The unique mitochondrial form and function of Antarctic channichthyid icefishes

Antarctic icefishes of the family Channichthyidae are the only vertebrate animals that as adults do not express the circulating oxygen-binding protein hemoglobin (Hb). Six of the 16 family members also lack the intracellular oxygen-binding protein myoglobin (Mb) in the ventricle of their hearts and all lack Mb in oxidative skeletal muscle. The loss of Hb has led to substantial remodeling in the cardiovascular system of icefishes to facilitate adequate oxygenation of tissues. One of the more curious adaptations to the loss of Hb and Mb is an increase in mitochondrial density in cardiac myocytes and oxidative skeletal muscle fibers. The proliferation of mitochondria in the aerobic musculature of icefishes does not arise through a canonical pathway of mitochondrial biogenesis. Rather, the biosynthesis of mitochondrial phospholipids is up-regulated independently of the synthesis of proteins and mitochondrial DNA, and newly-synthesized phospholipids are targeted primarily to the outer-mitochondrial membrane. Consequently, icefish mitochondria have a higher lipid-to-protein ratio compared to those from red-blooded species. Elevated levels of nitric oxide in the blood plasma of icefishes, compared to red-blooded notothenioids, may mediate alterations in mitochondrial density and architecture. Modifications in mitochondrial structure minimally impact state III respiration rates but may significantly enhance intracellular diffusion of oxygen. The rate of oxygen diffusion is greater within the hydrocarbon core of membrane lipids compared to the aqueous cytosol and impeded only by proteins within the lipid bilayer. Thus, the proliferation of icefish's mitochondrial membranes provides an optimal conduit for the intracellular diffusion of oxygen and compensates for the loss of Hb and Mb. Currently little is known about how mitochondrial phospholipid synthesis is regulated and integrated into mitochondrial biogenesis. The unique architecture of the oxidative muscle cells of icefishes highlights the need for further studies in this area.     

Thermal tolerance of Antarctic notothenioid fishes correlates with level of circulating hemoglobin

The West Antarctic Peninsula region is experiencing some of the most rapid elevations in temperature of any marine environment. We assessed thermal tolerance of white- and red-blooded Antarctic notothenioid fishes inhabiting these waters, using a modified critical thermal maximum (CT(max)) design. Temperature was elevated acutely from ambient at a constant rate of 3.6°C h(-1), and CT(max) was defined as the temperature where animals lost righting response. CT(max) temperatures of white-blooded icefishes Chionodraco rastrospinosus (13.3° ± 0.2°C) and Chaenocephalus aceratus (13.9° ± 0.4°C) were significantly lower than those of red-blooded fishes Gobionotothen gibberifrons (15.5° ± 0.2°C) and Notothenia coriiceps (17.1° ± 0.2°C). Lepidonotothen squamifrons, a red-blooded species with low hematocrit, exhibited a CT(max) (14.2° ± 0.4°C) that was significantly lower than that of the other red-blooded animals and similar to that of icefishes. A strong relationship between CT(max) and hematocrit (r(2) = 0.76) suggests that the oxygen-carrying capacity of blood may partially dictate acute lethal temperature. Despite a short treatment duration, we detected a rise in the mRNA level of hypoxia response gene HIF-1α in N. coriiceps heart tissue. One-week exposure to 4°C had no effect on the CT(max) of N. coriiceps, indicating an inability to compensate for rising temperature under these experimental conditions. Our results suggest that icefishes are particularly sensitive to temperature elevation because of a lack of hemoglobin and may be a sentinel taxon for climate change.     

Developmental and physiological challenges of octopus (Octopus vulgaris) early life stages under ocean warming

The ability to understand and predict the effects of ocean warming (under realistic scenarios) on marine biota is of paramount importance, especially at the most vulnerable early life stages. Here we investigated the impact of predicted environmental warming (+3 °C) on the development, metabolism, heat shock response and antioxidant defense mechanisms of the early stages of the common octopus, Octopus vulgaris. As expected, warming shortened embryonic developmental time by 13 days, from 38 days at 18 °C to 25 days at 21 °C. Concomitantly, survival decreased significantly (~29.9 %). Size at hatching varied inversely with temperature, and the percentage of smaller premature paralarvae increased drastically, from 0 % at 18 °C to 17.8 % at 21 °C. The metabolic costs of the transition from an encapsulated embryo to a free planktonic form increased significantly with warming, and HSP70 concentrations and glutathione S-transferase activity levels were significantly magnified from late embryonic to paralarval stages. Yet, despite the presence of effective antioxidant defense mechanisms, ocean warming led to an augmentation of malondialdehyde levels (an indicative of enhanced ROS action), a process considered to be one of the most frequent cellular injury mechanisms. Thus, the present study provides clues about how the magnitude and rate of ocean warming will challenge the buffering capacities of octopus embryos and hatchlings’ physiology. The prediction and understanding of the biochemical and physiological responses to warmer temperatures (under realistic scenarios) is crucial for the management of highly commercial and ecologically important species, such as O. vulgaris.     

Thermal tolerance and preference of exploited turbinid snails near their range limit in a global warming hotspot

Predicted global climate change has prompted numerous studies of thermal tolerances of marine species. The upper thermal tolerance is unknown for most marine species, but will determine their vulnerability to ocean warming. Gastropods in the family Turbinidae are widely harvested for human consumption. To investigate the responses of turbinid snails to future conditions we determined critical thermal maxima (CTMax) and preferred temperatures of Turbo militaris and Lunella undulata from the tropical-temperate overlap region of northern New South Wales, on the Australian east coast. CTMax were determined at two warming rates: 1 °C/30 min and 1 °C/12 h. The number of snails that lost attachment to the tank wall was recorded at each temperature increment. At the faster rate, T. militaris had a significantly higher CTMax (34.0 °C) than L. undulata (32.2 °C). At the slower rate the mean of both species was lower and there was no significant difference between them (29.4 °C for T. militaris and 29.6 °C for L. undulata). This is consistent with differences in thermal inertia possibly allowing animals to tolerate short periods at higher temperatures than is possible during longer exposure times, but other mechanisms are not discounted. The thermoregulatory behaviour of the turban snails was determined in a horizontal thermal gradient. Both species actively sought out particular temperatures along the gradient, suggesting that behavioural responses may be important in ameliorating short-term temperature changes. The preferred temperatures of both species were higher at night (24.0 °C and 26.0 °C) than during the day (22.0 °C and 23.9 °C). As the snails approached their preferred temperature, net hourly displacement decreased. Preferred temperatures were within the average seasonal seawater temperature range in this region. However, with future predicted water temperature trends, the species could experience increased periods of thermal stress, possibly exceeding CTMax and potentially leading to range contractions.     

Effects of temperature acclimation on cardiorespiratory performance of the Antarctic notothenioid Trematomus bernacchii

Notothenioid fishes of the Southern Ocean have evolved under cold and stable temperatures for millions of years. Due to rising temperatures in the Southern Ocean, investigating thermal limits and the capacities for inducing a temperature acclimation response in notothenioids has become of increasing interest. Here, we investigated effects of temperature acclimation on cardiorespiratory responses and cardiac and skeletal muscle energy metabolism in a benthic Antarctic notothenioid, Trematomus bernacchii. We acclimated specimens to ?1, 2 and 4.5 °C for 14 days and quantified heart rates and ventilation rates during an acute increase in temperature. Ventilation rates showed an effect of acclimation both at initial steady-state acclimation conditions and during an acute temperature increase, suggesting a partial thermal compensatory response. However, acclimation did not affect heart rates at steady-state acclimation conditions and the temperatures at which onset of cardiac arrhythmia occurred, suggesting lack of inducible thermal tolerance in cardiac performance. Citrate synthase (CS), lactate dehydrogenase (LDH) and 3-hydroxyacyl dehydrogenase activities in skeletal muscle tissues suggested acclimation-induced shifts in metabolic fuel preferences, and a marked increase in LDH activity with acclimation to 4.5 °C showed an increase in anaerobic metabolism. In heart tissue, CS and LDH activities decreased with acclimation to 4.5 °C, suggesting reduced cardiac ATP production. Overall, the data suggest a partial acclimatory response to temperature by T. bernacchii and support the hypothesis that reduced cardiac acclimatory capacity may play a role in limiting the thermal plasticity of T. bernacchii.     

Ocean cleaning stations under a changing climate: biological responses of tropical and temperate fish‐cleaner shrimp to global warming

Cleaning symbioses play an important role in the health of certain coastal marine communities. These interspecific associations often occur at specific sites (cleaning stations) where a cleaner organism (commonly a fish or shrimp) removes ectoparasites/damaged tissue from a ‘client’ (a larger cooperating fish). At present, the potential impact of climate change on the fitness of cleaner organisms remains unknown. This study investigated the physiological and biochemical responses of tropical (Lysmata amboinensis) and temperate (L. seticaudata) cleaner shrimp to global warming. Specifically, thermal limits (CTMax), metabolic rates, thermal sensitivity, heat shock response (HSR), lipid peroxidation [malondialdehyde (MDA) concentration], lactate levels, antioxidant (GST, SOD and catalase) and digestive enzyme activities (trypsin and alkaline phosphatase) at current and warming (+3 °C) temperature conditions. In contrast to the temperate species, CTMax values decreased significantly from current (24–27 °C) to warming temperature conditions (30 °C) for the tropical shrimp, where metabolic thermal sensitivity was affected and the HSR was significantly reduced. MDA levels in tropical shrimp increased dramatically, indicating extreme cellular lipid peroxidation, which was not observed in the temperate shrimp. Lactate levels, GST and SOD activities were significantly enhanced within the muscle tissue of the tropical species. Digestive enzyme activities in the hepatopancreas of both species were significantly decreased by warmer temperatures. Our data suggest that the tropical cleaner shrimp will be more vulnerable to global warming than the temperate Lysmata seticaudata; the latter evolved in a relatively unstable environment with seasonal thermal variations that may have conferred greater adaptive plasticity. Thus, tropical cleaning symbioses may be challenged at a greater degree by warming‐related anthropogenic forcing, with potential cascading effects on the health and structuring of tropical coastal communities (e.g. coral reefs).     

Behavioural thermoregulation and critical thermal limits of Macrobrachium acanthurus (Wiegman)

• (1)The preferred temperatures of Macrobrachium acanthurus were determined for prawns acclimated to 20°C, 23°C, 26°C, 29°C and 32°C, and the final preferendum estimate was (29.5°C).
• (2)The critical thermal minima (CTMin) and maxima (CTMax) were 11.0°C, 12.1°C, 13.0°C and 14.8°C, and 34.2°C, 35.0°C, 36.1°C and 39.8°C, respectively.
• (3)The zone of thermal tolerance assessed using the CTMin and CTMax boundaries was 644°C².
• (4)The acclimation response ratio was between 0.33 and 0.62.
• (5)To cultivate this species in the southeastern region of México it should be done in not <15°C (CTMin) during the winter and below 38°C in summer (CTMax).

     

Effect of warming rate on the critical thermal maxima of crabs,shrimp and fish

The threat of global warming has prompted numerous recent studies on the thermal tolerance of marine species. A widely used method to determine the upper thermal limit has been the Critical Thermal Maximum (CTMax), a dynamic method, meaning that temperature is increased gradually until a critical point is reached. This method presents several advantages over static methods, however, there is one main issue that hinders interpretation and comparison of CTMax results: the rate at which the temperature is increased. This rate varies widely among published protocols. The aim of the present work was to determine the effect of warming rate on CTMax values, using different animal groups. The influence of the thermal niche occupied by each species (intertidal vs subtidal) and habitat (intertidal vs subtidal) was also investigated. CTMax were estimated at three different rates: 1 °C min⁻¹, 1 °C 30 min⁻¹ and 1 °C h⁻¹, in two species of crab, Eurypanopeus abbreviatus and Menippe nodifrons, shrimp Palaemon northropi and Hippolyte obliquimanus and fish Bathygobius soporator and Parablennius marmoreus. While there were significant differences in the effect of warming rates for some species, for other species warming rate produced no significant differences (H. obliquimanus and B. soporator). While in some species slower warming rates lead to lower CTMax values (P. northropi and P. marmoreus) in other species the opposite occurred (E. abbreviatus and M. nodifrons). Biological group has a significant effect with crabs' CTMax increasing at slower warming rates, which did not happen for shrimp and fish. Subtidal species presented lower CTMax, at all warming rates tested. This study highlights the importance of estimating CTMax values at realistic rates that species encounter in their environment and thus have an ecological value.     

Phenological Sensitivity of Early and Late Flowering Species Under Seasonal Warming and Altered Precipitation in a Seminatural Temperate Grassland Ecosystem

Shifts in flowering phenology of plants are indicators of climate change. The great majority of existing phenological studies refer solely to gradual warming. However, knowledge on how flowering phenology responds to changes in seasonal variation of warming and precipitation regimes is missing. We report the onset of 22 early (flowering before/within May) and 23 late flowering (flowering after May) species in response to manipulated seasonal warming (equal to + 1.2°C; last 100-year summer/winter warming), additional winter rainfall, and modified precipitation variability (including a 1000-year extreme drought event followed by heavy rainfall) over the growing season in two consecutive years for a species-rich temperate grassland ecosystem. The average onset of flowering (over 2 years) was significantly advanced 3.1 days by winter warming and 1.5 days by summer warming compared to control. Early flowering species responded to seasonal warming in both years, while late-flowering species responded in only 1 year to summer warming. The average onset of early flowering species was significantly advanced, 4.9 days by winter warming and 2.3 days by summer warming. Species-specific analysis showed that even within the early flowering community there were divergences. A positive correlation between plant height and shift in flowering onset was detected under winter warming (R² = 0.20, p = 0.005). The average onsets of early and late flowering community were affected by neither winter rain nor growing season precipitation variability. Seasonal differences in warming, and particularly winter warming, might alter community dynamics among early and late flowering species which can cause shifts in the seasonal performances of temperate ecosystems.     

GH–IGF system regulation of attenuated muscle growth and lipolysis in Atlantic salmon reared at elevated sea temperatures

Growth regulation in adult Atlantic salmon (1.6 kg) was investigated during 45 days in seawater at 13, 15, 17, and 19 °C. We focused on feed intake, nutrient uptake, nutrient utilization, and endocrine regulation through growth hormone (GH), insulin-like growth factors (IGF), and IGF-binding proteins (IGFBP). During prolonged thermal exposure, salmon reduced feed intake and growth. Feed utilization was reduced at 19 °C after 45 days compared with fish at lower temperatures, and body lipid storage was depleted with increasing water temperature. Although plasma IGF-1 concentrations did not change, 32-Da and 43-kDa IGFBP increased in fish reared at ≤17 °C, and dropped in fish reared at 19 °C. Muscle igf1 mRNA levels were reduced at 15 and 45 days in fish reared at 15, 17, and 19 °C. Muscle igf2 mRNA levels did not change after 15 days in response to increasing temperature, but were reduced after 45 days. Although liver igf2 mRNA levels were reduced with increasing temperatures after 15 and 45 days, temperature had no effect on igf1 mRNA levels. The liver igfbp2b mRNA level, which corresponds to circulating 43-kDa IGFBP, exhibited similar responses after 45 days. IGFBP of 23 kDa was only detected in plasma in fish reared at 17 °C, and up-regulation of the corresponding igfbp1b gene indicated a time-dependent catabolic response, which was not observed in fish reared at 19 °C. However, higher muscle ghr mRNA levels were detected in fish at 17 and 19 °C than in fish at lower temperatures, indicating lipolytic regulation in muscle. These results show that the reduction of muscle growth in large salmon is mediated by decreased igf1 and igf2 mRNA levels in addition to GH-associated lipolytic action to cope with prolonged thermal exposure. Accordingly, 13 °C appears to be a more optimal temperature for the growth of adult Atlantic salmon at sea.     

Growth and thermal tolerance of a Tibet fish Schizopygopsis younghusbandi juveniles acclimated to three temperature levels

Schizopygopsis younghusbandi is an endemic fish of Tibet characterized by slow growth. Artificial stock enhancement was applied to rebuild the natural population of S. younghusbandi in recent years. However, the optimal growth temperature and thermal tolerance of S. younghusbandi has not been studied, which restricts the production of S. younghusbandi fingerling for stock enhancement. The purpose of this paper is to determine the growth, critical thermal maximum (CTMax), lethal thermal maximum (LTMax) and acclimation response ratio (ARR) of S. younghusbandi juveniles (body weight 5.7 ± 1.2 g) at three acclimation temperature levels (10, 15, 20°C). The results showed that acclimation temperature significantly affected the growth, CTMax, LTMax and ARR of the experimental fish. Largest final weight (7.5 ± 2.3 g) was recorded in 15°C group. At a heating rate of 1°C/30 min, CTMax ranged from 30.98 to 32.01°C and LTMax ranged from 31.76 to 32.31°C in the three acclimation temperatures. Schizopygopsis younghusbandi had lower ARR value (0.097) than most other fish species. Low ARR value indicates that S. younghusbandi may have narrower thermal tolerance range and weaker acclimation ability to global warming. For successful aquaculture of S. younghusbandi juveniles, temperature should be maintained around 15°C.     

Chronic mitochondrial uncoupling treatment prevents acute cold-induced oxidative stress in birds

Endotherms have evolved two major types of thermogenesis that allow them to actively produce heat in response to cold exposure, either through muscular activity (i.e. shivering thermogenesis) or through futile electro-chemical cycles (i.e. non-shivering thermogenesis). Amongst the latter, mitochondrial uncoupling is of key importance because it is suggested to drive heat production at a low cost in terms of oxidative stress. While this has been experimentally shown in mammals, the oxidative stress consequences of cold exposure and mitochondrial uncoupling are clearly less understood in the other class of endotherms, the birds. We compared metabolic and oxidative stress responses of zebra finches chronically treated with or without a chemical mitochondrial uncoupler (2,4-dinitrophenol: DNP), undergoing an acute (24 h) and a chronic (4 weeks) cold exposure (12 °C). We predicted that control birds should present at least a transient elevation of oxidative stress levels in response to cold exposure. This oxidative stress cost should be more pronounced in control birds than in DNP-treated birds, due to their lower basal uncoupling state. Despite similar increase in metabolism, control birds presented elevated levels of DNA oxidative damage in response to acute (but not chronic) cold exposure, while DNP-treated birds did not. Plasma antioxidant capacity decreased overall in response to chronic cold exposure. These results show that acute cold exposure increases oxidative stress in birds. However, uncoupling mitochondrial functioning appears as a putative compensatory mechanism preventing cold-induced oxidative stress. This result confirms previous observations in mice and underlines non-shivering thermogenesis as a putative key mechanism for endotherms in mounting a response to cold at a low oxidative cost.     

Mitochondrial function in Antarctic notothenioid fishes that differ in the expression of oxygen-binding proteins

State III respiration rates were measured in mitochondria isolated from hearts of Antarctic notothenioid fishes that differ in the expression of hemoglobin (Hb) and myoglobin (Mb). Respiration rates were measured at temperatures between 2 and 40°C in Gobionotothen gibberifrons (+Hb/+Mb), Chaenocephalus aceratus (–Hb/–Mb) and Chionodraco rastrospinosus (–Hb/+Mb). Blood osmolarity was measured in all three species and physiological buffers prepared for isolating mitochondria and measuring respiration rates. Respiration rates were higher in mitochondria from G. gibberifrons compared to those from C. aceratus at 2°C, but were similar among all species at temperatures between 10 and 26°C. Respiration rates were significantly lower in icefishes at 35 and 40°C compared to G. gibberifrons. The respiratory control ratio of isolated mitochondria was lower in C. aceratus compared to G. gibberifrons at all temperatures below 35°C. At 35 and 40°C, mitochondria were uncoupled in all species. The Arrhenius break temperature of state III respiration was similar among all three species (30.5 ± 0.9°C) and higher than values previously reported for Antarctic notothenioids, likely due to the higher osmolarity of buffers used in this study. These results suggest that differences in mitochondrial structure, correlated with the expression of oxygen-binding proteins, minimally impact mitochondrial function.     

Growth and physiological responses in largemouth bass populations to environmental warming: Effects of inhabiting chronically heated environments

Ectotherms are susceptible to increasing environmental temperatures associated with anthropogenic warming. Supra-optimum temperatures lead to declining aerobic capacity and can increase exposure to lethal temperatures, resulting in reduced performance. Although the capacity of phenotypic plasticity to minimize the effects of temperature on physiological processes is well studied, evidence of generational changes (e.g. transgenerational plasticity and rapid adaptation) in response to environmental warming is limited in natural populations. We investigated metabolism, growth, and thermal tolerance of largemouth bass (Micropterus salmoides) populations inhabiting thermally altered lakes (i.e. power plant cooling lakes) which have year-round elevated temperature regimes and exhibit supra-optimum temperatures on a yearly basis, and compared these traits with those in largemouth bass populations from ambient lakes. Largemouth bass from ambient and heated groups (n = 3 populations per group) were spawned in an ambient, common garden pond environment, then acclimated to either a normal summertime temperature (24 °C) or a supra-optimum temperature (30 °C). Fish from heated populations had significant reductions in the resting metabolic rate at both temperatures and markedly increased growth rates at 30 °C. By comparing pond-raised fish to fish removed directly from heated lakes, we showed that developmental plasticity played little role in establishing the metabolic rate. A lower resting metabolic rate contributed to an increase in the conversion efficiency of food to biomass of largemouth bass from heated lakes, regardless of temperature. Despite inhabiting heated lakes for many decades, neither critical thermal maximum nor minimum were altered in heated populations when raised in a common garden environment. These results suggest that largemouth bass can lessen sub-lethal effects of warming by altering physiological processes to reduce the impact of warming on aerobic scope and that these changes are generationally transient, but changes in maximum thermal tolerance in response to warming is limited to phenotypic plasticity.     

The thermal tolerance of crown-of-thorns (Acanthaster planci) embryos and bipinnaria larvae: implications for spatial and temporal variation in adult populations

To understand the role of sea temperature on the population biology of the crown-of-thorns sea star Acanthaster planci, the thermal window for embryonic and larval development was investigated. In two experiments, the response of embryos and larvae across 12 temperatures from 19.4 to 36.5 °C was quantified as the percentage of individuals reaching cleavage stage embryos, blastula, gastrula, early-bipinnaria, late-bipinnaria larvae or abnormal. Measurements were made at 7 times up to 72 h post-fertilisation, with the morphometrics of larvae measured in the 72-h sample. Acanthaster planci developed at temperatures between 19.4 and 33.2 °C, with a thermal window for development to the late-bipinnaria stage between 25.6 and 31.6 °C. Development rate, normal development and larval size were optimal at 28.7 °C, with development rates remaining relatively constant up to 31.6 °C. Rates of abnormality increased steadily (early embryonic stages) above 28.7 °C and was 100 % at temperatures approaching 33 °C. These experiments provide a more detailed insight into the response of A. planci developmental stages to temperature. The present day distribution of the species in eastern Australia overlap with the optimal thermal window for development to the late-bipinnaria stage (≈25–32 °C), implying a role of temperature in controlling population distributions and abundances. Despite this, short- or long-term temperature increases may not be a major modulator of the crown-of-thorns recruitment success, population dynamics and distribution in the future as no significant change in development rates, larval survival and growth occurred within this thermal window. Therefore, moderate (1–2 °C) increases in sea temperatures caused by El Niño or near-future ocean warming may not drive an increase in developmental and settlement success. Indeed, without any acclimation to warmer temperatures expected under near-future warming (+2 to 4 °C), climate change could ultimately reduce larval survival due to elevated mortality above the optimal development temperature.     

Effect of salinity on the thermoregulatory behavior of juvenile blue shrimp Litopenaeus stylirostris Stimpson

Preferred temperature (PT) of juveniles of Litopenaeus stylirostris was not modified (P>0.05) by salinity. The final preferendum of juveniles was 27.8 °C.The critical thermal maxima (CTMax) determined at 42 combinations (6 temperatures×7 salinities) in blue shrimp was not affected significantly by salinity (P>0.05). We obtained a direct relationship between the CTMax and the acclimation temperature.The end point of CTMax in L. stylirostris was defined as the loss of righting response (LRR).The acclimation response ratio (ARR) for the juveniles of blue shrimp had an interval of 0.45–0.50, values that agreed with others obtained for crustaceans from tropical and sub tropical climates.