Thermal Tolerance Response Research Articles

Baseline dynamics of Symbiodiniaceae genera and photochemical efficiency in corals from reefs with different thermal histories.

Ocean warming and marine heatwaves induced by climate change are impacting coral reefs globally, leading to coral bleaching and mortality. Yet, coral resistance and resilience to warming are not uniform across reef sites and corals can show inter- and intraspecific variability. To understand changes in coral health and to elucidate mechanisms of coral thermal tolerance, baseline data on the dynamics of coral holobiont performance under non-stressed conditions are needed. We monitored the seasonal dynamics of algal symbionts (family Symbiodiniaceae) hosted by corals from a chronically warmed and thermally variable reef compared to a thermally stable reef in southern Taiwan over 15 months. We assessed the genera and photochemical efficiency of Symbiodiniaceae in three coral species: Acropora nana, Pocillopora acuta, and Porites lutea. Both Durusdinium and Cladocopium were present in all coral species at both reef sites across all seasons, but general trends in their detection (based on qPCR cycle) varied between sites and among species. Photochemical efficiency (i.e., maximum quantum yield; Fv/Fm) was relatively similar between reef sites but differed consistently among species; no clear evidence of seasonal trends in Fv/Fm was found. Quantifying natural Symbiodiniaceae dynamics can help facilitate a more comprehensive interpretation of thermal tolerance response as well as plasticity potential of the coral holobiont.

Thermal tolerance responses of the two-spotted stink bug, Bathycoelia distincta (Hemiptera: Pentatomidae), vary with life stage and the sex of adults

Temperature tolerance is an essential component of insect fitness, and its understanding can provide a predictive framework for their distribution and abundance. The two-spotted stink bug, Bathycoelia distincta Distant, is a significant pest of macadamia. The main goal of this study was to investigate the thermal tolerance of B. distincta across different life stages. Thermal tolerance indices investigated included critical thermal maximum (CTmax), critical thermal minimum (CTmin), effects of acclimation on CTmax and CTmin at 20, 25, and 30 °C, and rapid heat hardening (RHH), and rapid cold hardening (RCH). The Kruskal-Wallis test was used to explore the effects of life stage and acclimation on CTmax and CTmin and Generalized Linear Models (GLM) for the probability of survival after pre-exposure to RHH at 41 °C for 2 h and RCH at −8 °C for 2 h. CTmax and CTmin varied significantly between life stages at all acclimation temperatures, but CTmin (3.5 °C) varied more than CTmax (2.1 °C). Higher acclimation temperatures resulted in larger variations between life stages for both CTmax and CTmin. A significant acclimation response was observed for the CTmax of instar 2 (1.7 °C) and CTmin of females (2.7 °C) across acclimation temperatures (20–30 °C). Pre-exposure significantly improved the heat and cold survival probability of instar 2 and the cold survival probability of instar 3 and males. The response between life stages was more variable in RCH than in RHH. Instar 2 appeared to be the most thermally plastic life stage of B. distincta. These results suggest that the thermal plastic traits of B. distincta life stages may enable this pest to survive in temperature regimes under the ongoing climate change, with early life stages (except for instar 2) more temperature sensitive than later life stages.

Comparative transcriptome analyses reveal the dynamic responses of avian myotubes to acute heat stress

The detrimental effects of acute heat stress (AHS) on poultry production have been widely reported. Unraveling the physiological and metabolic responses to AHS could help to provide theoretical basis for developing strategies to mitigate hyperthermia-induced muscle damage. Here, we investigated the effects of different durations of AHS (45 °C for 0.5, 1, 2 and 4 h) on differentiated avian myotubes. Results indicated that AHS destroyed the morphology of differentiated myotubes, and the degree of damage increased with the prolongation of AHS. Dynamic transcriptomic profiling identified 67, 467, 1355 and 2627 differentially expressed genes (DEGs) after 0.5, 1, 2, and 4 h of heat stress, respectively. Only 50 DEGs were regulated across all time points. In addition, genes involved in cell cycle, metabolic process and immune response were upregulated upon short-term heat stress (0.5 and 1 h). However, these thermal-tolerance responses were suppressed upon prolonged heat stress (2 and 4 h). Furthermore, the quick response of molecular chaperone genes might be major targets for acclimation to hyperthermia. Overall, the current transcriptome analyses reveal the dynamic changes of avian myotubes to AHS and promote an understanding of the molecular mechanisms involved in the heat stress response in poultry.

Variation in thermal tolerance response associated with geographic location during early development of the neogastropod Ocenebra erinaceus (Linnaeus, 1758)

Environmental temperature plays an important role in shaping the distribution and abundance of marine ectothermic organisms. As a general rule, larvae and juveniles are more sensitive to thermal stress than adults and, as a consequence, represent key life stages that determine in part the geographic range of a species. Identifying critical thermal limits during ontogeny allows for the prediction of the potential impacts of climate warming on the distribution of marine ectotherms. However, thermal tolerance - and therefore the potential to meet the challenge of warming- is known to vary at population scale for many species. In order to fully appreciate a species' future under climate warming, multiple populations studies from different thermal environments are necessary. In this study, we compared the thermal tolerance response during the intracapsular development of the marine gastropod Ocenebra erinaceus between two geographically separated populations: one from the middle (Solent, UK) and another from the south of the species' geographic range (Arcachon, France). The results show that the thermal tolerance response was influenced by geographic origin. Embryos from the relatively warm-water southern population (France) show a warm-eurythermal tolerance window with optimal temperatures between 12 and 18 °C. On the contrary, embryos from the cold-water northern population (UK) exhibit a narrow, warm-stenothermal, thermal tolerance window with optimal temperatures between 14 and 16 °C. In both populations, temperatures outside of the thermal range cause lethal and sub-lethal effects. Importantly, previously observed dispersal polymorphism was not observed at hatching time in either population in our study. Our study demonstrates that during early developmental stages, embryos are adapted to local thermal conditions and that they live very close to their upper thermal limits. Temperatures outside this range cause detrimental and contrasting effects on embryonic development of O. erinaceus, implying that the effects of future warming will depend on the population response to local environmental history. Our results suggest that global warming could shift the geographical distribution range of O. erinaceus poleward.

Rearing temperature conditions (constant vs. thermocycle) affect daily rhythms of thermal tolerance and sensing in zebrafish.

In the wild, the environment does not remain constant, but periodically oscillates so that temperature rises in the daytime and drops at night, which generates a daily thermocycle. The effects of thermocycles on thermal tolerance have been previously described in fish. However, the impact of thermocycles on daytime-dependent thermal responses and daily rhythms of temperature tolerance and sensing expression mechanisms remain poorly understood. This study investigates the effects of two rearing conditions: constant (26°C, C) versus a daily thermocycle (28°C in the daytime; 24°C at night, T) on the thermal tolerance response in zebrafish. Thermal tolerance (mortality) was assessed in 4dpf (days post fertilization) zebrafish larvae after acute heat shock (39°C for 1h) at two time points: middle of the light phase (ML) or middle of the dark phase (MD). Thermal stress responses were evaluated in adult zebrafish after a 37°C challenge for 1hat ML or MD to examine the expression of the heat-shock protein (HSP) (hsp70, hsp90ab1, grp94, hsp90aa1, hspb1, hsp47, cirbp) and transient receptor potential (TRP) channels (trpv4, trpm4a, trpm2, trpa1b) in the brain. Finally, the daily rhythms of gene expression of HSPs and TRPs were measured every 4h for 24h. The results revealed the larval mortality rates and the expression induction of most HSPs in adult zebrafish brain reached the highest values in fish reared under constant temperature and subjected to thermal shock at MD. The expression of most HSPs and TRPs was mainly synchronized to the light/dark (LD) cycle, regardless of the temperature regime. Most HSPs involved in hyperthermic challenges displayed diurnal rhythms with their acrophases in phase with warm-sensing thermoTRPs acrophases. The cold-sensing trpa1b peaked in the second half of the light period and slightly shifted toward the dark phase anticipating the acrophase of cirpb, which is involved in hypothermic challenges. These findings indicated that: a) thermal shocks are best tolerated in the daytime; b) the implementation of daily thermocycles during larval development reduces mortality and stress-cellular expression of HSPs to an acute thermal stress at MD; c) daily rhythms need to be considered when discussing physiological responses of thermal sensing and thermotolerance in zebrafish.

Thermal tolerance and routine oxygen consumption of convict cichlid, Archocentrus nigrofasciatus, acclimated to constant temperatures (20°C and 30°C) and a daily temperature cycle (20°C → 30°C).

Organismal temperature tolerance and metabolic responses are correlated to recent thermal history, but responses to thermal variability are less frequently assessed. There is great interest in whether organisms that experience greater thermal variability can gain metabolic or tolerance advantages through phenotypic plasticity. We compared thermal tolerance and routine aerobic metabolism of Convict cichlid acclimated for 2weeks to constant 20°C, constant 30°C, or a daily cycle of 20 → 30°C (1.7°C/h). Acute routine mass-specific oxygen consumption ([Formula: see text]O2) and critical thermal maxima/minima (CTMax/CTMin) were compared between groups, with cycle-acclimated fish sampled from the daily minimum (20°C, 0900h) and maximum (30°C, 1600h). Cycle-acclimated fish demonstrated statistically similar CTMax at the daily minimum and maximum (39.0°C, 38.6°C) but distinct CTMin values, with CTMin 2.4°C higher for fish sampled from the daily 30°C maximum (14.8°C) compared to the daily 20°C minimum (12.4°C). Measured acutely at 30°C, [Formula: see text]O2 decreased with increasing acclimation temperature; 20°C acclimated fish had an 85% higher average [Formula: see text]O2 than 30°C acclimated fish. Similarly, acute [Formula: see text]O2 at 20°C was 139% higher in 20°C acclimated fish compared to 30°C acclimated fish. Chronic [Formula: see text]O2 was measured in separate fish continually across the 20 → 30°C daily cycle for all 3 acclimation groups. Chronic [Formula: see text]O2 responses were very similar between groups between average individual hourly values, as temperatures increased or decreased (1.7°C/h). Acute [Formula: see text]O2 and thermal tolerance responses highlight "classic" trends, but dynamic, chronic trials suggest acclimation history has little effect on the relative change in oxygen consumption during a thermal cycle. Our results strongly suggest that the minimum and maximum temperatures experienced more strongly influence fish physiology, rather than the thermal cycle itself. This research highlights the importance of collecting data in both cycling and static (constant) thermal conditions, and further research should seek to understand whether ectotherm metabolism does respond uniquely to fluctuating temperatures.

Intraspecific plasticity and trans-generational adaptation of reproductive traits and early development in a temperate marine neogastropod

Climate warming is altering the distribution of species, producing range shifts and promoting local extinctions. There is an urgent need to understand the underlying mechanisms that influence the persistence of populations across a species' distribution range in the face of global warming. Ocenebra erinaceus is a marine gastropod that exhibits high intraspecific variability in maternal investment and physiological capacity during early stages, which suggests local adaptation to natal environmental conditions. In this study, reproductive traits and trans-generational adaptation were measured in two subtidal populations: one from the middle (the Solent, UK) and another towards the southern end of their geographic distribution (Arcachon, France). Local adaptation was evaluated with a transfer experiment (i.e. Arcachon females transferred to Solent thermal conditions) and trans-generational adaptation was evaluated in the thermal tolerance response of embryos exposed to temperatures between 10 and 20 °C. This study shows that both populations have similar fitness; however, there are adaptive costs to live under their natal location, resulting in trade-offs between reproductive traits. Transferred females show lower reproductive output, which suggests that females are maladapted to live under a new environment. The trans-generational experiment demonstrates contrasting thermal tolerance ranges between populations. Adaptation to local thermal conditions was observed in transferred embryos, showing poor performance and high mortalities under the new environment. Our results provide a better understanding of intraspecific differences and adaptations across a species’ distribution range and provide insights into how climate warming will impact encapsulated species exhibiting location-specific adaptation.

Assessment of recommended thermal inactivation parameters for fruit juices

The aim of this study was to evaluate the efficacy of recommended and recalculated thermal process parameters to achieve mandatory 5-log reduction of shiga toxin-producing Escherichia coli (STEC), Salmonella, and Listeria monocytogenes in fruit juices in the United States. Logarithms of published D-values of pathogens were plotted against temperatures (°C) to recalculate the pasteurization parameters for apple, orange and all studied fruit juices. Fruit juices were inoculated with non-adapted cells grown in TSB without glucose and acid adapted strains grown in TSB containing 1% glucose and TSB with adjusted pH to 5.0 with 1 N HCl. Microcapillary tubes with inoculated apple and orange juice were heat treated in water bath at 71 ± 1 °C for 6, 12, 36, and 48 ± 1 s. Acid adaptation increased the heat resistance of STEC, Salmonella, and L. monocytogenes. Different acid adaptation procedures affected thermal tolerance responses of tested strains. A 5-log reduction of Salmonella and STEC at 71.1 °C was achieved with minimum heat treatment for 6 s in apple juice and 6 to 12 ± 1 s in orange juice. Data presented in this study suggests that current recommended pasteurization parameters failed to reduce viable acid adapted L. monocytogenes by 5-log.

Thermal resilience may shape population abundance of two sympatric congeneric Cotesia species (Hymenoptera: Braconidae).

Basal and plasticity of thermal tolerance determine abundance, biogeographical patterns and activity of insects over spatial and temporal scales. For coexisting stemborer parasitoids, offering synergistic impact for biological control, mismatches in thermal tolerance may influence their ultimate impact in biocontrol programs under climate variability. Using laboratory-reared congeneric parasitoid species Cotesia sesamiae Cameron and Cotesia flavipes Cameron (Hymenoptera: Braconidae), we examined basal thermal tolerance to understand potential impact of climate variability on their survival and limits to activity. We measured upper- and lower -lethal temperatures (ULTs and LLTs), critical thermal limits [CTLs] (CTmin and CTmax), supercooling points (SCPs), chill-coma recovery time (CCRT) and heat knock-down time (HKDT) of adults. Results showed LLTs ranging -5 to 5°C and -15 to -1°C whilst ULTs ranged 35 to 42°C and 37 to 44°C for C. sesamiae and C. flavipes respectively. Cotesia flavipes had significantly higher heat tolerance (measured as CTmax), as well as cold tolerance (measured as CTmin) relative to C. sesamiae (P<0.0001). While SCPs did not vary significantly (P>0.05), C. flavipes recovered significantly faster following chill-coma and had higher HKDT compared to C. sesamiae. The results suggest marked differential basal thermal tolerance responses between the two congeners, with C. flavipes having an advantage at both temperature extremes. Thus, under predicted climate change, the two species may differ in phenologies and biogeography with consequences on their efficacy as biological control agents. These results may assist in predicting spatio-temporal activity patterns which can be used in integrated pest management programs under climate variability.

Testing the heat-invariant and cold-variability tolerance hypotheses across geographic gradients

Changes in temperature across geographic gradients can occur on a wide temporal range, from fluctuations within hours as a result of day-night to those over many years. These events will drive many organisms towards their physiological limits of thermal tolerance. Recently, many reports support a limited scope for adaptive evolutionary responses to high temperatures, meaning a conserved heat tolerance among ectotherms in general. We address this problem and tested the heat and cold tolerance invariant–variant hypotheses in terrestrial isopods. We studied five different populations of Porcellio laevis and three populations of Porcellio scaber, spanning 30° S latitudinal gradient in Chile. The heat tolerance of woodlice was conserved with little variation along latitude and environmental temperatures, but cold tolerance decreases significantly with environmental temperatures and latitudes. Indeed, a significant and negative correlation was observed between cold tolerance and latitude. Also, significant and positive correlations were observed among cold tolerance and environmental temperatures. Conversely, heat tolerance was not significantly correlated with any of the environmental temperatures tested neither with latitude. This macrophysiological pattern indicated that heat and cold-tolerances of species and populations not always change across geographical gradients meaning that thermal tolerance responses to high temperatures may be evolutionary constrained.

Physiological plasticity is key to the presence of the isopod Idotea baltica (Pallas) in the Baltic Sea

The low salinity of the Baltic Sea presents a physiological challenge to marine species. The marine isopod Idotea baltica is notably dominant among the shallow sublittoral of the Baltic Sea in association with Fucus vesiculosus, with permanent populations documented in salinities as low as 3psu. To investigate the role of physiological plasticity in the successful colonisation of the Baltic by I. baltica three populations from the Swedish coast were here studied, one from the Kattegat (Malmö) and two from the Baltic Sea (Kalmar and Öregrund). These three sites cover the geographic range of this species within the Baltic Sea on the Swedish coast, and also the salinity range of this species within the Baltic Sea (10–5psu). Individuals from these populations were exposed in the laboratory to a fully crossed experiment with the factors salinity and food source, to test for differences in the physiology of these populations under different conditions that may indicate local adaptation, or no differences that indicate physiological plasticity to differing salinity and food source. Metabolic rate, growth and thermal tolerance responses did not differ between the three populations across salinity treatments after a 12week exposure. The results of this study indicate that the physiology of adult I. baltica is highly plastic with regard to salinity; this plasticity is likely to have facilitated their colonisation of the Baltic Sea.

Life stage-related differences in hardening and acclimation of thermal tolerance traits in the kelp fly, Paractora dreuxi (Diptera, Helcomyzidae)

It is widely appreciated that physiological tolerances differ between life stages. However, few studies have examined stage-related differences in acclimation and hardening. In addition, the behavioural responses involved in determining the form and extent of the short-term phenotypic response are rarely considered. Here, we investigate life stage differences in the acclimation and hardening responses of the survival of a standard heat shock (SHS) and standard low temperature (or cold) shock (SCS), and the crystallization temperature (or supercooling point, SCP) of adults and larvae of the sub-Antarctic kelp fly , Paractora dreuxi. These stages live in the same habitat, but differ substantially in their mobility and thus environmental temperatures experienced. Results showed that neither acclimation nor hardening affected the lower lethal limits in larvae or adults. Adults showed an increase in survival of upper lethal limits after low temperature acclimation, whilst larvae showed a consistent lack of response. The acclimation × hardening interaction significantly affected the SCP in adults, but no response to either acclimation or hardening was found in the larvae. This study further demonstrates the complexities of thermal tolerance responses in P. dreuxi.

Hyperthermia responses in cell lines with normal and deficient DNA repairs systems

Earlier data showed that cultured cells are more hyperthermia sensitive in S phase of the cell cycle. In part this sensitivity may be related to the disruption of DNA repair/processing activity in S phase. It is well known that many components of DNA repair systems are in fact involved in DNA replication/processing. For this study we set out to evaluate a wide range of DNA repair mutants to determine their thermal responses compared to the wild-type cells. Mutants of nucleotide excision repair (NER), homologous recombination repair (HR) and nonhomologous endjoining (NHEJ) were studied. In all cases the mutants were more thermally sensitive than the wild-type counterparts. In addition, studies on thermal tolerance (TT) showed that mutants did not have a smaller TT response than the wild type thus ruling out TT as a cause in the increased sensitivity. Cell cycle analysis showed no significant difference amongst mutant and wild-type cell line pairs and thus effects of differing cell cycle distribution was also ruled out. It is speculated that it may be the involvement of the mutated pathways in DNA replication/progressing that make mutated cells more sensitive than the wild types.

Differential responses of thermal tolerance to acclimation in the sub‐Antarctic rove beetle Halmaeusa atriceps

Abstract. Investigations of the responses to acclimation of upper and lower lethal limits and limits to activity in insects have focused primarily on Drosophila. In the present study, Halmaeusa atriceps (Staphylinidae) is examined for thermal tolerance responses to acclimation, and seasonal acclimatization. In summer and winter, lower lethal temperatures of adults and larvae are approximately −7.6 ± 0.03 and −11.1 ± 0.06 °C, respectively. Supercooling points (SCPs) are more variable, with winter SCPs of −5.4 ± 0.4 °C in larvae and −6.3 ± 0.8 °C in adults. The species appears to be chill susceptible in summer and moderately freeze tolerant in winter, thus showing seasonal acclimatization. Similar changes cannot be induced solely by acclimation to low temperatures in the laboratory. Upper lethal temperatures show a weaker response to acclimation. There are also significant responses to acclimation of critical thermal limits. Critical thermal minima vary between −3.6 ± 0.2 and −0.6 ± 0.2 °C in larvae, and from −4.1 ± 0.1 to −0.8 ± 0.2 °C in adults. By contrast, critical thermal maxima vary much less within adults and larvae. These findings are in keeping with the general pattern found in insects, although this species differs in several respects from others found on Marion Island.

Thermal Tolerance Responses of Laboratory-Acclimated and Seasonally Acclimatized Atlantic Stingray, Dasyatis sabina

Abstract Atlantic stingrays, Dasyatis sabina, inhabit shallow bays subject to rapid temperature changes, yet little is known about their thermal tolerance strategies. We quantified critical thermal maxima (CTMaxima) and minima (CTMinima) of Atlantic stingrays from St. Joseph's Bay, Florida. Spiracle contraction cessation for more than one minute was the experimental endpoint. Laboratory-acclimated fish held at 10.8, 20.5, or 35.1 C exhibited CTMaxima of 35.7, 39.3, or 43.2 C, and CTMinima of 0.8, 4.8, or 10.8 C, respectively. Regression analysis revealed that CTMaxima increased by 0.31 C and CTMinima decreased by 0.41 C for every 1.0 C increase in acclimation temperature. Atlantic stingrays exposed to diel thermoperiods of 34.0–37.3 C and 7.0–11.0 C had CTMaxima of 43.1 and 33.4 C and CTMinima of 9.6 and 0.3 C, respectively, suggesting that fish acclimated to low cycle temperatures. A thermal tolerance polygon produced from laboratory data had an area of 978 C2, the third largest ever measured in a fish. ...