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North cod populations face a loss of habitat if global warming exceeds 1.5 ° C


Rapid climate change in the northeastern Atlantic and the Arctic poses a threat to some of the world's largest fish stocks. Impacts of warming and acidification can be accessed through risk-based mechanisms and suitability suitability projects in the future. It turns out that acidification of the oceans causes a narrowing of the embryonic temperature ranges that determine the suitability of friction habitats as a critical site in historical life for two species of cod. Embryonic tolerance ranges associated with climatic simulations reveal that ever-increasing CO2 emissions [Representative Concentration Pathway (RCP) 8.5] worsening the suitability of the current cod frost environment (Gadus morhua) and polar cod (Boreogadus said) by 2100. Mild warming (RCP4.5) can avert dangerous climate impacts on cod but still there are few places to fend off more vulnerable polar bears that also lose the benefits of the ice-covered ocean. Emissions to RCP2.6, however, support a largely unchanged habitat suitability for both species, indicating that the risks are minimized if the warming is kept "below 2 ° C, if not 1.5 ° C" as shown in the Paris agreement.


Oceane Heating and Acidification (OWA), powered by pure CO2 is expected to limit the survival and reproduction of many marine organisms (1). Current knowledge suggests that the physiological limits of the stage in early life define the vulnerability of species to OWA (2). Worst-case impact scenario studies are important for raising risk awareness and accepting social acceptance for mitigation policy (3). More important, however, is the identification of emission pathways necessary to minimize impacts on hazards and to find potential havens for endangered species that should have priority in conservation (13). Risk assessments based on mechanisms that integrate endangered living conditions and their specific environmental needs into the scenario are hardly available, especially for marine species living in Arctic regions (4, 5).

The Subarctic and the Arctic Sea in Northern Europe (ie the Icelandic Sea, the Norwegian Sea, the East Greenland Sea and the Barents Sea) are assumed to experience higher ocean warmth, acidification and loss of sea ice than most other marine areas on Earth6). These ocean areas – formerly called the Norden7) – are inhabited by highly productive fish stocks, most of which migrate to specific friction sites every year (4). The biophysical characteristics of suitable reproductive habitats support the survival of early stages of life and their dispersal into suitable crèches (8). Considering that fish embryos are often more sensitive to environmental changes than to subsequent stages of life (2), embryonic tolerance may act as a basic limitation for the suitability of the reproduction site. For example, temperature tolerances, which are narrower in fish embryos than in other stages of life, may present a biogeographical restriction (8) and are probably explained by the incomplete development of cardiovascular and other homeostatic systems (9). Ocean acidification (OA) due to increased CO emissions2 levels may worsen the disruption of homeostasis (10), thereby reducing the thermal range (2, 11) and is likely to reduce the suitability for the reproductive site by aggravating the survival of the eggs.

Atlantic cod and polar cod are key members of fish fauna of the northern latitude but differ depending on the thermal affinity and the preference of reproduction (4, 5). Atlantic cod is a "thermal generalist" that captures mild to arctic waters between -1.5 ° and 20 ° C (12). Polar cod is a "heat specialist" that is endemic to high arctic and is rarely found at temperatures above 3 ° C (13). Due to the overlapping temperature intervals of adults and adolescents, both species occur when migrating to feeding in the summer (14). During winter and spring, however, reproduction occurs in separate places with different water temperatures and sea-ice conditions (Figure 1). Given that cod preferably favors warmer waters (3 ° to 7 ° C) than polar cod (-1 ° to 2 ° C), generic species are considered to be particularly vulnerable to climate change (5, 14). Moreover, another indirect threat to the reproduction of polar cod is the loss of sea ice, which serves as a breeding site for larvae and youngsters during spring and summer (5).

Fig. 1 Distribution structures of cod and polar cod in the Norden Sea.

(AND) Cod; (B) Polar cod. The populations of both species are reproduced at specific locations (ie cod: 3 ° to 7 ° C, open water, polar cod: -1 °) in winter and spring (cod: March to May, polar cod: December to March) up to 2 ° C, closed sea ice cover). The green arrows show the dispersion of eggs and larvae driven by the predominant surface currents. During summer, the fodder areas (green shadows) of both species partially overlap, for example, around Svalbardu, the northernmost distribution boundary of cod. The red symbols indicate the origin of the animals (adults) used in this study. Distribution maps were redrawn after (4, 13, 33). NEW, NORTHWEST POLYNYA water; FJL, Franz-Joseph-Land; NZ, Novaya Zemlya.

Aggregation of cod and polar cod – often involving many millions of individuals – are important resources for humans and other marine predators. For example, the Norwegian fishery itself generates annual revenue of USD 800 million (15), while polar cod is an important food for many seabirds and mammals (5). Estimation of the change in the suitability of suitable locations for the occurrence of friction in these focal species is therefore of great socioeconomic significance (4). Embedded OWA embedded functional responses to habitat models can help identify spatial risks and benefits across different emission scenarios, including the goal of limiting global warming to 1.5 ° C above pre-industrial levels (16).

Here we evaluate the embryonic ranges of the temperature tolerance under OA in cod and polar cod. Oxygen consumption rate (MO2) of stage embryos and morphometry of larvae in the lid provide an overview of the energy limitations imposed by OWA. The usefulness of a suitable environment was mapped in the Norden seas under various representative concentration pathways (RCPs) by linking the survival data of eggs with the phase 5 climatic simulations (CMIP5). RCPs assume either "no greenhouse gas mitigation" (RCP8.5), "Intermediate mitigation" (RCP4.5) or "strong mitigation" (RCP2.6). The second scenario was developed to limit the increase in average average surface temperature (averaged over land and sea level) to less than 2 ° C in relation to the reference period 1850-1900 and is appropriate to provide a first estimate of the effects of maintaining global warming on "well below 2 ° C, if not 1.5 ° C ", as stated in the Paris Agreement (16).


Embryonic Oxygen Consumption (MO2) increases with or decreases at the warmest temperatures (cod: ≥9 ° C, polar cod: ≥4.5 ° C, Figures 2, A and B), which is in combination with increased mortality (Figure 3), indicating strong thermal stress. Embryos acclimated to lower temperatures (<9 ° / 4.5 ° C) and elevated Pwhat2 (partial pressure CO2) consumed 10% more oxygen compared to those that were kept under control Pwhat2. This trend was reversed after warming, suggesting that at critical high temperatures, additional Oxygen and related energy requirements could not be achieved under OA conditions, resulting in a decrease in the upper temperature limit of metabolic maintenance. Higher energy requirements at altitude Pwhat2 may result from the cumulative costs of increasing acid base regulation, protein turnover and damage (9, 10). The allocation of energy to sustainable functions should take precedence over growth (17), as evidenced by the CO2– and the induced reduction in the size of larvae in the lid (Figures 2, C to F and Fig. S2). Relative decrease of body surface without larval yolk due to increased Pwhat2 10% for cod (P < 0.001) and 13% for polar cod (P < 0.001), the smallest larvae hatched at the warmest temperature (Figures 2, C and D and Table S1). Reducing larva size and dry weight (Figures 2, E and F and Table S1) are consistent with CO2-reduces the redistribution of energy from growth, which is also reflected in other fish species (18).

Figure 2 Effects increased Pwhat2 on the temperature of oxygen consumption (MO2) and cod embryos and pollen embryos (right).

(AND and B). MO2 was measured in embryonic embryos (Figure). Symbols are means (± SEM displayed as bars, n = 6 or 4). The power curves (lines) are based on n = 28 data points. Dark and light shadows show 90% and 95% of Bayesian credible confidence intervals. (C and D) The incidence of yolk free body area in the hatch was evaluated as an indicator of somatic growth and recovery (yolk). Plots folded with individual values ​​display the 25th, 50th and 75th percentiles; whiskers indicate 95% confidence intervals. (D) Sufficient sample sizes were not available at 6 ° C because most individuals died or slipped. (E and F) Offsets between regression lines (with 95% confidence intervals) indicate CO2(the relationship between the size and weight of newly hatched larvae (image)). Individuals were collected at temperature treatments (E: 0 ° to 12 ° C, F: 0 ° to 3 ° C). (A to F) Significant main effects of temperature, Pwhat2, or their interaction (T * * * Pwhat2) are marked with black ★, while orange ★ indicates significant CO2 effects on temperature treatments (Tukey post hoc test, n = 6 or 4 for treatment). For detailed information on the statistical tests, see Table S1. N.a., is not available.

Figure 3 Effects increased Pwhat2 the temperature-dependent survival of eggs in cod and polar cod.

(AND) Cod; (B) Polar cod. The symbols represent means (± SEM displayed as bars, n = 6). Thermal performance curves (TPC, line) of each type are based on n = 36 data points. Dark and light shadows show 90% and 95% of Bayesian credible confidence intervals. TPCs were extrapolated to temperatures below the warming point by incorporating the frost tolerance thresholds from the literature (materials and methods). Significant major effects of temperatures, Pwhat2, or their interaction (T * * * Pwhat2) are marked with black ★, while orange ★ indicates significant CO2 effects on temperature treatments (Tukey post hoc test, n = 6 or 4 for treatment). For detailed information on the statistical tests, see Table S1.

Ovulation survival has fallen below the preferred cod frying temperatures (≤0 ° and ≥9 ° C) and polar cod (≥3 ° C), in particular under the influence of increased Pwhat2 (Figure 3 and Table S1). Accordingly, our results confirm that the range of embryonic tolerances represents a severe limitation in the field of cod reproduction of cod and polar cod. WHAT2(6 ° C, Figure 3A) than polar cod (0 ° to 1.5 ° C, Figure 3B). This observation corresponds to the CO variation2 susceptibility reported by earlier studies of fish early life stages that were tested for OWA effects only under optimal temperature conditions (18). However, for both species there was a similar CO2(-48% at 9 ° C for cod and -67% at 3 ° C for polar cod). Increased thermal sensitivity of the embryos under the projection Pwhat2 the level of the tolerance range and thus the species reproduction niche (2). As a result, the spatial range of the heat-suited environment for cod and polar cod friction can not be shifted to higher latitudes, but also as a result of OWA.

Compared to the current (known) cod and polar cod codons in the study area (blue areas in Figure 1, yellow dashed areas in Figure 4), our basic simulations (1985-2004) indicate that friction occurs exclusively in within the optimal temperature range of the embryo development [>90% potential egg survival (PES), Fig. 4]. However, the area of ​​heat-suited breeding medium (PES> 90%) is larger than the area where friction actually occurs. E.g. Despite favorable temperatures, cod flies are not fished in the northeast Barents Sea (19), indicating that the suitability of the friction station also depends on factors other than the temperature. Mechanisms that exclude certain sites from friction may include aberrant dispersion of eggs and larvae, unfavorable feeding conditions, and predatory pressure (8, 19).

Fig. 4 Current (default) suitable location for cod and pollack in the Norden Sea.

(AND) Cod; (B) Polar cod. The usefulness of a suitable environment is expressed as PES (% PES, color coded) by the combination of experimental survival data (Figure 3) with the WOA13 temperature range (1 ° × 1 °, 50 m above sea level) for the initial period 1984-2005. The values ​​are averaged over the reproduction seasons (cod: March to May, polar cod: December to March) and refers to the places where the friction was recorded[yellowinterruptedareas([yellowdashedareas([žlutépřerušovanéoblasti([yellowdashedareas(13, 33)]. The spatial range of the heat-suited environment (PES> 90%) is typically greater than the "realized reproduction space" because other limiting factors are not taken into account. The dotted purple lines indicate the relative seating positions of the sea ice (defined as areas with ice concentrations> 70%, note that the sea ice boundaries vary slightly between different species due to different annual reproduction seasons).

Until 2100, immature OWA (RCP8.5) is expected to cause a significant decrease in PES at the main reproduction sites of both species (Figures 5, A through C). For cod, it is assumed that PES will decrease around Iceland (-10 to -40%) and Faroe Islands (-20 to -60%) and across the Norwegian coast (-20 to -60%), including the most important friction points on the Lofoten archipelago (at 68 ° N, Figure 5A). Extensive shelf areas outside Svalbard and the northeastern Barents Sea will become more suitable (PES, +10 to + 60%) due to warming and lowering of sea ice coverage. However, the potential gains of habitats in the North are limited by the reduced tolerance of cod embryos under OA conditions and possibly by unknown limitation factors (see above). Under the RCP4.5, declines in PES for cod in some southern places (eg Faroe Islands: -10 to -40%) predominate the thermal benefits (PES, + 20 to + 60%) in the Barents northeast (between Svalbard, Franz Josef Land and Novaya Zemlya, Figures 5, D and F).

Fig. 5 Change of the heat-suited reproductive environment for cod (left) and polar cod (on the right) in the Norden seas under the RCP.

(AND on C) RCP8.5: Unbated OWA. (D on F) RCP4.5: Intermediate (no acidification). (G on AND) RCP2.6: Less than 2 ° C global warming (not acidification). The maps show a shift in PES between the baseline period (1985-2004, cod cod season: March to May, polar cod fowl period: December to March, see Figure 3) and the median of the CMIP5 multimodal projection (seasonal surface temperature, 0 to 50 m, see materials and methods) at the end of this century (2081-2100). Black shading indicates areas (cells, 1 ° × 1 °) with high uncertainty (i.e., the PES shift within that cell is smaller than the CMIP5 layout, see materials and methods). The colored purple lines represent the position of sea ice edges in the relevant species friction period (defined as areas with ice concentration> 70%). (C, F, and I) For each map, values ​​(change in PES) of individual cells are summed according to kernel density estimates, the width corresponds to the relative occurrence of the values. Box charts display the 25th, 50th and 75th percentiles; hair ends indicate 95% intervals.

Polar cod is likely to experience the most dramatic losses of the breeding environment south of Svalbard and Novaya Zemlya (PES, -40 to -80%, RCP8.5, Figure 5B). In addition, polar cod loses most of its bogged habitats, except for a small shelter on the East Greenland shelf (Figure 5B). Even OA-free warming (RCP4.5, Figures 5, E and F) significantly reduces the suitability of important reproducible polar grass stations outside Svalbard (PES, -20 to -60%) and Novaya Zemlya (PES, 40%). The wider loss of sea ice under the RCP8.5 and RCP4.5 scenarios can indirectly affect the reproductive success of the Polar cod, since ice protects adults from passing and serves as a feedstock for an early stage (5). Limiting global warming to about 1.5 ° C above pre-industrialization levels (ie Medium Temperature RCP2.6) can not only minimize PES reduction in the current core areas of both species to less than 10% (Figures 5, G to I), but also maintain some sea ice coverage.


Our projections suggest that OWA's impact on egg survival and subsequent changes in suitability may be the primary determinants of climate dependencies on cod and polar cod. The current findings are consistent with the hypothesis that the tolerance temperature ranges and embryonic habitat of both species are compressed by a progressive OWA2). Our findings also confirm the idea that immediate climate change is an existential threat to cold-treated species such as polar cod20), although we have identified this species in a cold refuge in the High Arctic. Atlantic cod can follow shading of its thermal optimum, which is likely to lead to the establishment of this commercially significant species in areas currently dominated by polar cod. The parallel decline in the desirability of locations outside Iceland and the Norwegian coast (within RCP8.5) means that by 2100, the cod may not be possible in the south of the Arctic Circle (eg South of Lofoten). Potential movements of commercially significant fish stocks across management boundaries and exclusive economic zones are major problems not only for national fishermen and nature conservation (5) but also to international bodies and regulations aimed at preventing resource over-exploitation, resource conflicts and the degradation of untouched ecosystems in the Arctic (4, 21).

However, if global warming is limited to 1.5 ° C above pre-industrial levels, it is unlikely that the changes in the thermal suitability of existing reproduction sites will exceed the critical cod and polar value thresholds. Residual risks can be further reduced as both species can potentially adapt to climate change by responding (i) to shifts in timing and / or friction locations in current areas (22) or (ii) via transgenerational processes that increase physiological tolerance (23). Uncertainties in our results also concern (iii) the reliability and resolution of CMIP5 climate projections (24).

First, the time window for friction in the north is limited to late winter and spring due to extreme seasonal light and associated primary production (feed for planktonic larvae) at high latitudes (> 60 ° N) (22). Significant changes in feminine friction are therefore unlikely to occur in this area. Instead, the Northern expansion of friction during the historical and ongoing warming is well documented, especially for cod, which has prolonged its friction activity at West Svalbard in the 1930s (25). Kernel breeding areas (such as the Lofoten Archipelago for the Barents Sea population) have always been occupied in the past centuries, perhaps due to favorable combinations of biotic and abiotic factors that maximize recruitment success (8, 22). After splitting, the distribution of eggs and larvae plays an important role in offspring – sometimes over hundreds of kilometers – in terms of life cycle connectivity and population replenishment (8). Friction in alternative locations (as required by RCP8.5 for both species and under RCP4.5 for polar cod) could interfere with interconnection, thereby increasing the risk of advent losses and recruitment failure (8). Successful establishment of new breeding habitats will largely depend on a number of factors other than egg survival (ie prey availability, predatory pressure and connectivity), which are currently difficult to predict (2, 22).

Second, our results assume that the range of embryonic tolerances is constant across populations and generations (ie, no evolutionary change during this century). These assumptions are supported by experimental data[seemstobetheoptimaltemperatureandthedevelopmentofvarioussourcesandthegeneral[egsimilartemperatureoptimaforeggdevelopmentamongdifferentAtlanticcodpopulations([napřpodobnáoptimálníteplotaprovývojvajecmezirůznýmipopulacemitreskyobecné([egsimilartemperatureoptimaforeggdevelopmentamongdifferentAtlanticcodpopulations(26); see also Figure S1], as well as field observations[suchasthepersistentdisplacementofthereporttotheforwarding/forwardingtemplate([egconsistentnorthwardshiftofcodspawningactivityresponseetoprevious/ongoingwarming([napřtrvalýposunaktivitytreskytreskysměremnasevervreakcinapředchozí/probíhajícíoteplování([egconsistentnorthwardshiftofcodspawningactivityinresponsetoprevious/ongoingwarming(17)]and phylogenetic analysis of heat tolerance in seafood[eg<01°Cchangeoverto1milion([eg<01°Cchangeinthermaltoleranceper1millionyears([např<01°Czměnatepelnétolerancena1miliónlet([eg<01°Cchangeinthermaltoleranceper1millionyears(27)]. Transgenerational Plasticity (TGP) can support short-term adaptation to environmental changes through nongenical heritage (eg Mothers Transfer) (23). However, unlike the TGP theory, experiments on Atlantic cod suggest that egg life is disturbed during similar degrees of warmth if women are exposed to heat during gonads maturation (28). This example of negative TGP corresponds to most (57%) of TGP studies in fish that scored neutral (33%) or negative (24%) responses (29). Given the limited capacity of short-term adaptation, it is most likely that species will leave their traditional habitat once the physiological limits have been exceeded (2). That is why our results identify not only high-risk areas but also potential havens that should take priority over the implementation of marine reserves.

Thirdly, CMIP5 climate projections include uncertainties (24). To some extent, these uncertainties can be reduced and assessed by considering the results of the multimodel (see materials and methods). Coastal habitats are poorly represented in current global climate models (24). Confidence in weather forecasts for these areas could be improved in future studies, most elegantly using global multiresolutionary ocean models with unstructured meshes (30).

In light of embryonic intolerance to OWA, we show that with undamaged greenhouse gas emissions, large areas currently used for reproduction will become less suitable for recruiting cod and polar cod, which is likely to lead to cascading impacts on Arctic Food Networks, and related ecosystem services4, 5). However, the results of our research also point out that mitigation measures, as the Paris Treaty has undertaken, can improve the effects of climate change on both species. Given that the current CO2 Emission Trajectories provide a 1% chance of limiting global warming to 1.5 ° C above pre-industrial levels (31), our results require an immediate reduction of emissions by 1.5 ° C warming-compatible scenarios to avoid irreversible damage to the Arctic ecosystem and elsewhere.



Atlantic cod was captured in March 2014 in the southern Barents Sea (Tromsøflaket: 70 ° 28'00 "N, 18 ° 00'00" east longitude). Ripe fish were transported to marine aquaculture centers (Nofima AS, Tromsø, Norway) and kept in a flow tank (25 m3) under the ambient light, salinity [34 practical salinity units (PSU)], and temperature conditions (5 ° ± 0.5 ° C). Polar cod was caught in Kongsfjorden (Western Svalbard: 78 ° 95 & 029 ° N, 11 ° 99 & 84 ° E) by trawl in January 2014. Selected fish were kept in flow tanks (0.5 m3) and relocated to the Karvoka aquaculture research station (NOFIMA, Norway University of UiT, Tromsø). At the station the fish were kept in a flow tank (2 m3) at a water temperature of 3 ° ± 0.3 ° C (34 PSU) and complete darkness. In both experiments, gametes used for in vitro fertilization are harvested from the belts n = 13 (Polar cod: 12) Men and n = 6 women (Table S2).

Fertilizer protocol

All fertilization was done within 30 minutes after stripping. Each dose of eggs was divided into half and fertilized by filtered and ultraviolet (UV) sterilized seawater (34 PSU) which was pre-set to keep broiler (cod: 5 ° C, polar cod: 3 ° C) and two different Pwhat2 conditions[management[control[řízení[controlPwhat2: 400 μm, pH(Free scale) 8.15; high Pwhat2: 1100 μm, pHF 7.77]. Standardized protocol for dry fertilization with aliquots of n = 3 men were used to maximize the success of fertilization (32).

Success of fertilization

The success of fertilization was assessed in partial samples (3 × 100 eggs per dose a Pwhat2 ) which were incubated in closed Petri dishes up to 8/16 cells (Atlantic cod: 12 hours, 5 ° C, polar cod: 24 hours, 3 ° C) and photographed under stereomicroscope for subsequent evaluation (Table S3). These images were also used to determine the average egg batch diameter (30 eggs per dose, Table S3).

Incubation settings

According to different mowing periods, both experiments could be conducted sequentially with the same experimental arrangement in 2014 (polar cod: February to April, Atlantic cod: April to May). Eggs that were previously fertilized, either in control or high Pwhat2 were maintained on the relevant CO2 (cod: 0 °, 3 °, 6 °, 9 ° and 12 ° C, polar cod: 0 °, 1.5 °, 3 °, 4.5 °, and 6 ° C). The temperature ranges were selected to cover the preference of cod friction (3 ° to 7 ° C) (33) and polar cod (≤ 2 ° C) (13) and assumed warming scenarios for the region. Each egg dose treatment group was divided into two stagnant incubators (20 incubators per female, 120 in each experiment). In order to avoid survival, only one of the two incubators was used to evaluate the survival of the eggs (and the morphometry of the larvae in the hatch), while the partial samples required for the embryonic MO2 measurements were made from the second incubator.

Initially, all incubators (1000 ml capacity) were filled with filtered (0.2 μm) and UV-sterilized seawater (34 PSU) adjusted to the appropriate fertilization treatment and stocked with positive hovering eggs. With regard to the supply of oxygen in a standing incubator, it is important to ensure that the eggs have enough space to arrange them in one layer under the water surface. Therefore, we have adjusted the number of eggs per incubator (cod: ~ 300 to 500, polar cod: ~ 200 to 300) according to the egg difference between cod (~ 1.45 mm) and polar cod (~ 1.65 mm). The loaded incubators were then placed in variously thermostated baths with sea water (volume, 400 liters) to ensure a smooth temperature change within the incubator. Translucent, lower leg incubators were sealed with polystyrene cover to prevent CO2 degassing and temperature fluctuations. Under natural light regimes, cod eggs were reduced by light with a daylight rhythm of 8 hours of light / 16 hours of darkness, and polar cod eggs were kept in the dark with the exception of shaded light during manipulation. Every 24 hours, 90% of the volume of water in each incubator was replaced by filtered (0.2 μm) and UV-sterilized seawater to prevent oxygen depletion. On the underside of the incubators a drain valve was mounted so that the sea water crawled with dead eggs that had lost buoyancy and descended. Each seawater bath contained two 60-liter tank containers that were used to pre-adjust the seawater to the temperature and Pwhat2 conditions. Water temperatures inside the water baths were controlled by thermostats and recorded automatically every 15 minutes (± 0.1 ° C) via a multi-channel aquarium computer (IKS-Aquastar, IKS Systems, Germany). Future Pwhat2 conditions were determined by injection of pure CO2 gas into submerged tank containers of 60 liters at each temperature. To control the pH of the water, a multichannel feedback system (IKS-Aquastar) connected to individual pH probes (IKS-Aquastar) and solenoid valves Pwhat2 values. The Pwhat2 reservoir tank was measured in situ prior to each change of water with infrared radiation Pwhat2 probe (Vaisala GMP 343, manual temperature compensation, accuracy ± 5 μm, Vaisala, Finland). The probe was equipped with a MI70 reader and a suction pump that was connected to a degassing membrane (G541, Liqui-Cel, 3M, USA) for measuring Pwhat2 in air that is equilibrated to gases from dissolved water (34). Calibration at the factory was confirmed by measuring sea water previously bubbled through the gas mixture (1000 μm CO2 in air, Air Liquide, Germany). Před každodenní výměnou vody byly hodnoty pH zásobníkových nádrží měřeny laboratorní elektrodou pH na tři desetinná místa (Mettler Toledo InLab Routine Pt 1000 s teplotní kompenzací, Mettler Toledo, Švýcarsko), který byl připojen k hodnotě pH WTW 3310 Metr. Dvoubodová kalibrace s nárazníky NBS (National Bureau of Standards) byla provedena denně. Převedení NBS na volnou stupnici koncentrace protonů pro pH mořské vody (35) byla elektroda kalibrována tlmivými roztoky tris-HCl z mořských řas (36), které byly před každým měřením aklimatizovány na odpovídající inkubační teplotu. Hodnoty pH mořské vody se vztahují k volné hodnotě pH (pHF) v tomto rukopisu. Parametry mořské vody jsou shrnuty na obr. S3.

Přežití vajec

Úmrtnost vajec byla zaznamenána 24 hodin, dokud všechny jedinci v inkubátoru buď nezemřeli, nebo vylíhli (obr. S4). Jakmile začalo líhnutí, byly rány shromažďovány volně plavecké larvy, byly eutanazovány předávkováním tricain-methansulfonátu (MS-222) a po vizuálním vyšetření byly po stereomikroskopu počítány morfologické deformace. Výskyt larválních deformací byl kvantifikován jako procento mláďat, které vykazovaly silné deformace žloutkového vaku, lebky nebo páteře. Přežívání vajíček bylo definováno jako procentní podíl nezralých, životaschopných larv, které se vylíhly z počátečního počtu oplodněných vajec (obr. S5). Podíl oplodněných vajec v inkubátoru byl odhadnut z průměrného úspěchu hnojení příslušné šarže vajec (tabulka S3).


Míra spotřeby kyslíku (MÓ2) embryí v očích (při 50% pigmentaci očí, obr. S4) byly měřeny v uzavřených komorách pro dýchání s řízenou teplotou (OXY0 41 A, Collotec Meßtechnik GmbH, Německo). Dvoustěnné komory byly připojeny k průtokovému termostatu pro nastavení teploty dýchací komory na odpovídající inkubační teplotu vajíček. Měření byla prováděna ve třech opakováních s 10 až 20 vajíčky každé ženské a kombinace léčby. Vejce byly umístěny do komory s objemem 1 ml sterilizované mořské vody upravené na odpovídající Pwhat2 léčba. Magnetický mikrospotřebič (3 mm) byl umístěn pod plovoucí vejce, aby se zabránilo stratifikaci kyslíku v dýchací komoře. The change in oxygen saturation was detected by micro-optodes (fiber-optic microsensor, flat broken tip, diameter: 140 μm, PreSens GmbH, Germany) connected to a Microx TX3 (PreSens GmbH, Germany). Recordings were stopped as soon as the oxygen saturation declined below 80% air saturation. Subsequently, the water volume of the respiration chamber and wet weight of the measured eggs (gww) were determined by weighing (±1 mg). Oxygen consumption was expressed as[nmolO[nmolO[nmolO[nmolO2 (gww * min)−1]and corrected for bacterial oxygen consumption (<5%) and optode drift, which was determined by blank measurements before and after three successive egg respiration measurements.

Larval morphometrics

Subsamples of 10 to 30 nonmalformed larvae from each female and treatment combination were photographed for subsequent measurements of larval morphometrics (standard length, yolk-free body area, total body area, and yolk sac area) using Olympus image analysis software (Stream Essentials, Olympus, Tokyo, Japan). Only samples obtained from the same daily cohort (during peak hatch at each temperature treatment) were used for statistical comparison. After being photographed, 10 to 20 larvae were freeze dried to determine individual dry weights (±0.1 μg, XP6U Micro Comparator, Mettler Toledo, Columbus, OH, USA). Replicates with less than 10 nonmalformed larvae were precluded from statistical analyses.

Statistical analysis

Statistics were conducted with the open source software R, version 3.3.3 ( Linear mixed effect models[package“lme4”([package“lme4”([package“lme4”([package“lme4”(37)]were used to analyze data on egg survival and MÓ2. In each case, we treated different levels of temperature and Pwhat2 as fixed factors and included “female” (egg batch) as a random effect. Differences in larval morphometrics (yolk-free body area, total body area, dry weight, standard length, and yolk sac area) were determined by multifactorial analysis of covariance. These models were run with temperature and Pwhat2 as fixed factors and egg diameter as a covariate. Levene’s and Shapiro-Wilk methods confirmed normality and homoscedasticity, respectively. The package “lsmeans” (38) was used for pairwise comparisons (P values were adjusted according to Tukey’s post hoc test method). All data are presented as means (± SEM) and statistical tests with P < 0.05 were considered significant. Results are summarized in table S1.

Curve fitting

Generalized additive models[package“mgcv”([package“mgcv”([package“mgcv”([package“mgcv”(39)]were used to fit temperature-dependent curves of successful development building on egg survival and MÓ2. This method has the benefit of avoiding a priori assumptions about the shape of the performance curve, which is crucial in assessing the impact of elevated Pwhat2 on thermal sensitivity. “Betar” and “Gaussian” error distributions were used for egg survival and MÓ2 data, respectively. To avoid overfitting, the complexity of the curve (i.e., the number of degrees of freedom) was determined by penalized regression splines and generalized cross-validation (39). Models of egg survival were constrained at thermal minima because eggs of cold-water fish can survive subzero temperatures far below any applicable in rearing practice. Following Niehaus et al. (40), we forced each model with artificial zero values (n = 6) based on absolute cold limits from the literature. These limits were set to −4°C for Atlantic cod (41) and −9°C for Polar cod assuming similar freezing resistance, as reported for another ice-associated fish species from Antarctica (42).

Spawning habitat maps

Fitted treatment effects on normalized egg survival data (fig. S6A; raw data are shown in Fig. 3) were linked to climate projections for the Seas of Norden to infer spatially explicit changes in the maximum PES under different RCPs. That is, the treatment fits were evaluated for gridded upper-ocean water temperatures (monthly averages) bilinearly interpolated to a horizontal resolution of 1° × 1° and a vertical resolution of 10 m. To account for species-specific reproduction behavior, we first constrained each map according to spawning seasonality and depth preferences reported for Atlantic cod[MarchtoMay50to400m([MarchtoMay50to400m([MarchtoMay50to400m([MarchtoMay50to400m(33)]and Polar cod[DecembertoMarch5to400m([DecembertoMarch5to400m([DecembertoMarch5to400m([DecembertoMarch5to400m(13)]. As both species produce pelagic eggs that immediately ascend into the upper mixed layer if spawned at greater depths (13, 33), we further limited the eligible depth range to the upper 50 m. PES at a given latitude and longitude was then estimated from the calculations by selecting the value at the depth of maximum egg survival (at 0 to 50 m depth). Egg dispersal was not considered since the major bulk of temperature- and acidification-related mortality occurs during the first week of development (fig. S4).

Oceanic conditions were expressed as climatological averages of water temperatures, sea-ice concentrations, and the pH of surface water. Our observational baseline is represented by monthly water temperatures[WOA13([WOA13([WOA13([WOA13(43)]and sea-ice concentrations[HadISST([HadISST([HadISST([HadISST(44)], averaged from 1985 to 2004, and by pH values averaged over the period 1972–2013[GLODAPv2([GLODAPv2([GLODAPv2([GLODAPv2(45, 46)]. Simulated ocean climate conditions were expressed as 20-year averages of monthly seawater temperatures and sea-ice concentrations and of 20-year averages of annual pH values of surface water. End-of-century projections were derived from climate simulations for 2081–2100 carried out in CMIP5 (45). We considered only those 10 ensemble members (see table S4) that provide data on each of the relevant parameters (water temperature, sea ice, and pH) under RCP8.5, RCP4.5, and RCP2.6 (47). Projected pH values and temperatures are shown in fig. S6 (E to L). To account for potential model biases, we diagnosed for each of the 10 CMIP5 models the differences between simulations and observations for the baseline period and subtracted these anomalies from the CMIP5-RCP results for 2081–2100. For 2081–2100, we considered the CMIP5-RCPs ensemble median of maximum PES and assessed the uncertainty of PES at a given location by defining a signal-to-noise ratio that relates the temporal change in PES between 2081–2100 and 1985–2004 (ΔPES) to the median absolute deviation (MAD) of results for 2081–2100. Model results are not robust where the temporal change in PES is smaller than the ensemble spread, i.e., ΔPES/MAD < 1. PES calculations for scenarios RCP2.6 and RCP4.5 were carried out for Pwhat2 = 400 μatm. The effect of elevated Pwhat2 (1100 μatm) on PES was only considered under scenario RCP8.5.


Supplementary material for this article is available at

Fig. S1 Thermal niches of adult Atlantic cod and Polar cod.

Fig. S2 Treatment effects on larval morphometrics at hatch.

Fig. S3. Water quality measurements.

Fig. S4. Effects of temperature and Pwhat2 on daily mortality rates of Atlantic cod and Polar cod.

Fig. S5. Effects of temperature and Pwhat2 on embryonic development of Atlantic cod and Polar cod.

Fig. S6. Spawning habitat maps for Atlantic cod and Polar cod are based on experimental egg survival data and climate projections under different emission scenarios.

Table S1. Summary table for statistical analyses conducted on data presented in Figs. 2 and 3 of the main text and in figs. S1 and S5.

Table S2. Length and weight of female and male Atlantic cod and Polar cod used for strip spawning and artificial fertilization.

Table S3. Mean egg diameter and fertilization success of egg batches (±SD, n = 3) produced by different females (n = 6).

Table S4. List of CMIP5 models that met the requirements for this study (for details, see the “Spawning habitat maps” section in the main text).

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This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is No for commercial advantage and provided the original work is properly cited.


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Acknowledgments: We acknowledge the support of S. Hardenberg, E. Leo, M. Stiasny, C. Clemmensen, G. Göttler, F. Mark, and C. Bridges. Special thanks are dedicated to the staff of the Tromsø Aquaculture Research Station and the Centre for Marine Aquaculture. Funding: Funding was received from the research program BIOACID [Biological Impacts of Ocean Acidification by the German Federal Ministry of Education and Research (BMBF), FKZ 03F0655B to H.-O.P. and FKZ 03F0728B to D.S.]. Funding was also received from AQUAculture infrastructures for EXCELlence in European fish research (AQUAEXCEL, TNA 0092/06/08/21 to D.S.). F.T.D., M.B., H.-O.P., and D.S. were supported by the PACES (Polar Regions and Coasts in a Changing Earth System) program of the Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research (AWI). Previous and additional support from grants POLARIZATION (Norwegian Research Council grant no. 214184 to J.N.) and METAFISCH (BMBF grant no. FZK01LS1604A to H.-O.P. and F.T.D.) are also acknowledged. Author contributions: F.T.D. and D.S. devised the study and designed the experiments. F.T.D. conducted the experiments. J.N., V.P., and A.M. provided equipment and facility infrastructure. F.T.D. analyzed the experimental data. M.B. analyzed climate data and generated habitat maps. F.T.D. drafted the manuscript. F.T.D., D.S., M.B., and H.-O.P. wrote the manuscript. J.N., V.P., and A.M. edited the manuscript. Competing interests: The authors declare that they have no competing interests. Data and materials availability: All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. Additional data related to this paper may be requested from the authors. The experimental data supporting the findings of this study are available from PANGEA (, a member of the ICSU World Data System.

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