No abstract

Acidification narrows thermal ranges of Arctic fish embryos and thereby constraints reproductive opportunities in a warming ocean.

Background: Hypercapnia and elevated temperatures resulting from climate change may have adverse consequences for many marine organisms. While diverse physiological and ecological effects have been identified, changes in those molecular mechanisms, which shape the physiological phenotype of a species and limit its capacity to compensate, remain poorly understood. Here, we use global gene expression profiling through RNA-Sequencing to study the transcriptional responses to ocean acidification and warming in gills of the boreal spider crab Hyas araneus exposed medium-term (10 weeks) to intermediate (1,120 μatm) and high (1,960 μatm) PCO 2 at different temperatures (5°C and 10°C).Results: The analyses reveal shifts in steady state gene expression from control to intermediate and from intermediate to high CO 2 exposures. At 5°C acid-base, energy metabolism and stress response related genes were upregulated at intermediate PCO 2 , whereas high PCO 2 induced a relative reduction in expression to levels closer to controls. A similar pattern was found at elevated temperature (10°C). There was a strong coordination between acid-base, metabolic and stress-related processes. Hemolymph parameters at intermediate PCO 2 indicate enhanced capacity in acid-base compensation potentially supported by upregulation of a V-ATPase. The likely enhanced energy demand might be met by the upregulation of the electron transport system (ETS), but may lead to increased oxidative stress reflected in upregulated antioxidant defense transcripts. These mechanisms were attenuated by high PCO 2 , possibly as a result of limited acid-base compensation and metabolic down-regulation. Conclusion:Our findings indicate a PCO 2 dependent threshold beyond which compensation by acclimation fails progressively. They also indicate a limited ability of this stenoecious crustacean to compensate for the effects of ocean acidification with and without concomitant warming.

Thermal tolerance windows serve as a powerful tool for estimating the vulnerability of marine species and their life stages to increasing temperature means and extremes. However, it remains uncertain to which extent additional drivers, such as ocean acidification, modify organismal responses to temperature. This study investigated the effects of CO -driven ocean acidification on embryonic thermal sensitivity and performance in Atlantic cod, Gadus morhua, from the Kattegat. Fertilized eggs were exposed to factorial combinations of two PCO conditions (400 μatm vs. 1100 μatm) and five temperature treatments (0, 3, 6, 9 and 12 °C), which allow identifying both lower and upper thermal tolerance thresholds. We quantified hatching success, oxygen consumption (MO ) and mitochondrial functioning of embryos as well as larval morphometrics at hatch and the abundance of acid-base-relevant ionocytes on the yolk sac epithelium of newly hatched larvae. Hatching success was high under ambient spawning conditions (3-6 °C), but decreased towards both cold and warm temperature extremes. Elevated PCO caused a significant decrease in hatching success, particularly at cold (3 and 0 °C) and warm (12 °C) temperatures. Warming imposed limitations to MO and mitochondrial capacities. Elevated PCO stimulated MO at cold and intermediate temperatures, but exacerbated warming-induced constraints on MO , indicating a synergistic interaction with temperature. Mitochondrial functioning was not affected by PCO . Increased MO in response to elevated PCO was paralleled by reduced larval size at hatch. Finally, ionocyte abundance decreased with increasing temperature, but did not differ between PCO treatments. Our results demonstrate increased thermal sensitivity of cod embryos under future PCO conditions and suggest that acclimation to elevated PCO requires reallocation of limited resources at the expense of embryonic growth. We conclude that ocean acidification constrains the thermal performance window of embryos, which has important implication for the susceptibility of cod to projected climate change.

Organisms in all domains, Archaea, Bacteria, and Eukarya will respond to climate change with differential vulnerabilities resulting in shifts in species distribution, coexistence, and interactions. The identification of unifying principles of organism functioning across all domains would facilitate a cause and effect understanding of such changes and their implications for ecosystem shifts. For example, the functional specialization of all organisms in limited temperature ranges leads us to ask for unifying functional reasons. Organisms also specialize in either anoxic or various oxygen ranges, with animals and plants depending on high oxygen levels. Here, we identify thermal ranges, heat limits of growth, and critically low (hypoxic) oxygen concentrations as proxies of tolerance in a meta-analysis of data available for marine organisms, with special reference to domain-specific limits. For an explanation of the patterns and differences observed, we define and quantify a proxy for organismic complexity across species from all domains. Rising complexity causes heat (and hypoxia) tolerances to decrease from Archaea to Bacteria to uni-and then multicellular Eukarya. Within and across domains, taxon-specific tolerance limits likely reflect ultimate evolutionary limits of its species to acclimatization and adaptation. We hypothesize that rising taxon-specific complexities in structure and function constrain organisms to narrower environmental ranges. Low complexity as in Archaea and some Bacteria provide life options in extreme environments. In the warmest oceans, temperature maxima reach and will surpass the permanent limits to the existence of multicellular animals, plants and unicellular phytoplankter. Smaller, less complex unicellular Eukarya, Bacteria, and Archaea will thus benefit and predominate even more in a future, warmer, and hypoxic ocean.

Capacities and effects of cold or warm acclimation were investigated in two zoarcid species from the North Sea (Zoarces viviparus) and the Antarctic (Pachycara brachycephalum) by investigating temperature dependent mitochondrial respiration and activities of citrate synthase (CS) and NADP + -dependent isocitrate dehydrogenase (IDH) in the liver. Antarctic eelpout were acclimated to 5°C and 0°C (controls) for at least 10 months, whereas boreal eelpout, Z. viviparus (North Sea) were acclimated to 5°C and to 10°C (controls). Liver sizes were found to be increased in both species in the cold, with a concomitant rise in liver mitochondrial protein content. As a result, total liver state III rates were elevated in both cold-versus and warm-exposed P. brachycephalum and Z. viviparus, with the highest rates in boreal eelpout acclimated to 5°C. CS and IDH activities in the total liver were similar in Z. viviparus acclimated to 5°C and 10°C, but decreased in those warm acclimated versus control P. brachycephalum. Enzyme capacities in the total liver were higher in eelpout from Antarctica than those from the North Sea. In conclusion, cold compensation of aerobic capacities in the liver seems to be linked to an increase in organ size with unchanged specific mitochondrial protein content. Despite its life in permanently cold climate, P. brachycephalum was able to reduce liver aerobic capacities in warm climate and thus, displayed a capacity for temperature acclimation.

SUMMARYStudies of thermal tolerance in marine ectotherms are key in understanding climate effects on ecosystems; however, tolerance of their larval stages has rarely been analyzed. Larval stages are expected to be particularly sensitive. Thermal stress may affect their potential for dispersal and zoogeographical distribution. A mismatch between oxygen demand and the limited capacity of oxygen supply to tissues has been hypothesized to be the first mechanism restricting survival at thermal extremes. Therefore, thermal tolerance of stage zoea I larvae was examined in two populations of the Chilean kelp crab Taliepus dentatus, which are separated by latitude and the thermal regime. We measured temperature-dependent activity, oxygen consumption, cardiac performance, body mass and the carbon (C) and nitrogen (N) composition in order to: (1) examine thermal effects from organismal to cellular levels, and (2) compare the thermal tolerance of larvae from two environmental temperature regimes. We found that larval performance is affected at thermal extremes indicated by decreases in activity, mainly in maxilliped beat rates, followed by decreases in oxygen consumption rates. Cardiac stroke volume was almost temperature-independent. Through changes in heart rate, cardiac output supported oxygen demand within the thermal window whereas at low and high temperature extremes heart rate declined. The comparison between southern and central populations suggests the adaptation of southern larvae to a colder temperature regime, with higher cardiac outputs due to increased cardiac stroke volumes, larger body sizes but similar body composition as indicated by similar C:N ratios. This limited but clear differentiation of thermal windows between populations allows the species to widen its biogeographical range.

BackgroundOcean acidification and warming are happening fast in the Arctic but little is known about the effects of ocean acidification and warming on the physiological performance and survival of Arctic fish.ResultsIn this study we investigated the metabolic background of performance through analyses of cardiac mitochondrial function in response to control and elevated water temperatures and PCO2 of two gadoid fish species, Polar cod (Boreogadus saida), an endemic Arctic species, and Atlantic cod (Gadus morhua), which is a temperate to cold eurytherm and currently expanding into Arctic waters in the wake of ocean warming. We studied their responses to the above-mentioned drivers and their acclimation potential through analysing the cardiac mitochondrial function in permeabilised cardiac muscle fibres after 4 months of incubation at different temperatures (Polar cod: 0, 3, 6, 8 °C and Atlantic cod: 3, 8, 12, 16 °C), combined with exposure to present (400μatm) and year 2100 (1170μatm) levels of CO2.OXPHOS, proton leak and ATP production efficiency in Polar cod were similar in the groups acclimated at 400μatm and 1170μatm of CO2, while incubation at 8 °C evoked increased proton leak resulting in decreased ATP production efficiency and decreased Complex IV capacity. In contrast, OXPHOS of Atlantic cod increased with temperature without compromising the ATP production efficiency, whereas the combination of high temperature and high PCO2 depressed OXPHOS and ATP production efficiency.ConclusionsPolar cod mitochondrial efficiency decreased at 8 °C while Atlantic cod mitochondria were more resilient to elevated temperature; however, this resilience was constrained by high PCO2. In line with its lower habitat temperature and higher degree of stenothermy, Polar cod has a lower acclimation potential to warming than Atlantic cod.