Thermally Variable Research Articles

Oxidative stress across multiple tissues in house sparrows (Passer domesticus) acclimated to warm, stable cold, and unpredictable cold thermal treatments.

With climate change increasing not just mean temperatures but the frequency of cold snaps and heat waves, animals occupying thermally variable areas may be faced with thermal conditions for which they are not prepared. Studies of physiological adaptations of temperate resident birds to such thermal variability are largely lacking in the literature. To address this gap, we acclimated winter-phenotype house sparrows (Passer domesticus) to stable warm, stable cold, and fluctuating cold temperatures. We then measured several metrics of the oxidative stress (OS) system, including enzymatic and non-enzymatic antioxidants and lipid oxidative damage, in brain (post-mitotic), kidney (mitotic), liver (mitotic) and pectoralis muscle (post-mitotic). We predicted that high metabolic flexibility could be linked to increases in reactive oxygen damage. Alternatively, if variation in ROS production is not associated with metabolic flexibility, then we predict no antioxidant compensation with thermal variation. Our data suggest that ROS production is not associated with metabolic flexibility, as we found no differences across thermal treatment groups. However, we did find differences across tissues. Brain catalase activity demonstrated the lowest values compared with kidney, liver and muscle. In contrast, brain glutathione peroxidase (GPx) activities were higher than those in kidney and liver. Muscle GPx activities were intermediate to brain and kidney/liver. Lipid peroxidation damage was lowest in the kidney and highest in muscle tissue.

Role of climatic variability in shaping intraspecific variation of thermal tolerance in Mediterranean water beetles.

The climatic variability hypothesis (CVH) predicts that organisms in more thermally variable environments have wider thermal breadths and higher thermal plasticity than those from more stable environments. However, due to evolutionary trade-offs, taxa with greater absolute thermal limits may have little plasticity of such limits (trade-off hypothesis). The CVH assumes that climatic variability is the ultimate driver of thermal tolerance variation across latitudinal and altitudinal gradients, but average temperature also varies along such gradients. We explored intraspecific variation of thermal tolerance in three typical Mediterranean saline water beetles (families Hydrophilidae and Dytiscidae). For each species, we compared two populations where the species coexist, with similar annual mean temperature but contrasting thermal variability (continental vs. coastal population). We estimated thermal limits of adults from each population, previously acclimated at 17, 20, or 25 °C. We found species-specific patterns but overall, our results agree with the CVH regarding thermal ranges, which were wider in the continental (more variable) population. In the two hydrophilid species, this came at the cost of losing plasticity of the upper thermal limit in this population, supporting the trade-off hypothesis, but not in the dytiscid one. Our results support the role of local adaptation to thermal variability and trade-offs between basal tolerance and physiological plasticity in shaping thermal tolerance in aquatic ectotherms, but also suggest that intraspecific variation of thermal tolerance does not fit a general pattern among aquatic insects. Overlooking such intraspecific variation could lead to inaccurate predictions of the vulnerability of aquatic insects to global warming.

Fine-scale heterogeneity reveals disproportionate thermal stress and coral mortality in thermally variable reef habitats during a marine heatwave.

The online version contains supplementary material available at 10.1007/s00338-022-02328-6.

Effect of thermal variation on the cardiac thermal limits of a eurythermal marine teleost (Girella nigricans).

Although most animals live in complex, thermally variable environments, the impact of this variability on specific physiological systems is still unresolved. The ectotherm heart is known to change in both structure and function to ensure appropriate oxygen delivery under different thermal regimes, but the plasticity of the upper thermal limits of the heart under stable or variable thermal acclimation conditions remains unknown. To investigate the role of thermal variability on cardiac acclimation potential, we acclimated a eurythermal fish, opaleye (Girella nigricans), to three static temperature treatments (13, 16, and 19 °C) as well as two oscillating treatments which cycled between maximum and minimum temperatures every 12 h (13–19 °C and 16–22 °C). These temperatures and daily thermal ranges were chosen to mimic the conditions observed in the rocky intertidal environments in Santa Barbara, CA, USA where the fish were collected. We hypothesized that increasing temperature would increase upper thermal limits of the heart, and that variable acclimations would result in broader acute thermal performance curves (TPCs) compared to static acclimations. We measured maximum heart rate during acute warming to determine cardiac thermal performance (i.e., the temperature corresponding to the onset of cardiac arrythmia, the temperature at maximum heart rate, absolute maximum heart rate, and the Arrhenius breakpoint temperature) and construct acute TPCs. Rising static acclimation temperatures increased upper thermal limits but had no impact on peak maximum heart rate. The warmest static temperature did, however, cause a narrowing of the acute TPC. Fish acclimated to variable conditions had the same upper thermal limits compared to fish acclimated to static conditions with the same mean temperature in all metrics of thermal performance. Further, there was no significant broadening of the acute TPC. This study suggests that cardiac plasticity is robust to thermal variation in this eurythermal fish.

Thermal tolerance, safety margins and vulnerability of coastal species: Projected impact of climate change induced cold water variability in a temperate African region

Anthropogenic induced climate change is predicted to increase the thermal variability in coastal waters, which can have strong physiological effects on individuals and populations of marine ectotherms. The magnitude and direction of these thermal effects varies depending on species, life stage, biogeography, habitat and season. This study aimed to compare the thermal tolerance of a range of juvenile fish and adult macro-invertebrates from intertidal and estuarine habitats in a warm-temperate, thermally variable region on the south-east coast of South Africa. Seasonal variability in thermal tolerance was compared between species, taxonomic groups, biogeographical distribution and habitat affinity and related to existing and projected water temperature data to gauge the local vulnerability of each species. Critical thermal maximum (CTmax), critical thermal minimum (CTmin), thermal breadths and scopes, and the thermal safety margins of each species were quantified. The greatest differences in thermal tolerance patterns were based on taxonomy, with macro-invertebrates having broader thermal tolerance compared to fish, with the exception of the Cape sea urchin, in both summer and winter. Relatively narrow lower breadths in tolerance and safety margin values for transient juvenile sub-tropical and temperate fish species from the intertidal rocky low-shore habitat were observed in both summer and winter. This indicates that these fish species and the Cape sea urchin may be more vulnerable to projected increases in cold temperature (upwelling in summer) than warm temperature variability in this warm-temperate region if they are unable to seek thermal habitat refuge.

Thermal variability during ectotherm egg incubation: A synthesis and framework.

Natural populations of ectothermic oviparous vertebrates typically experience thermal variability in their incubation environment. Yet an overwhelming number of laboratory studies incubate animals under constant thermal conditions that cannot capture natural thermal variability. Here, we systematically searched for studies that incubated eggs of ectothermic vertebrates, including both fishes and herpetofauna, under thermally variable regimes. We ultimately developed a compendium of 66 studies that used thermally variable conditions for egg incubation. In this review, we qualitatively discuss key findings from literature in the compendium, including the phenotypic effects resulting from different patterns of thermally variable incubation, as well as the ontogenetic persistence of these effects. We also describe a physiological framework for contextualizing some of these effects, based on thermal performance theory. Lastly, we highlight key gaps in our understanding of thermally variable incubation and offer suggestions for future studies.

Rapid within- and transgenerational changes in thermal tolerance and fitness in variable thermal landscapes.

Phenotypic plasticity may increase the performance and fitness and allow organisms to cope with variable environmental conditions. We studied within‐generation plasticity and transgenerational effects of thermal conditions on temperature tolerance and demographic parameters in Drosophila melanogaster. We employed a fully factorial design, in which both parental (P) and offspring generations (F1) were reared in a constant or a variable thermal environment. Thermal variability during ontogeny increased heat tolerance in P, but with demographic cost as this treatment resulted in substantially lower survival, fecundity, and net reproductive rate. The adverse effects of thermal variability (V) on demographic parameters were less drastic in flies from the F1, which exhibited higher net reproductive rates than their parents. These compensatory responses could not totally overcome the challenges of the thermally variable regime, contrasting with the offspring of flies raised in a constant temperature (C) that showed no reduction in fitness with thermal variation. Thus, the parental thermal environment had effects on thermal tolerance and demographic parameters in fruit fly. These results demonstrate how transgenerational effects of environmental conditions on heat tolerance, as well as their potential costs on other fitness components, can have a major impact on populations’ resilience to warming temperatures and more frequent thermal extremes.

Preferred temperature of intertidal ectotherms: Broad patterns and methodological approaches.

Preferred temperature (Tpref) has been measured in over 100 species of aquatic and 300 species of terrestrial ectotherms as a metric for assessing behavioural thermoregulation in variable environments and, as such, has been linked to ecological processes ranging from individual behaviour to population and community dynamics. Due to the asymmetric shape of performance curves, Tpref is typically lower than the optimal temperature (Topt, where physiological performance is at its peak), and the degree of this mismatch increases with variability in Tb. Intertidal ectotherms experience huge variability in Tb on a daily basis and therefore provide a good system to test whether the relationship between Tpref and variation in Tb holds in more extreme environments. A review of the literature, however, only revealed comparisons between Tpref and Topt for five intertidal species and measurements of Tpref for 23 species. An analysis of this limited literature for intertidal ectotherms showed a positive relationship between acclimation temperature and Tpref. There was, however, great variation in the methodologies employed to make these assessments. Factors contributing to behavioural thermoregulation in intertidal ectotherms including small body size; low mobility; interactions among individuals; endogenous clocks; metabolic effects; thermal sensitivity; sampling of the thermal environment and recent acclimation history were considered to varying degrees when measuring Tpref, confounding comparisons between species. The methodologies used to measure Tpref in intertidal ectotherms were reviewed in light of each of these factors, and methodologies proposed to standardize approaches. Given the theoretical predictions about the relationships between Tpref and variability in Tb, the spatial and temporal thermal variability experienced by intertidal ectotherms provides numerous opportunities to test these expectations if assessed in a standardized manner, and can potentially provide insights into the value of behavioural thermoregulation in the more thermally variable environments predicted to occur in the near future.

Distinct Responses of the Nitrogen-Fixing Marine Cyanobacterium Trichodesmium to a Thermally Variable Environment as a Function of Phosphorus Availability.

Surface temperature in the ocean is projected to be elevated and more variable in the future, which will interact with other environmental changes like reduced nutrient supplies. To explore these multiple stressor relationships, we tested the influence of thermal variation on the key marine diazotrophic cyanobacterium Trichodesmium erythraeum GBRTRLI101 as a function of the limiting nutrient phosphorus (P). Two constant temperature treatments represented current winter (22°C) and summer (30°C) mean values. Three variable temperature treatments fluctuated around the constant control values: Mean 22°C, either ± 2°C or ± 4°C; and mean 30°C ± 2°C. Each thermal treatment was grown under both P-replete (10 μmol/L) and P-limiting conditions (0.2 μmol/L). Effects of thermal variability on Trichodesmium were mainly found in the two winter variable temperature treatments (22°C ± 2°C or ± 4°C). P availability affected growth and physiology in all treatments and had significant interactions with temperature. P-replete cultures had higher growth and nitrogen and carbon fixation rates in the 22°C constant control, than in the corresponding variable treatments. However, physiological rates were not different in the P-replete constant and variable treatments at 30°C. In contrast, in P-limited cultures an advantage of constant temperature over variable temperature was not apparent. Phosphorus use efficiencies (PUE, mol N or C fixed h-1 mol cellular P-1) for nitrogen and carbon fixation were significantly elevated under P-limited conditions, and increased with temperature from 22 to 30°C, implying a potential advantage in a future warmer, P-limited environment. Taken together, these results imply that future increasing temperature and greater thermal variability could have significant feedback interactions with the projected intensification of P-limitation of marine N2-fixing cyanobacteria.

The Devil is in the Details: Identifying Aspects of Temperature Variation that Underlie Sex Determination in Species with TSD.

Most organisms experience thermal variability in their environment; however, our understanding of how organisms cope with this variation is under-developed. For example, in organisms with temperature-dependent sex determination (TSD), an inability to predict sex ratios under fluctuating incubation temperatures in the field hinders predictions of how species with TSD will fare in a changing climate. To better understand how sex determination is affected by thermal variation, we incubated Trachemys scripta eggs using a "heat wave" design, where embryos experienced a male-producing temperature of 25 ± 3°C for the majority of development and varying durations at a female-producing temperature of 29.5 ± 3°C during the window of development when sex is determined. We compared the sex ratios from these incubation conditions with a previous data set that utilized a similar heat wave design, but instead incubated eggs at a male-producing temperature of 27 ± 3°C but utilized the same female-producing temperature of 29.5 ± 3°C. We compared the sex ratio reaction norms produced from these two incubation conditions and found that, despite differences in average temperatures, both conditions produced 50:50 sex ratios after ∼8 days of exposure to female-producing conditions. This emphasizes that sex can be determined in just a few days at female-producing conditions and that sex determination is relatively unaffected by temperatures outside of this short window. Further, these data demonstrate the reduced accuracy of the constant temperature equivalent model (the leading method of predicting sex ratios) under thermally variable temperatures. Conceptualizing sex determination as the number of days spent incubating at female-producing conditions rather than an aggregate statistic is supported by the mechanistic underpinnings of TSD, helps to improve sex ratio estimation methods, and has important consequences for predicting how species with TSD will fare in a changing climate.

High-frequency temperature variability mirrors fixed differences in thermal limits of the massive coral Porites lobata.

Spatial heterogeneity in environmental characteristics can drive adaptive differentiation when contrasting environments exert divergent selection pressures. This environmental and genetic heterogeneity can substantially influence population and community resilience to disturbance events. Here, we investigated corals from the highly variable back-reef habitats of Ofu Island in American Samoa that thrive in thermal conditions known to elicit widespread bleaching and mortality elsewhere. To investigate the relative importance of acclimation versus site of origin in shaping previously observed differences in coral tolerance limits at Ofu Island, specimens of the common Indo-Pacific coral Porites lobata from locations with differing levels of thermal variability were acclimated to low and high thermal variation in controlled common garden aquaria. Overall, there were minimal effects of the acclimation exposure. Corals native to the site with the highest level of daily variability grew fastest, regardless of acclimation treatment. When exposed to lethal thermal stress, corals native to both variable sites contained elevated levels of heat shock proteins and maintained photosynthetic performance for 1-2 days longer than corals from the stable environment. Despite being separated by <5 km, there was significant genetic differentiation among coral colonies (FST=0.206, P<0.0001; nuclear ribosomal DNA), whereas Symbiodiniaceae were all Cladocopium sp. (ITS type C15). Our study demonstrates consistent signatures of adaptation in growth and stress resistance in corals from naturally thermally variable habitats, suggesting that differences in the amount of thermal variability may be an important contributor to adaptive differentiation in reef-building corals.

Coral Symbiodinium Community Composition Across the Belize Mesoamerican Barrier Reef System is Influenced by Host Species and Thermal Variability.

Reef-building corals maintain a symbiotic relationship with dinoflagellate algae of the genus Symbiodinium, and this symbiosis is vital for the survival of the coral holobiont. Symbiodinium community composition within the coral host has been shown to influence a coral's ability to resist and recover from stress. A multitude of stressors including ocean warming, ocean acidification, and eutrophication have been linked to global scale decline in coral health and cover in recent decades. Three distinct thermal regimes (highTP, modTP, and lowTP) following an inshore-offshore gradient of declining average temperatures and thermal variation were identified on the Belize Mesoamerican Barrier Reef System (MBRS). Quantitative metabarcoding of the ITS-2 locus was employed to investigate differences and similarities in Symbiodinium genetic diversity of the Caribbean corals Siderastrea siderea, S. radians, and Pseudodiploria strigosa between the three thermal regimes. A total of ten Symbiodinium lineages were identified across the three coral host species. S. siderea was associated with distinct Symbiodinium communities; however, Symbiodinium communities of its congener, S. radians and P. strigosa, were more similar to one another. Thermal regime played a role in defining Symbiodinium communities in S. siderea but not S. radians or P. strigosa. Against expectations, Symbiodinium trenchii, a symbiont known to confer thermal tolerance, was dominant only in S. siderea at one sampled offshore site and was rare inshore, suggesting that coral thermal tolerance in more thermally variable inshore habitats is achieved through alternative mechanisms. Overall, thermal parameters alone were likely not the only primary drivers of Symbiodinium community composition, suggesting that environmental variables unrelated to temperature (i.e., light availability or nutrients) may play key roles in structuring coral-algal communities in Belize and that the relative importance of these environmental variables may vary by coral host species.

Thermal variability alters the impact of climate warming on consumer-resource systems.

Thermal variation through space and time are prominent features of ecosystems that influence processes at multiple levels of biological organization. Yet, it remains unclear how populations embedded within biological communities will respond to climate warming in thermally variable environments, particularly as climate change alters existing patterns of thermal spatial and temporal variability. As environmental temperatures increase above historical ranges, organisms may increasingly rely on extreme habitats to effectively thermoregulate. Such locations desirable in their thermal attributes (e.g., thermal refugia) are often suboptimal for resource acquisition (e.g., underground tunnels). Thus, via the expected increase in both mean temperatures and diel thermal variation, climate warming may heighten the trade-off for consumers between behaviors maximizing thermal performance and those maximizing resource acquisition. Here, we integrate behavioral, physiological, and trophic ecology to provide a general framework for understanding how temporal thermal variation, mediated by access to a thermal refugium, alters the response of consumer-resource systems to warming. We use this framework to predict how temporal variation and access to thermal refugia affect the persistence of consumers and resources during climate warming, how the quality of thermal refugia impact consumer-resource systems, and how consumer-resource systems with fast vs. slow ecological dynamics respond to warming. Our results show that the spatial thermal variability provided by refugia can elevate consumer biomass at warmer temperatures despite reducing the fraction of time consumers spend foraging, that temporal variability detrimentally impacts consumers at high environmental temperatures, and that consumer-resource systems with fast ecological dynamics are most vulnerable to climate warming. Thus, incorporating both estimates of thermal variability and species interactions may be necessary to accurately predict how populations respond to warming.

Aquatic and terrestrial locomotor performance of juvenile three-keeled pond turtles acclimated to different temperatures

Locomotion is important for behaviors such as foraging and predator avoidance, and is influenced by temperature in ectotherms. To investigate this in turtles, we acclimated juvenile Chinese three-keeled pond turtles,Chinemys reevesii, under three thermal conditions for four weeks. Subsequently, we measured three locomotor performances (swimming, running, and righting) at different test temperatures. Overall, swimming and running speeds of turtles increased with increasing test temperature in the range of 13-33°C and decreased at higher test temperatures, whereas righting time decreased with increasing test temperature in the range of 13-33°C and slightly increased at higher test temperatures. Acclimation temperature affected both swimming and running speeds, with the high temperature-acclimated turtles swimming and running faster than low temperature-acclimated turtles, but it did not affect righting performance. From the constructed thermal performance curves, between-group differences were found in the estimated maximal speed (swimming and running) and optimal temperature, but not in the performance breadth. Juvenile turtles acclimated to relatively warm temperatures had better performances than those acclimated to cool temperatures, supporting the “hotter is better” hypothesis. A similar acclimatory change was found during aquatic and terrestrial locomotion in juvenileC. reevesii. Our findings are consistent with the hypothesis that animals from less thermally variable environments should have a greater acclimatory ability than those from more variable environments, because turtles were acclimated under aquatic environments with no thermal variability.

Wind-driven upwelling in lakes destabilizes thermal regimes of downstream rivers

Natural lakes are generally assumed to stabilize thermal regimes of downstream rivers. This conceptual model does not account for the potential destabilizing effects that wind has on the surface temperatures of thermally stratified lakes and, therefore, on thermal regimes of outflowing rivers. We examined the thermal variation in streams and rivers from 24 watersheds without lakes and 15 draining lakes that varied in surface area (0.3–101 km2) and thus, their potential exposure to wind. Rivers draining large lakes (> 10 km2 surface area) had summer thermal regimes with 1.8 times more variation (expressed as the coefficient of variation) than both rivers draining smaller lakes and watersheds lacking lakes. Statistical decomposition of thermal regimes revealed that ∼ 3% (range: 1–5%) of the thermal variability in rivers below large lakes was from diel-scale variation, compared to 31% (14–48%) in streams lacking lakes and 24% (6–34%) in those draining smaller lakes. Instead, rivers downstream of large lakes had distinct summer thermal regimes characterized by abrupt cooling events involving drops in temperature of 5–10°C that lasted 1–3 d. These events were generally synchronous across space and not observed in watersheds without lakes or in watersheds draining small lakes. Cooling events in rivers were coordinated with high velocity winds that passed thresholds for upwelling of cool hypolimnetic water to lake outlets. Wind driven upwelling may be a common source of thermal variation in rivers draining large stratified lakes and reservoirs, making them more thermally variable than previously appreciated. The ecological responses to this thermal instability remain unexplored.

Coping with daily thermal variability: behavioural performance of an ectotherm model in a warming world.

Global climate change poses one of the greatest threats to species persistence. Most analyses of the potential biological impacts have focused on changes in mean temperature, but changes in thermal variance will also impact organisms and populations. We assessed the effects of acclimation to daily variance of temperature on dispersal and exploratory behavior in the terrestrial isopod Porcellio laevis in an open field. Acclimation treatments were 24±0, 24±4 and 24±8°C. Because the performance of ectotherms relates nonlinearly to temperature, we predicted that animals acclimated to a higher daily thermal variation should minimize the time exposed in the centre of open field, – i.e. increase the linearity of displacements. Consistent with our prediction, isopods acclimated to a thermally variable environment reduce their exploratory behaviour, hypothetically to minimize their exposure to adverse environmental conditions. This scenario as well as the long latency of animals after releases acclimated to variable environments is consistent with this idea. We suggested that to develop more realistic predictions about the biological impacts of climate change, one must consider the interactions between the mean and variance of environmental temperature on animals' performance.

Is post-feeding thermotaxis advantageous in elasmobranch fishes?

The effects of post-feeding thermotaxis on ileum evacuation and absorption rates were examined in the laboratory using two elasmobranch species, the Atlantic stingray Dasyatis sabina, which inhabits thermally variable environments, and the whitespotted bamboo shark Chiloscyllium plagiosum, a stenothermic fish living on Indo-Pacific reefs. Experiments at temperatures similar to those experienced in nature revealed temperature change had no significant effect on C. plagiosum absorption or evacuation rates, suggesting stenothermic sharks cannot exploit temperature differences as a means to improve digestion efficiency. On the other hand, D. sabina showed significantly lower evacuation and absorption rates at lower temperatures. The relative decrease was greater for evacuation (Q₁₀ = 3·08) than absorption rates (Q₁₀ = 2·20), resulting in a significant increase in total absorption, suggesting D. sabina can benefit from using shuttling behaviour to exploit thermal variability in their environment to maximize energetic uptake.