Testing metabolic cold adaptation and the climatic variability hypothesis in two latitudinally distant populations of a supratidal water beetle.

Temperature significantly impacts ectotherm physiology, with thermal tolerance and metabolic traits typically varying with latitude across species ranges. The drivers of this variation remain unclear, however, despite obvious consequences for population persistence and conservation in the face of ongoing global change. This study explored local adaptation and phenotypic plasticity of metabolic rates and thermal limits in the supratidal rockpool beetle Ochthebius lejolisii. Using populations from localities at different ends of the species range that experience contrasting thermal variability, we simultaneously tested two of the major paradigms of spatial physiological ecology: metabolic cold adaptation (MCA) and the climatic variability hypothesis (CVH). Reciprocal acclimation was conducted under spring temperature regimes of both localities, incorporating local diurnal variation. Metabolic rates were measured by closed respirometry, and thermal tolerance limits estimated through thermography. In line with MCA, the higher-latitude population (colder climate) showed higher metabolic rates and temperature coefficients (Q10s) at lower temperatures than the lower-latitude population. As predicted by the CVH, the lower-latitude population (more variable climate) showed higher upper thermal tolerance but only the higher-latitude population was able to acclimate upper thermal limits. This result suggests trade-offs between physiological thermal limits and thermal plasticity in this species. A limited acclimation capacity could make populations on Mediterranean coasts especially vulnerable in the face of projected increases in extreme temperatures under ongoing climate change.

Cardiac plasticity influences aerobic performance and thermal tolerance in a tropical, freshwater fish at elevated temperatures.

Fishes faced with novel thermal conditions often modify physiological functioning to compensate for elevated temperatures. This physiological plasticity (thermal acclimation) has been shown to improve metabolic performance and extend thermal limits in many species. Adjustments in cardiorespiratory function are often invoked as mechanisms underlying thermal plasticity because limitations in oxygen supply have been predicted to define thermal optima in fishes; however, few studies have explicitly linked cardiorespiratory plasticity to metabolic compensation. Here, we quantified thermal acclimation capacity in the commercially harvested Nile perch (Lates niloticus) of East Africa, and investigated mechanisms underlying observed changes. We reared juvenile Nile perch for 3 months under two temperature regimes, and then measured a series of metabolic traits (e.g. aerobic scope) and critical thermal maximum (CTmax) upon acute exposure to a range of experimental temperatures. We also measured morphological traits of heart ventricles, gills and brains to identify potential mechanisms for compensation. We found that long-term (3 month) exposure to elevated temperature induced compensation in upper thermal tolerance (CTmax) and metabolic performance (standard and maximum metabolic rate, and aerobic scope), and induced cardiac remodeling in Nile perch. Furthermore, variation in heart morphology influenced variations in metabolic function and thermal tolerance. These results indicate that plastic changes enacted over longer exposures lead to differences in metabolic flexibility when organisms are acutely exposed to temperature variation. Furthermore, we established functional links between cardiac plasticity, metabolic performance and thermal tolerance, providing evidence that plasticity in cardiac capacity may be one mechanism for coping with climate change.

Combined effects of thermal conditions and food availability on thermal tolerance of the marine bivalve, Perna viridis.

Organisms can mitigate the effects of long term variation in environmental conditions through acclimation, which involves changes in various physiological responses. To elucidate the possible effects of temperature and food concentrations on acclimation capacity, physiological responses of the mussel, Perna viridis, were measured after individuals were held for six weeks under varying temperatures and food availability. Warm-acclimated mussels experiencing higher food levels had significantly greater upper thermal limits than those maintained on lower food levels. In contrast, the upper thermal limits of cold-acclimated mussels were not affected by food levels. For warm-acclimated mussels, differences in upper thermal limits were likely due to rapid depletion of energy storage as predicted by Dynamic Energy Budget model simulations for P. viridis exposed to lower food levels. Clearance rates of cold-acclimated mussels were significantly lower than warm-acclimated mussels, regardless of food availability. The impacts of lower food acquisition on energy storage, however, could be compensated by lower metabolic rates of the cold-acclimated mussels. The availability and the ability to acquire food are not, therefore, the main drivers differentiating between the upper thermal tolerances of cold- and warm-acclimated mussels, but these differences are driven by the past thermal history the mussels experienced. The temperature tolerance range of P. viridis showed a positive shift to tolerate higher temperatures after acclimation. Such flexibility in thermal tolerance implies P. viridis has high capacity to acclimate to novel environments, which will enhance its future success given its commercial importance as an aquaculture species.

Acclimation capacity of the three-spined stickleback (Gasterosteus aculeatus, L.) to a sudden biological stress following a polymetallic exposure.

To get closer to the environmental reality, ecotoxicological studies should no longer consider the evaluation of a single pollutant, but rather combination of stress and their interaction. The aim of this study was to determine if responses of a fish to a sudden biological stress could be modified by a prior exposure to a chemical stress (a polymetallic contamination). For this purpose, in situ experiment was conducted in three ponds in the Haute-Vienne department (France). One pond was chosen for its high uranium concentration due to uranium mine tailings, and the two other ponds, which were not submitted to these tailings. Three-spined sticklebacks (Gasterosteus aculeatus) were caged in these ponds for 14 days. After this period, fish were submitted to a biological stress, exerted by lipopolysaccharides injection after anesthesia, and were sacrificed 4 days after these injections for multi-biomarkers analyses (leucocyte viability, phagocytic capacity and reactive oxygen species production, antioxidant peptide and enzymes, lipid peroxidation and DNA damage). The pond which received uranium mine tailings had higher metallic concentrations. Without biological stress, sticklebacks caged in this pond presented an oxidative stress, with increasing of reactive oxygen species levels, modification of some parts of the antioxidant system, and lipid peroxidation. Caging in the two most metal-contaminated ponds resulted in an increase of susceptibility of sticklebacks to the biological stress, preventing their phagocytic responses to lipopolysaccharides and modifying their glutathione contents and glutathione-S-transferase activity.

Antarctic notothenioid fish: what are the future consequences of 'losses' and 'gains' acquired during long-term evolution at cold and stable temperatures?

Antarctic notothenioids dominate the fish fauna of the Southern Ocean. Evolution for millions of years at cold and stable temperatures has led to the acquisition of numerous biochemical traits that allow these fishes to thrive in sub-zero waters. The gain of antifreeze glycoproteins has afforded notothenioids the ability to avert freezing and survive at temperatures often hovering near the freezing point of seawater. Additionally, possession of cold-adapted proteins and membranes permits them to sustain appropriate metabolic rates at exceptionally low body temperatures. The notothenioid genome is also distinguished by the disappearance of traits in some species, losses that might prove costly in a warmer environment. Perhaps the best-illustrated example is the lack of expression of hemoglobin in white-blooded icefishes from the family Channichthyidae. Loss of key elements of the cellular stress response, notably the heat shock response, has also been observed. Along with their attainment of cold tolerance, notothenioids have developed an extreme stenothermy and many species perish at temperatures only a few degrees above their habitat temperatures. Thus, in light of today's rapidly changing climate, it is critical to evaluate how these extreme stenotherms will respond to rising ocean temperatures. It is conceivable that the remarkable cold specialization of notothenioids may ultimately leave them vulnerable to future thermal increases and threaten their fitness and survival. Within this context, our review provides a current summary of the biochemical losses and gains that are known for notothenioids and examines these cold-adapted traits with a focus on processes underlying thermal tolerance and acclimation capacity.

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.

Optimal temperature and thermal tolerance of postlarvae of the freshwater prawn Cryphiops (Cryphiops) caementarius acclimated to different temperatures.

In this study, the optimum temperature and thermal tolerance of postlarvae of the commercially important freshwater prawn Cryphiops (Cryphiops) caementarius were determined after acclimation to six different rearing temperatures (19 °C, 22 °C, 24 °C, 26 °C, 28 °C, and 30 °C) during a 45 day-culture period. Best growth parameter values were obtained within the temperature range of 24 °C to 28 °C, where the optimum temperature for growth was found to be at 26 °C (weight gain 81.70%; specific growth rate 1.33 %/day) but had not significant effect (p > 0.05) on survival (64%-71%) of postlarvae. Increasing the acclimation temperature significantly (p < 0.05) increased both the critical thermal maximum (CTMax: from 33.82 °C to 38.48 °C) and minimum (CTMin: from 9.27 °C to 14.58 °C). The thermal tolerance interval increased (p < 0.05) from 24.55 °C to 25.48 °C in postlarvae acclimated at 28 °C but decreased (p < 0.05) to 23.90 °C in those acclimated at 30 °C. The acclimation response rate was lower for CTMax and higher for CTMin. The current (12.48 °C) and future (9.48 °C) thermal safety margins were like those reported for other tropical crustaceans. A thermal tolerance polygon over the range of 19-30 °C resulted in a calculated area of 242.25 °C2. The presented results can be used for aquaculture activities and also to help to protect this species against expected climate warming impacts.

Cellular stress response and acclimation capacity of the ditch shrimp Palaemon varians to extreme weather events - How plastic can a plastic species be?

Species from shallow marine environments are particularly vulnerable to extreme weather events (heatwaves and extreme rainfall) that can promote abrupt environmental shifts, namely in temperature and salinity (respectively). To assess how these shifts impact species' cellular stress responses (CSR), ditch shrimps Palaemon varians were exposed to a chronic (28 days) thermohaline stress experiment. Three levels of temperature (20, 23 and 26 °C) and two levels of salinity (20 and 40) were tested in a full factorial experiment, and shrimps sampled at the 7th, 14th, 21st and 28th day of exposure. Survival, wet weight (as proxy for growth), and cellular stress biomarkers associated with oxidative stress (LPO - Lipid Peroxidation, GST - Glutathione-S-Transferase, SOD - Superoxide Dismutase, TAC - Total Antioxidant Capacity and CAT - Catalase) and protein denaturation (UBI - Ubiquitin and HSP-70 - Heat Shock Protein 70 kDa) were analysed in shrimps' muscle at each sampling day. Temperature and time of exposure significantly affected biomarker levels, with shrimps exposed to 20 and 26 °C revealing more pronounced differences. No interactions were detected between temperature and salinity, suggesting that these factors display additive effects on shrimps' CSR. Antioxidant agents (CAT and TAC) increased under elevated temperature, while protein denaturation markers (UBI and HSP-70) were mostly affected by time of exposure, decreasing at 28 days. Total protein reserves increased throughout time and no effects on wet weight were observed. A negative correlation between wet weight and HSP-70 was detected, suggesting that HSP-70 levels are dependent on organism size. Peak survival (~73 %) was found under 20 °C and salinity 40 and lower survival (~30-40 %) was associated with higher temperatures (23 and 26 °C) and lower salinity (20). We conclude that P. varians displays some level of acclimation capacity but differences in survival may indicate effects on osmoregulation processes and the need for longer timeframes to fully acclimate to heat and hyposaline stress.

The effect of thermal microenvironment in upper thermal tolerance plasticity in tropical tadpoles. Implications for vulnerability to climate warming.

Current climate change is generating accelerated increase in extreme heat events and organismal plastic adjustments in upper thermal tolerances, (critical thermal maximum -CTmax ) are recognized as the quicker mitigating mechanisms. However, current research casts doubt on the actual mitigating role of thermal acclimation to face heat impacts, due to its low magnitude and weak environmental signal. Here, we examined these drawbacks by first estimating maximum extent of thermal acclimation by examining known sources of variation affecting CTmax expression, such as daily thermal fluctuation and heating rates. Second, we examined whether the magnitude and pattern of CTmax plasticity is dependent of the thermal environment by comparing the acclimation responses of six species of tropical amphibian tadpoles inhabiting thermally contrasting open and shade habitats and, finally, estimating their warming tolerances (WT = CTmax - maximum temperatures) as estimator of heating risk. We found that plastic CTmax responses are improved in tadpoles exposed to fluctuating daily regimens. Slow heating rates implying longer duration assays determined a contrasting pattern in CTmax plastic expression, depending on species environment. Shade habitat species suffer a decline in CTmax whereas open habitat tadpoles greatly increase it, suggesting an adaptive differential ability of hot exposed species to quick hardening adjustments. Open habitat tadpoles although overall acclimate more than shade habitat species, cannot capitalize this beneficial increase in CTmax, because the maximum ambient temperatures are very close to their critical limits, and this increase may not be large enough to reduce acute heat stress under the ongoing global warming.

Critical thermal limits of Poecilia caucana (Steindachner, 1880) (Cyprinodontiformes: Poeciliidae)

Aunque la temperatura tiene grandes repercusiones en la biología de los peces, se desconocen los rangos de tolerancia térmica de la mayoría de los peces dulceacuícolas. Esta falta de información impide pronosticar respuestas al cambio climático y limita los análisis comparativos que podrían enriquecer estudios evolutivos y biogeográficos. Utilizamos la metodología del crítico térmico para cuantificar la capacidad de aclimatación y la tolerancia térmica en la especie neotropical dulceacuícola Poecilia caucana. Para peces aclimatados a 20C, 25ºC y 28ºC, los críticos térmicos mínimos (CTmin) fueron 12,52 ± 0,62ºC, 13,41 ± 0,56ºC y 14,24 ± 0,43ºC, respectivamente, y los críticos térmicos máximos (CTmax) fueron 38,43 ± 0,64ºC, 40,28 ± 0,92ºC y 41,57 ± 0,27ºC, respectivamente. Tanto el CTmin como el CTmax cambiaron significativamente con las temperaturas de aclimatación, indicando que P. caucana es efectivamente aclimatable. Comparada con otras especies de peces dulceacuícolas, la capacidad de aclimatación de P. cuacana fue baja para CTmin y promedio para CTmax. Estos resultados, en conjunto con los datos de otras especies, pueden ser utilizados para responder preguntas ecológicas y evolutivas más generales.

Although temperature has far-reaching effects on fish biology, the thermal tolerance ranges of most freshwater fish species are unknown. This lack of information precludes forecasting responses to climatic change and does not allow for comparative analyses that may inform evolutionary and biogeographic studies. We used the critical thermal methodology to quantify acclimation capacity and thermal tolerance in the Neotropical freshwater species Poecilia caucana . For fish acclimated to 20C, 25ºC, and 28ºC, critical thermal minima (CTmin) were 12.52 ± 0.62ºC, 13.41 ± 0.56ºC and 14.24 ± 0.43ºC respectively, and critical thermal maxima (CTmax) were 38.43 ± 0.64ºC, 40.28 ± 0.92ºC and 41.57 ± 0.27ºC, respectively. Both CTmin and CTmax changed with acclimation temperatures, indicating that P. caucana was effectively acclimatable. Relative to values reported for other freshwater fish species, the acclimation capacity of P. caucana for CTmin was low, but it was average for CTmax. The data, together with similar work in other species, can be used in analyses focusing on broad ecological and evolutionary questions.