teau of high elasticity values across the young of the year and the juvenile ages. However, survival elasticity falls at maturity and declines rapidly with increasing adult age. Changes to fecundity have relatively little impact; the total of the fecundity elasticities over all ages is equal to the single young-of-the-year survival elasticity. Even though the young-of-the-year survival elasticity is equal to that of any other juvenile age, the overall opportunity for af- fecting l is strongest in the young-of-the-year age-class because of its exceptional potential for increase to survival. The juvenile and adult stages have roughly equal total survival elas- ticities. These findings are particularly relevant in understanding the contributions of hatch- eries, harvest regulations and habitat restoration as strategies for sturgeon conservation. Hatcheries are focused on the young of the year, the demographically most sensitive compo- nent of sturgeon life histories, and thus have the potential to make significant increases to l if the genetic, evolutionary and ecological impacts of hatcheries can be controlled. Harvest, even at low levels, can have a significant negative impact on l when it affects multiple age classes. Managers can use elasticity analysis to calculate the total impact of harvest and to mathematically evaluate the trade-off in exploiting young versus older individuals. Habitat restoration strategies, usually assessed in terms of survivals of the age classes impacted, would also benefit from using elasticity analysis to interpret their contributions to l. If resto- ration efforts target the survival of age classes with high elasticities, significant population growth may be achieved.
Understanding the resilience of ectotherms to high temperatures is essential because of the influence of climate change on aquatic ecosystems. The ability of species to acclimate to high temperatures may determine whether populations can persist in their native ranges. We examined physiological and molecular responses of juvenile brook trout (Salvelinus fontinalis) to six acclimation temperatures (5, 10, 15, 20, 23 and 25°C) that span the thermal distribution of the species to predict acclimation limits. Brook trout exhibited an upregulation of stress-related mRNA transcripts (heat shock protein 90-beta, heat shock cognate 71 kDa protein, glutathione peroxidase 1) and downregulation of transcription factors and osmoregulation-related transcripts (nuclear protein 1, Na+/K+/2Cl− co-transporter-1-a) at temperatures ≥20°C. We then examined the effects of acclimation temperature on metabolic rate (MR) and physiological parameters in fish exposed to an acute exhaustive exercise and air exposure stress. Fish acclimated to temperatures ≥20°C exhibited elevated plasma cortisol and glucose, and muscle lactate after exposure to the acute stress. Fish exhibited longer MR recovery times at 15 and 20°C compared with the 5 and 10°C groups; however, cortisol levels remained elevated at temperatures ≥20°C after 24 h. Oxygen consumption in fish acclimated to 23°C recovered quickest after exposure to acute stress. Standard MR was highest and factorial aerobic scope was lowest for fish held at temperatures ≥20°C. Our findings demonstrate how molecular and physiological responses predict acclimation limits in a freshwater fish as the brook trout in the present study had a limited ability to acclimate to temperatures beyond 20°C.
Increasing heart rate (ƒH) is a central, if not primary mechanism used by fishes to support their elevated tissue oxygen consumption during acute warming. Thermal acclimation can adjust this acute response to improve cardiac performance and heat tolerance under the prevailing temperatures. We predict that such acclimation will be particularly important in regions undergoing rapid environmental change such as the Arctic. Therefore, we acclimated Arctic char (Salvelinus alpinus), a high latitude, cold-adapted salmonid, to ecologically relevant temperatures (2, 6, 10, 14 and 18 °C) and examined how thermal acclimation influenced their cardiac heat tolerance by measuring the maximum heart rate (ƒHmax) response to acute warming. As expected, acute warming increased ƒHmax in all Arctic char before ƒHmax reached a peak and then became arrhythmic. The peak ƒHmax, and the temperature at which peak ƒHmax (Tpeak) and that at which arrhythmia first occurred (Tarr) all increased progressively (+33%, 49% and 35%, respectively) with acclimation temperature from 2 to 14 °C. When compared at the same test temperature ƒHmax also decreased by as much as 29% with increasing acclimation temperature, indicating significant thermal compensation. The upper temperature at which fish first lost their equilibrium (critical thermal maximum: CTmax) also increased with acclimation temperature, albeit to a lesser extent (+11%). Importantly, Arctic char experienced mortality after several weeks of acclimation at 18 °C and survivors did not have elevated cardiac thermal tolerance. Collectively, these findings suggest that if wild Arctic char have access to suitable temperatures (<18 °C) for a sufficient duration, warm acclimation can potentially mitigate some of the cardiorespiratory impairments previously documented during acute heat exposure.
Marine ectotherms are often sensitive to thermal stress, and certain life stages can be particularly vulnerable (e.g., larvae or spawners). In this study, we investigated the critical thermal maxima (CTmax) of larval and early juvenile life stages of three tropical marine fishes (Acanthochromis polyacanthus, Amphiprion melanopus, and Lates calcarifer). We tested for potential effects of developmental acclimation, life stage, and experimental heating rates, and we measured metabolic enzyme activities from aerobic (citrate synthase, CS) and anaerobic pathways (lactate dehydrogenase, LDH). A slightly elevated rearing temperature neither influenced CTmax nor CS activity, which otherwise could have indicated thermal acclimation. However, we found CTmax to either remain stable (Acanthrochromis polyacanthus) or increase with body mass during early ontogeny (Amphiprion melanopus and Lates calcarifer). In all three species, faster heating rates lead to higher CTmax. Acute temperature stress did not change CS or LDH activities, suggesting that overall aerobic and anaerobic metabolism remained stable. Lates calcarifer, a catadromous species that migrates from oceanic to riverine habitats upon metamorphosis, had higher CTmax than the two coral reef fish species. We highlight that, for obtaining conservative estimates of a fish species’ upper thermal limits, several developmental stages and body mass ranges should be examined. Moreover, upper thermal limits should be assessed using standardized heating rates. This will not only benefit comparative approaches but also aid in assessing geographic (re-) distributions and climate change sensitivity of marine fishes.
The cellular stress response (CSR) is critical for enabling organisms to cope with thermal damage to proteins, nucleic acids, and membranes. It is a graded response whose properties vary with the degree of cellular damage. Molecular damage has positive, as well as negative, function-perturbing effects. Positive effects include crucial regulatory interactions that orchestrate involvement of the different components of the CSR. Thermally unfolded proteins signal for rapid initiation of transcription of genes encoding heat shock proteins (HSPs), central elements of the heat shock response (HSR). Thermal disruption of messenger RNA (mRNA) secondary structures in untranslated regions leads to the culling of the mRNA pool: thermally labile mRNAs for housekeeping proteins are degraded by exonucleases; heat-resistant mRNAs for stress proteins like HSPs then can monopolize the translational apparatus. Thus, proteins and RNA function as "cellular thermometers," and evolved differences in their thermal stabilities enable rapid initiation of the CSR whenever cell temperature rises significantly above the normal thermal range of a species. Covalent DNA damage, which may result from increased production of reactive oxygen species, is temperature-dependent; its extent may determine cellular survival. High levels of stress that exceed capacities for molecular repair can lead to proteolysis, inhibition of cell division, and programmed cell death (apoptosis). Onset of these processes may occur later in the stress period, after initiation of the HSR, to allow HSPs opportunity to restore protein homeostasis. Delay of these energy costly processes may also result from shortfalls in availability of adenosine triphosphate and reducing power during times of peak stress.
Virtually all organisms respond to heat shock by transcription of genes encoding for heat shock proteins (HSPs), but the mechanisms behind post-transcriptional regulation are not known in detail. When we exposed zebrafish to 5 and 7 °C above normal rearing temperature for 30 min, hsp70 mRNA expression was 28 and 150 -fold higher than in control, respectively. Protein expression, on the other hand, showed no significant change at the +5 °C and a 2-fold increase at the +7 °C exposure. This suggests that the transcription of hsp70 gene does not immediately correspond to translation to related proteins under certain stress temperatures, but, when the temperature is higher, and potentially detrimental, transcription and translation are intimately coupled. Those results confirm that temperature is an important abiotic factor involved in heat shock post-transcriptional regulation mechanisms in fish. However, further studies are needed to determine the relationship between this environmental factor and post-transcriptional regulation mechanisms. Earlier, the coupling/uncoupling of hsp transcription and translation has only been studied using cold-water fish, or zebrafish embryos. With current findings, we suggest this mechanism might be present even in adult warm water fish like the zebrafish.
The structural features of the fish gill necessary for oxygen uptake also favor undesirable, passive movements of ions and water. Reversible gill remodeling is one solution to this conflict. Cell masses that limit functional surface area are lost when oxygen availability decreases in hypoxia or oxygen demand increases with exercise or high temperature. However, much remains to be learned about how widespread reversible gill remodeling is among fish species, and how and why it occurs.
Heat‐shock proteins (Hsps) and their cognates are primary mitigators of cell stress. With increasingly severe impacts of climate change and other human modifications of the biosphere, the ability of the heat‐shock system to affect evolutionary fitness in environments outside the laboratory and to evolve in response are topics of growing importance. Since the last major reviews, several advances have occurred. First, demonstrations of the heat‐shock response outside the laboratory now include many additional taxa and environments. Many of these demonstrations are only correlative, however. More importantly, technical advances in “omic” quantification of nucleic acids and proteins, genome‐wide association analysis, and manipulation of genes and their expression have enabled the field to move beyond correlation. Several consequent advances are already evident: The pathway from heat‐shock gene expression to stress tolerance in nature can be extremely complex, mediated through multiple biological processes and systems, and even multiple species. The underlying genes are more numerous, diverse, and variable than previously appreciated, especially with respect to their regulatory variation and epigenetic changes. The impacts and limitations (e.g., due to trade‐offs) of natural selection on these genes have become more obvious and better established. Finally, as evolutionary capacitors Hsps may have distinctive impacts on the evolution of other genes and ecological consequences.
This article is protected by copyright. All rights reserved.
Cardiac mitochondrial metabolism provides 90% of the ATP necessary for the contractile exertion of the heart muscle. Mitochondria are therefore assumed to play a pivotal role in heart failure (HF), cardiovascular disease and ageing. Heat stress increases energy metabolism and oxygen demand in tissues throughout the body and imposes a major challenge on the heart, which is suspected of being the first organ to fail during heat stress. The underlying mechanisms inducing heart failure are still unclear. To pinpoint the processes implicated in HF during heat stress, we measured mitochondrial respiration rates and hydrogen peroxide production of isolated Arctic char (Salvelinus alpinus) heart mitochondria at 4 temperatures: 10°C(acclimation), 15°C, 20°C and 25°C (just over critical maximum). We found that at temperature ranges causing the loss of an organism's general homeostasis (between 20°C and 25°C) and with a substrate combination close to physiological conditions, the heat-induced increase in mitochondrial oxygen consumption levels off. More importantly, at the same state, hydrogen peroxide efflux increased by almost 50%. In addition, we found that individuals with low mitochondrial respiration rates produced more hydrogen peroxide at 10°C, 15°C and 20°C. This could indicate that individuals with cardiac mitochondria having a low respiratory capacity, have a more fragile heart and will be more prone to oxidative stress and HF, and less tolerant to temperature changes and other stressors. Our results show that, at temperatures close to the thermal limit, mitochondrial capacity is compromised and ROS production rates increase. This could potentially alter the performance of the cardiac muscle and lead to heat-induced HF underlining the important role that mitochondria play in setting thermal tolerance limits.
The present study aimed to investigate in Hoplosternum littorale (Hancock, 1828) the effects of different water temperatures (10 °C, 25 °C-control group-and 33 °C) on physiologic and metabolic traits following acute (1 day) and chronic (21 days) exposures. We analyzed several biomarker responses in order to achieve a comprehensive survey of fish physiology and metabolism under the effect of this natural stressor. We measured morphological indices, biochemical and hematological parameters as well as oxidative stress markers. To evaluate energy consumption, muscle and hepatic total lipid, protein and glycogen concentrations were also quantified. Extreme temperatures exposures clearly resulted in metabolic adjustments, being liver energy reserves and plasma metabolites the most sensitive parameters detecting those changes. We observed reduced hepatosomatic index after acute and chronic exposure to 33 °C while glycogen levels decreased at both temperatures and time of exposure tested. Additionally, acute and chronic exposures to 10 °C increased liver lipid content and plasma triglycerides. Total protein concentration was higher in liver and lower in plasma after chronic exposures to 10 °C and 33 °C. Acute exposition at both temperatures caused significant changes in antioxidant enzymes tested in the different tissues without oxidative damage to lipids. Antioxidant defenses in fish failed to protect them when they were exposed for 21 days to 10 °C, promoting higher lipid peroxidation in liver, kidney and gills. According to multivariate analysis, oxidative stress and metabolic biomarkers clearly differentiated fish exposed chronically to 10 °C. Taken together, these results demonstrated that cold exposure was more stressful for H. littorale than heat stress. However, this species could cope with variations in temperature, allowing physiological processes and biochemical reactions to proceed efficiently at different temperatures and times of exposure. Our study showed the ability of H. littorale to resist a wide range of environmental temperatures and contributes for the understanding of how this species is adapted to environments with highly variable physicochemical conditions.
This new edition to the classic book by ggplot2 creator Hadley Wickham highlights compatibility with knitr and RStudio. ggplot2 is a data visualization package for R that helps users create data graphics, including those that are multi-layered, with ease. With ggplot2, it's easy to:
• produce handsome, publication-quality plots with automatic legends created from the plot specification
• superimpose multiple layers (points, lines, maps, tiles, box plots) from different data sources with automatically adjusted common scales
• add customizable smoothers that use powerful modeling capabilities of R, such as loess, linear models, generalized additive models, and robust regression
• save any ggplot2 plot (or part thereof) for later modification or reuse
• create custom themes that capture in-house or journal style requirements and that can easily be applied to multiple plots
• approach a graph from a visual perspective, thinking about how each component of the data is represented on the final plot
This book will be useful to everyone who has struggled with displaying data in an informative and attractive way. Some basic knowledge of R is necessary (e.g., importing data into R). ggplot2 is a mini-language specifically tailored for producing graphics, and you'll learn everything you need in the book. After reading this book you'll be able to produce graphics customized precisely for your problems, and you'll find it easy to get graphics out of your head and on to the screen or page. New to this edition:<
• Brings the book up-to-date with ggplot2 1.0, including major updates to the theme system
• New scales, stats and geoms added throughout
• Additional practice exercises
• A revised introduction that focuses on ggplot() instead of qplot()
• Updated chapters on data and modeling using tidyr, dplyr and broom
White Sturgeon, Acipenser transmontanus (WS), are distributed throughout three major river basins on the West Coast of North America: the Sacramento-San Joaquin, Columbia, and Fraser River drainages. Considered the largest North American freshwater fish, some WS use estuarine habitat and make limited marine movements between river basins. Some populations are listed by the United States or Canada as threatened or endangered (upper Columbia River above Grand Coulee Dam; Kootenai River; lower, middle and, upper Fraser River and Nechako River), while others do not warrant federal listing at this time (Sacramento-San Joaquin Rivers; Columbia River below Grand Coulee Dam; Snake River). Threats that impact WS throughout the species’ range include fishing effects and habitat alteration and degradation. Several populations suffer from recruitment limitations or collapse due to high early life mortality associated with these threats. Efforts to preserve WS populations include annual monitoring, harvest restrictions, habitat restoration, and conservation aquaculture. This paper provides a review of current knowledge on WS life history, ecology, physiology, behavior, and genetics and presents the status of WS in each drainage. Ongoing management and conservation efforts and additional research needs are identified to address present and future risks to the species.
Previous studies have demonstrated differences in thermotolerance between two wing morphs of Nilaparvata lugens, the most serious pest of rice across the Asia. To reveal the molecular regulatory mechanisms underlying the differential thermal resistance abilities between two wing morphs, a full-length of transcript encoding heat shock cognate protein 70 (Hsc70) was cloned, and its expression patterns across temperature gradients were analyzed. The results showed that the expression levels of NlHsc70 in macropters increased dramatically after heat shock from 32 to 38 °C, while NlHsc70 transcripts in brachypters remained constant under different temperature stress conditions. In addition, NlHsc70 expression in the macropters was significantly higher than that in brachypters at 1 and 2 h recovery from 40 °C heat shock. There was no significant difference in NlHsc70 mRNA expression between brachypters and macropters under cold shock conditions. Therefore, NlHsc70 was indeed a constitutively expressed member of the Hsp70 family in brachypters of N. lugens, while it was heat-inducible in macropters. Furthermore, the survival rates of both morphs injected with NlHsc70 dsRNA were significantly decreased following heat shock at 40 °C or cold shock at 0 °C for 1 h. These results suggested that the up-regulation of NlHsc70 is possibly related to the thermal resistance, and the more effective inducement expression of NlHsc70 in macropters promotes a greater thermal tolerance under temperature stress conditions.
We evaluated temperature tolerance in age-0 pallid and shovelnose sturgeon (Scaphirhynchus albus and Scaphirhynchus platorynchus), two species that occur sympatrically in the Missouri and Mississippi Rivers. Fish (0.04-18g) were acclimated to water temperatures of 13, 18 or 24°C to quantify temperatures associated with lethal thermal maxima (LTM). The results show that no difference in thermal tolerance existed between the two sturgeon species, but that LTM was significantly related to body mass and acclimation temperature. Multiple linear regression analysis was used to estimate LTM, and outputs from the model were compared with water temperatures measured in the shallow water habitat (SWH) of the Missouri River. Observed SWH temperatures were not found to yield LTM conditions. The model developed here is to serve as a general guideline in the development of future SWH.
Adverse effects associated with exposure to dioxin-like compounds (DLCs) are mediated primarily through activation of the aryl hydrocarbon receptor (AHR). However, little is known about the cascades of events that link activation of the AHR to apical adverse effects. Therefore, this study used high-throughput, next-generation molecular tools to investigate similarities and differences in whole transcriptome and whole proteome responses to equipotent concentrations of three agonists of the AHR, 2,3,7,8-TCDD, PCB 77, and benzo[a]pyrene, in livers of a non-model fish, the white sturgeon (Acipenser transmontanus). A total of 926 and 658 unique transcripts were up- and down-regulated, respectively, by one or more of the three chemicals. Of the transcripts shared by responses to all three chemicals, 85% of up-regulated transcripts and 75% of down-regulated transcripts had the same magnitude of response. A total of 290 and 110 unique proteins were up- and down-regulated, respectively, by one or more of the three chemicals. Of the proteins shared by responses to all three chemicals, 70% of up-regulated proteins and 48% of down-regulated proteins had the same magnitude of response. Among treatments there was 68% similarity between the global transcriptome and global proteome. Pathway analysis revealed that perturbed physiological processes were indistinguishable between equipotent concentrations of the three chemicals. The results of this study contribute towards more completely describing adverse outcome pathways associated with activation of the AHR.
We documented 17 white sturgeon Acipenser transmontanus spawning locations in the Snake River from the mouth to Lower Granite Dam (river lan 0 to 173). Spawning locations were determined by the collection of fertilized eggs on artificial substrates or in plankton nets. We collected 245 eggs at seven locations in McNary Reservoir, 22 eggs at three locations in Ice Harbor Reservoir, 30 eggs from two locations in Lower Monumental Reservoir, and 464 eggs at five locations in Little Goose Reservoir. All 17 locations were in high water velocity areas and between 1.0 and 7.0 lan downstream from a hydroelectric dam. The documentation of spawning areas is important because this habitat is necessary to maintain natural and viable populations.
The cytosolic 70KDa heat shock proteins (Hsp70s) are widely used as biomarkers of environmental stress in ecological and toxicological studies in fish. Here we analyze teleost genome sequences to show that two genes encoding inducible hsp70s (hsp70–1 and hsp70–2) are likely present in all teleost fish. Phylogenetic and synteny analyses indicate that hsp70–1 and hsp70–2 are distinct paralogs that originated prior to the diversification of the teleosts. The promoters of both genes contain a TATA box and conserved heat shock elements (HSEs), but unlike mammalian HSP70s, both genes contain an intron in the 5′ UTR. The hsp70–2 gene has undergone tandem duplication in several species. In addition, many other teleost genome assemblies have multiple copies of hsp70–2 present on separate, small, genomic scaffolds. To verify that these represent poorly assembled tandem duplicates, we cloned the genomic region surrounding hsp70–2 in Fundulus heteroclitus and showed that the hsp70–2 gene copies that are on separate scaffolds in the genome assembly are arranged as tandem duplicates. Real time quantitative PCR of F. heteroclitus genomic DNA indicates that four copies of the hsp70–2 gene are likely present in the F. heteroclitus genome. Comparison of expression patterns in F. heteroclitus and Gasterosteus aculeatus demonstrates that hsp70–2 has a higher fold increase than hsp70–1 following heat shock in gill but not muscle tissue, revealing a conserved difference in expression patterns between isoforms and tissues. These data indicate that ecological and toxicological studies using hsp70 as a biomarker in teleosts should take this complexity into account.
Measures of thermal tolerance quantify the subset of temperatures under which a species can maximize fitness defining a major component of a fish's abiotic niche. Thermal tolerance and a fish's physiological capacity for temperature have applications in both theoretical and applied biology. Although the theoretical discussions of thermal tolerance in evolutionary contexts of biogeography, macroecology, and biological laws will be introduced, the foci of this article are the different measures of thermal tolerance and how they may be used in applied thermal biology. Given predicted changes in temperature due to global climate change, knowledge concerning the thermal limits of all organisms and how to access these limits are keenly important. Of the various methods used to estimate thermal tolerances in fishes, the lower or upper incipient lethal temperature method (static temperature) and critical thermal minimum or maximum method (dynamic temperature) are the two most widely used and accepted. Fishes have lower and upper lethal temperatures that range from less than 0. °C to more than 45. °C. Temperature tolerances are strongly influenced by a suite of abiotic and biotic factors that include (but are not limited to) acclimation temperature, photoperiod, seasonality, environmental stressors, genetics, reproductive status, and ontogeny.
Because of its profound effects on the rates of biological processes such as aerobic metabolism, environmental temperature plays an important role in shaping the distribution and abundance of species. As temperature increases, the rate of metabolism increases and then rapidly declines at higher temperatures - a response that can be described using a thermal performance curve (TPC). Although the shape of the TPC for aerobic metabolism is often attributed to the competing effects of thermodynamics, which can be described using the Arrhenius equation, and the effects of temperature on protein stability, this account represents an over-simplification of the factors acting even at the level of single proteins. In addition, it cannot adequately account for the effects of temperature on complex multistep processes, such as aerobic metabolism, that rely on mechanisms acting across multiple levels of biological organization. The purpose of this review is to explore our current understanding of the factors that shape the TPC for aerobic metabolism in response to acute changes in temperature, and to highlight areas where this understanding is weak or insufficient. Developing a more strongly grounded mechanistic model to account for the shape of the TPC for aerobic metabolism is crucial because these TPCs are the foundation of several recent attempts to predict the responses of species to climate change, including the metabolic theory of ecology and the hypothesis of oxygen and capacity-limited thermal tolerance.
© 2015. Published by The Company of Biologists Ltd.
Although Hsp70, the principal inducible heat-shock protein of Drosophila melanogaster, has received intense scrutiny in laboratory strains, its variation within natural populations and the consequences of such variation for thermotolerance are unknown. We have characterized variation in first-instar larvae of 20 isofemale lines isolated from a single natural population of D. melanogaster, in which larvae are prone to thermal stress in nature. Hsp70 expression varied more than twofold among lines after induction by exposure to 36⚬C for one hour, with an estimated proportion of the variation due to genetic differences of 0.24 ± 0.08. Thermotolerance with and without a Hsp70-inducing pretreatment, survival at 25⚬C, and developmental time also varied significantly. As expected, expression of Hsp70 correlated positively with larval thermotolerance. By contrast, lines in which larval survival was high in the absence of heat stress showed lower than average Hsp70 expression and lower than average inducible thermotolerance. This conditional performance suggests an evolutionary trade-off between thermotolerance and the ability to produce higher concentrations of Hsp70, and survival in a benign environment.
Hochachka P.W., Somero G.N. (2002) Biochemical adaptation: mechanism and process in physiological evolution. New York: Oxford University Press. 466 p.
White sturgeon yolk sac larvae (YSL) were reared at 13.5 and 17.5 °C with and without gravel substrate. Larvae reared within the gravel emerged from the substrate after 11–14 days (depending on temperature), and all larvae were subsequently fed in bare tanks until 46 days post hatch (dph). Temperature and substrate significantly affected size; at 46 dph, fish reared in gravel at 17.5 °C were the largest (288 ± 19 mg), while fish reared at 13.5 °C without gravel were the smallest (107 ± 3 mg). Yolk absorption rate did not differ between substrate treatments but was greater at 17.5 °C than at 13.5 °C. In contrast, yolk absorption efficiency was independent of temperature but was significantly greater in gravel-reared larvae. YSL reared in gravel also had more lipid vacuoles in their liver. Substrate and temperature significantly affected survival. Greatest survival (84.6% ± 0.6%) was achieved when YSL were reared in gravel at 13.5 °C, and survival was lowest (46.6% ± 0.6%) when larvae were reared without gravel at 17.5 °C. Understanding factors that affect growth and survival during early life history provides insight into factors affecting wild recruitment and should improve hatchery production.
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.