Sunday , February 28 2021

North hives have a loss of habitat if the global warming exceeds 1.5 ° C


Rapid climate change in the northeast Atlantic and the Arctic pose a threat to some of the world's largest fish populations. The effects of warming and acidification can become available through a risk-based assessment of the mechanism and projections of future benefits for the habitat. We show that the ocean acid causes the embryonic thermal range to be narrowed, which identifies the benefit of the habitat of the cormorant as a critical bottleneck in life for two rich fish species. The extent of embryonic tolerances associated with climatic simulations reveals that there is a growing CO2 emissions [Representative Concentration Pathway (RCP) 8.5] will worsen the convenience of the existing habitat of hijacking for both Atlantic Grants (Gadus morhua) and Polar cod (Boreogadus saida) to 2100. Moderate heating (RCP4.5) can prevent dangerous climatic influences on the Atlantic, but it still leaves several areas of contamination for an even more vulnerable polar torch, which also loses the benefits of the ice ocean. Emissions accompanying RCP2.6, however, support largely unchanged habitat suitability for both species, indicating that risks are minimized if warming is maintained "below 2 ° C, if not 1.5 ° C," as this is stipulated by the Paris Agreement.


Ocean warming and acidification (OWA), driven by neutron CO2 are expected to limit the survival and reproduction of many marine organisms (1). Existing knowledge implies that physiological boundaries of earlier stages of life define vulnerability of species to OWA (2). Impact scenario studies of the worst-case scenario are important for raising awareness of risks and gaining social acceptance of mitigation policies (3). However, it is even more important to identify the emission pathways needed to minimize the risk of impact and to find potential hazards of endangered species that should be given priority in conservation (13). Nevertheless, risk-based assessments based on mechanisms that integrate endangered life stages and their specific habitat needs in the context of scenarios are barely accessible, especially for marine species living in the Arctic regions (4, 5).

It has been projected that subarctic and Arctic sea nuclei around Northern Europe (i.e., the Icelandic Sea, the Norwegian Sea, the East Greenland Sea and the Barents Sea) will experience higher rates of ocean warming, acidification and ice ice loss from most other marine areas on Earth6). These ocean regions – formerly called Seas Norden (7) – are inhabited by a highly productive fish population, most of which make annual migrations to specific locations of the spawn (4). Biophysical characteristics of suitable habitats support the survival of early stages, as well as their dispersion to the corresponding nursery areas (8). Considering that fish embryos are often sensitive to environmental changes from the subsequent life stages (2), embryonic tolerance can act as a fundamental limitation for the convenience of the habitat of standing. For example, the temperature range of tolerance that intensifies in the fish embryo than in other phases of life can be a biogeographical constraint (8) and are probably explained by the incomplete development of cardiovascular and other homeostatic systems (9). Ocean degradation (OA) caused by elevated aqueous CO2 levels may worsen the disorder of homeostasis (10), which narrows the thermal range (2, 11) and possibly reducing the benefits of honeycomb damage by damaging the survival of eggs.

Both Atlantic Atlantic and Polar Granny are key members of the Northern High Geographic Fauna, but differ in terms of thermal affinity and commitment (4, 5). Atlantic cane is a "thermal generalist" that occupies moderate to Arctic waters between -1.5 ° and 20 ° C (12). In contrast, Polar Reed is a "Thermal Specialist", an endemic high Arctic and rarely located at temperatures above 3 ° C (13). Because of the overlapping of the temperature ranges of underage and adult life phases, both species coexist during summer migrations (14). However, during winter and spring, the stench occurs at different locations with different water temperatures and sea ice conditions (Figure 1). Since Atlantic cane prefer hot water (3 ° to 7 ° C) from polar cane (-1 ° to 2 ° C), this second species is considered particularly vulnerable to climate change (5, 14). Moreover, another indirect threat to the polar reproduction of torches is the projected loss of sea ice, which serves as a nursery for larvae and minors during spring and summer (5).

Figure 1 Distribution patterns of Atlantic cane and Polar granny in the Norden seas.

(A) Atlantic; (B) Polar grandmother. Populations of both species are reproduced during winter and spring (Atlantic cod from March to May; Polar code: from December to March) at specific locations (eg, Habitat habitats, areas with blue tinting) with characteristic temperature and sea ice conditions: copper up to 7 ° C, open water, Polar Granule: -1 ° to 2 ° C, closed Ice Ice Cover). Green arrows indicate the dispersion of eggs and larvae affected by the prevailing surface currents. During the summer, the feeding grounds (areas with green shade) are partially overlapping, for example, around Svalbard, which indicates the northernmost border of the Atlantic cane distribution. Red symbols indicate the origin of animals (adult adults) used in this study. Distribution cards have been renamed after (4, 13, 33). NEW, northeast water Polynya; FJL, Franz-Joseph-Land; NZ, Novaya Zemlya.

The occurrence of the Atlantic and Polar reeds – often made up of many millions of people – represent important resources for humans and other marine predators. For example, only fishing in the Norwegian Atlantic race generates an annual income of $ 800 million (15), while Polar cane is the basic food for many seabirds and mammals (5). Estimation of changes in the benefits of habitats for these focal species therefore has a high socio-ecological importance (4). Functional responses from the embryo OWA embedded in habitat models can help identify spatial risks and benefits in different emission scenarios, including the goal of limiting global warming to 1.5 ° C above pre-industrial levels (16).

Here, we estimate the embryonic ranges of thermal tolerance under OA in the Atlantic Race and Polar Color. Oxygen consumption rate (MO2) embryos of the eye and larval morphometrics on the chain provide an insight into the energy constraints imposed by OWA. The habitat of the habitat was mapped across the North under various contextual reference concentrations (RCPs) by linking data on egg survival with climatic simulations of Phase 5 of the CMIP5 project. RCP assumes either "mitigation of gaseous greenhouse gases" (RCP8.5), "moderate mitigation" (RCP4.5) or "strong mitigation" (RCP2.6). The second scenario was developed in order to limit the increase in the global surface temperature of the surface (average on land and sea surface) to below 2 ° C in relation to the reference period 1850-1900 and is suitable for providing the first estimate of the consequences of maintaining global warming up to "significant below 2 ° C, if not 1.5 ° C, as stated in the Paris Agreement (16).


Embryonic consumption of oxygen (MO2) increases with increasing temperature, but leveling or decreasing at the hottest temperatures (Atlantic cane: ≥ 9 ° C; Polar shark: ≥4.5 ° C, Figure 2, A and B), which is combined with increased mortality under this conditions (Figure 3), which indicates a serious stress of heat. Embryos are acclimated at lower temperatures (<9 ° / 4.5 ° C) and elevated Pco2 (partial pressure CO2) consumed ~ 10% more oxygen compared to those under control Pco2. This trend has changed after heating, indicating that additional oxygen and associated energies in OA conditions can not be met at critically high temperatures, leading to a reduction in the upper thermal limit of metabolic maintenance. Higher energy demands have been raised Pco2 can be due to the cumulative costs of increased regulation of the acid base, protein transport and damage repair (9, 10). Energy distribution in life-sustaining functions should have priority over growth (17), as evidenced by the CO2– and a decrease in the size of the larva at the openings caused by heating (Fig. 2, C to F and Fig. S2). Relative reduction of body surface without larva without a yolk due to elevated Pco2 an average of 10% for the Atlantic code (P < 0.001) and 13% for the polar code (P < 0.001), with the smallest larvae at the hottest temperature (Fig. 2, C and D and Table S1). Reducing the size of the larvae and dry weight (Figure 2, E and F and Table S1) are in accordance with CO2– Redistribution of energy away from growth, which can be seen in other fish species (18).

Figure 2 Effects elevated Pco2 temperature dependent oxygen consumption (MO2) and growth of Atlantic embryos and polar embryos (right).

(A i B) MO2 It is measured in embryos of the eye (picture). Symbols are means (± SEM shown as bars, n = 6 or 4). Performance curves (lines) are based on n = 28 data points. Dark and light shadows indicate 90% and 95% Bayes credible confidence intervals, respectively. (C i D) The surface of the larva without rum was not assessed as an indicator of somatic growth and the use of resources (yolk). Boxes with covered individual values ​​show 25, 50 and 75 percentiles; mustache denotes 95% confidence interval. (D) Sufficient sample size was not available at 6 ° C, as most people died or found malformed. (E i F) Offset between regression lines (with 95% confidence intervals) indicates CO2Differences in the relationship between size and weight of newly born larvae (pictures) are associated. Individuals were associated for temperature treatments (E: 0 ° to 12 ° C, F: 0 ° to 3 ° C). (A to F) Significant main effects of temperature, Pco2, or their interaction (T * Pco2) are marked with black ★, while orange ★ marks significant CO2 effects within the treatment temperature (Tukey post hoc test, n = 6 or 4 per treatment). Refer to Table S1 for details on statistical tests. No, it's not available.

Figure 3 Effects elevated Pco2 about survival depending on temperature in the Atlantic race and Polar color.

(A) Atlantic; (B) Polar grandmother. Symbols represent the means (± SEM shown as bars, n = 6). The heat performance curves (TPCs, lines) of each type are based on n = 36 data points. Dark and light shadows indicate 90% and 95% Bayes credible confidence intervals, respectively. TPCs are extrapolated to underground temperatures by introducing thresholds of freezing tolerance from literature (Materials and methods). Significant main effects of temperature, Pco2, or their interaction (T * Pco2) are marked with black ★, while orange ★ marks significant CO2 effects within the treatment temperature (Tukey post hoc test, n = 6 or 4 per treatment). Refer to Table S1 for details on statistical tests.

The survival of eggs decreased beyond the preferred melting temperatures at Atlantic cane (≤0 ° and ≥9 ° C) and Polar Reed (≥3 ° C), especially under the influence of elevated Pco2 (Figure 3 and Table S1). Consequently, our results confirm that the range of embryonic tolerances constitutes a strong impediment to the thermal network of the Atlantic straws and polar copper. CO2Mortality caused by optimal ammunition ammunition temperature was less pronounced in Atlantic cane (6 ° C, Fig. 3A) than in polar reeds (0 ° to 1.5 ° C, Figure 3B). This observation corresponds to variation in CO2 sensitivity reported in previous studies on the early stages of fish that tested OWA effects exclusively under optimal temperature conditions (18). However, both types were similar to CO2(-48% at 9 ° C for Atlantic reed and -67% at 3 ° C for polar torch). Increased thermal sensitivity of the embryo below the projected Pco2 levels involve narrowing their range of thermal tolerance, and therefore reproductive niches of the species (2). As a consequence, the spatial range of thermally suitable standing boats for the boats in the Atlantic and Polar can not only go over to greater latitudes in response to warming, but also to an OWA contract.

Compared with the modern (well-known) Atlanta cane and polar reed marshals in the field of research (blue surfaces in Figure 1, yellow dotted areas in Figure 4), our basic simulations (1985-2004) suggest that spraying occurs exclusively within the thermal optimal range embryo development [>90% potential egg survival (PES), Fig. 4]. However, the area of ​​thermally appropriate horticultural habitats (PES> 90%) is larger than the area where the spawning actually occurs. For example, despite the appropriate temperatures, there is currently no evidence of Atlantic cod smashing in the northeastern Barents Sea (19), which indicates that the benefits of the habitat depend on non-temperature factors. Mechanisms that prevent certain surfaces as suitable for spraying may include unnecessary spread of eggs and larvae, unfavorable feeding conditions, and pressure of the transfer (8, 19).

Figure 4 The current (basic) benefits of a herd habit for the Atlantic cane and polar cod in the Norden seas.

(A) Atlantic; (B) Polar grandmother. The convenience of a standing habitat is expressed as PES (% PES, color coded) by combining experimental survival data (Figure 3) with the temperature field WOA13 (1 ° x 1 °, upper 50 m from the shelves) for the base period 1984-2005. Values ​​are calculated on average during seasons (cod in the Atlantic from March to May, polar code: from December to March), and refer to sites where the horn is documented[yellowpot([yellowdashedareas([žutepukotine([yellowdashedareas(13, 33)]. The spatial range of the heat-suitable livestock habitat (PES> 90%) is usually higher than the "realized livestock habitat" because other limiting factors are not taken into account. Pictured magnetic lines indicate the appropriate seasonal positions of the sea ice (defined as ice-bearing areas> 70%, note that the edge of the sea ice differs slightly between species due to different seasons for certain species.

By 2100, it was projected that the scars of OWA (RCP8.5) would cause a significant drop in PES at the main mating sites of both species (Figure 5, A to C). For the Atlantic reed, the PES is projected to shrink around Iceland (-10 to -40%) and Faroe Islands (-20 to -60%) and along the entire Norwegian coast (-20 to -60%), including the most important sites of hijacking at the Lofoten archipelago (68 ° S, Fig. 5A). In turn, more convenient areas from the Svalbard area and via the northeastern Barents Sea (PES, +10 to + 60%) will become more suitable for heating and reducing sea ice cover. However, the potential gain in habitats in the north is limited by the reduced cold tolerance of the Atlantic cane embryo under OA conditions and, possibly, unknown limitation factors (see above). Under RCP4.5, the reduction of Atlantic cane PES in some southern mourning sites (eg Faroe Islands: -10 to -40%) largely exceeds the thermal benefits (PES, +20 to + 60%) in the northeastern Barents Sea between Svalbard, Franz Josef and Newer Earth, Figures 5, D and F).

Figure 5 Change of the heat-suitable knitting habitat of the Atlantic cane (left) and Polar cane (right) in the Nordena seas under RCPs.

(A it C) RCP8.5: Unused OWA. (D it F) RCP4.5: Medium heating (no acid). (Mr it Yeah) RCP2.6: Global warming below 2 ° C (no acidification is taken into account). The maps show a shift in the PES between the initial period (1985-2004, the Atlantic cane seasoning from March to May, the polarization season for trees from December to March, see Figure 3) and the middle projection based on CMIP5 multimodal (seasonal sea surface temperature of 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 change in PES within that cell is smaller than the CMIP5 Enlargement Envelope, see Materials and Methods). Pictined magnetic lines represent the positions of the sea ice in the appropriate seasonal species specific species (defined as areas with ice concentrations> 70%). (C, F, and I) For each map, the values ​​(change in PES) of individual cells are summarized by kernel density estimates, the width corresponding to the relative occurrence of values. Boxes show the 25th, 50th and 75th percentiles; the ends of the limbs indicate an interval of 95%.

The Polar Bar will most likely experience the most persistent habitat losses in the southwest of Svalbard and Novaya Zemlya (PES, -40 to -80%, RCP8.5, Figure 5B). Moreover, Polar Reeds will lose most of their habitats under the ice, except for a small haven in the East Greenland field (Figure 5B). Even heating without effect of OA (RCP4.5, Figure 5, E and F) will significantly reduce the convenience of significant habitats for polar running Svalbard (PES, -20 to -60%) and Novaya Zemlya (PES, -10 to -40% ). The widespread loss of sea ice under scenarios RCP8.5 and RCP4.5 can indirectly affect the reproductive success of polar cane, as ice protects adult adults from prey and serves as a feeding habit for early stages (5). Restricting global warming to about 1.5 ° C above pre-industrial levels (i.e., mean RCP2.6 temperature) not only minimizes the decrease in PES in the current core of the spraying of both species to less than 10% (Figure 5, G to I) , but also keep a little ice cream cover.


Our projections suggest that the effects of OWA on egg survival and subsequent changes in the benefits of habitat habitations can be the primary determinants of climate-related constraints on the Atlantic and Polar boats. Current findings are consistent with the hypothesis that the thermal range of tolerance and embryonic habitats of both species is compressed with progressive OWA (2). Our results also support the idea that unchanged climate change poses an existential threat to cold-adapted species such as Polar cod (20), although we identified a cold refugium for this species in the High Arctic. The Atlantic cane can track the displacement of the half-heart of its thermal potential, which could lead to the establishment of this commercially important species in the regions currently dominated by Polar Reeds. Parallel reductions in the suitability of habitats from Iceland and the Norwegian coast (under RCP8.5) implies that by 2100 the migration south of the Arctic Circle (eg, South of Lofoten) can no longer be possible for the Atlantic. The potential shifts of commercially important fish stocks across the management boundaries and exclusive economic zones pose great challenges not only to national fishermen and conservators (5) but also to international bodies and regulations that intend to avoid excessive exploitation, resource conflicts and degradation of undiscovered ecosystems in the Arctic (4, 21).

However, if global warming is limited to 1.5 ° C above the level of pre-industrial production, it is likely that changes in the thermal benefits of existing habitats will not exceed the critical limits of the Atlantic cane and Polar Reed. Residual risks can be further reduced as both species can potentially be adapted to climate change by reacting either (i) through shift in time and / or location of the migration within existing regions (22) or (ii) transgenerational processes that increase physiological tolerance (23). The uncertainties in our results also relate to (iii) reliability and resolution of CMIP5 climate projections (24).

First, the temporal window for drifting in the north is limited to late winter-spring due to the extreme seasonality of light and associated primary production (planktonic larvae) in high latitudes (> 60 ° N) (22). Therefore, there will probably not be significant changes in the younger phenology in this region. Instead, the expansion of the horns in the north during the historic and current warming periods have been well documented, especially for the cod of the cod, which expanded its shingles to the Western Swalbard in the 1930s (25). However, the core of the spraying area (eg, the Archipelago Lofoten for the Barents Sea population) has always been occupied over the past centuries, probably thanks to favorable combinations of biotic and abiotic factors that maximize the success of employment (8, 22). After spraying, spreading eggs and larvae to appropriate seedling sites – sometimes over a hundred kilometers – plays an important role in terms of linking the life cycle and filling the population (8). Standing at alternative locations (according to RCP8.5 requirements for both species and under RCP4.5 for Polar Reed) may interfere with the association and thus increase the risk of adverse and job losses (8). Consequently, the successful establishment of new habitats will largely depend on a number of factors, in addition to the survival of eggs (i.e., availabilty of prey, predator pressure and connectivity), and all are currently difficult to predict (2, 22).

Secondly, our results assume that the range of embryonic tolerances is constant in different populations and generations (i.e., there are no evolutionary changes within this century). These assumptions are supported by experimental data[nprslicnetperatureoptimazarrazvojjudurazličitimpopulacijamatrskeuAtlantiku([egsimilartemperatureoptimaforeggdevelopmentamongdifferentAtlanticcodpopulations([nprsličnetemperatureoptimazarazvojjajameđurazličitimpopulacijamatrskeuAtlantiku([egsimilartemperatureoptimaforeggdevelopmentamongdifferentAtlanticcodpopulations(26); see also S1], as well as field observations[egconsistentreclamationoftheactivityofemails[egconsistentnorthwardshiftofcodspawningactivityinresponsetoprevious/ongoingwarming([nprdosljednoprebacivanjeaktivnostimriješenjabodećausjeverukaoodgovornaprethodno/tekućezagrevanje([egconsistentnorthwardshiftofcodspawningactivityinresponsetoprevious/ongoingwarming(17)]and phylogenetic analysis of thermal tolerance in sea fish[eg<01°Cchangedfrom1minuteto1year([eg<01°Cchangeinthermaltoleranceper1millionyears([npr<01°Cpromjenatoplotnetolerancijena1miliongodina([eg<01°Cchangeinthermaltoleranceper1millionyears(27)]. Transgenerational Plasticity (TGP) can promote a short-term adaptation to the environmental change through non-genetic inheritance (eg, Uterine Transmission) (23). However, unlike TGP theory, experiments on Atlantic cod indicate that the jawing ability of the eggs has been reduced during a similar degree of warming if women are exposed to heat during gonad root growth (28). This negative TGP case corresponds to the majority (57%) of TGP studies in fish that observed neutral (33%) or negative (24%) responses (29). Given the limited capacity for short-term adaptation, it is most likely that the species must leave their traditional habitats as soon as the physiological limits are exceeded (2). Consequently, our results identify not only high-risk areas, but also potential protected habitats that should have priority in terms of applying marine reserves.

Third, CMIP5 climate projections include ambiguities (24). To some extent, these uncertainties can be reduced and estimated by considering multimodal results (see Materials and Methods). Coastal habitats are poorly represented in current global climate models (24). The likelihood of climate impact projections for these areas could be improved in future studies, most notably by global multi-oceanic models with unstructured meshes (30).

In the light of embryonic intolerance towards OWA, we show that large greenhouse gas emissions currently used for spraying will become less suitable for the employment of Atlantic cane and Polar Reeds, which could lead to cascading impacts on Arctic food webs and related services ecosystem (4, 5). However, our results also emphasize that mitigation measures, as envisaged by the Paris Agreement, can improve the effects of climate change on both types. Given that the current CO2 emission trajectories yield a 1% chance to limit global warming to 1.5 ° C above the preindustrial level (31), our results require an immediate reduction of the emissions of the following scenarios that are compatible with heating at 1.5 ° C in order to prevent irreversible damage to the ecosystem in the Arctic and elsewhere.



The Atlantic cod was caught in March 2014 in the southern Barentian Sea (Tromsøflaket: 70 ° 28'00 "N, 18 ° 00'00" E). Mature fish is transported to the Marine Aquaculture Center (Nofima AS, Tromsø, Norway) and are kept in a flow reservoir (25 m3) under ambient light, salinity [34 practical salinity units (PSU)], and temperature conditions (5 ° ± 0.5 ° C). Polar cod are captured in Kongsfjorden (Western Svalbard: 78 ° 95 'N ", 11 ° 99'84" E) grass in January 2014. The selected fish were kept in flow reservoirs (0.5 m3) and transferred to the Research Station for aquaculture in Carwich (NOFIMA, Arctic University of Norway UiT, Tromsø). At the station, the fish was kept in a flow reservoir (2 m3) at 3 ° ± 0.3 ° C water temperature (34 PSU) and total darkness. In both experiments, gametes that were used for in vitro fertilizers were obtained from baits n = 13 (Polar cod: 12) men i n = 6 females (Table S2).

Fertilization Protocol

All fertilizers were carried out within 30 minutes after removal. Each egg series was split in half and was fertilized using filtered and ultraviolet (UV) -strozen sea water (34 PSU) previously adapted to the milk holding temperature (Atlantic cod: 5 ° C, Polar cane: 3 ° C) and two different Pco2 conditions[control[control[kontrola[controlPco2: 400 μm, pH(Free Scale) 8.15; high Pco2: 1100 μm, pHF 7.77]. Standardized dry fertilization protocol with aliquots milt of n = 3 males were used to maximize the success of fertilizing (32).

Success of fertilizer

The success of fertilization is estimated in the underground (3 × 100 eggs per batch and Pco2 treatment), incubated in closed petri dishes to the 8/16 cell stage (Atlantic cod: 12 hours, 5 ° C, Polar Reed: 24 hours, 3 ° C) and photographed under a post-mortem estimation stereomicroscope (Table S3). These images were also used to determine the average egg diameter of the egg series (30 eggs per lot, table S3).

Setting incubation

By different seasons, both experiments could be performed sequentially with the same experimental setup in 2014 (Polar COD: February-April, Atlantic: from April to May). Eggs that have been previously fertilized or controlled or high Pco2 were maintained at the appropriate CO2 is treated and incubated to open at five different temperatures (Atlantic cane: 0 °, 3 °, 6 °, 9 ° and 12 ° C; Polar code: 0 °, 1.5 °, 3 °, 4.5 ° and 6 ° ° C). Temperature ranges have been selected to cover the beehives of the preferences of the Atlantic bode (3 ° to 7 ° C) (33) and Polar Granny (≤2 ° C) (13) and projected heating scenarios for a particular region. Each cave group therapy is divided into two stagnant incubators (20 incubators per female, 120 in each experiment). In order not to estimate the survival estimate, only one of the two incubators was used to estimate the survival of eggs (and larval morphometrics at the openings), while the necessary sub-folders for embryonic MO2 measurements were taken from the second incubator.

Initially, all incubators (volume, 1000 ml) were filled with filtered (0.2 μm) and UV sterilized seawater (34 PSU) adapted to the appropriate fertilization treatment and pledged with positive floating eggs. Regarding the supply of oxygen in a stagnant incubator, it is important to ensure that the eggs have enough space to be arranged in one layer below the surface of the water. For this reason we set the amount of eggs per incubator (Atlantic cod: ~ 300 to 500; Polar cod: ~ 200 to 300) according to the differences in the size of the egg between the Atlantic cod (~ 1.45 mm) and the polar cod (~ 1.65 mm) . Closed incubators were then located in various thermostated seawater baths (volume, 400 liters) to ensure a smooth temperature change inside the incubator. Transparent incubators with a lower cone were sealed with a styropor lid to prevent CO2 extinguishing and temperature fluctuations. According to natural light regimes, eggs in the Atlantic can consume dark illumination with a daylight rhythm of 8 hours of light / 16 hours of darkness, and Polar eggs from the cane were dark, except for low illumination during handling. Every 24 hours, 90% of the volume of water in each incubator is replaced by filtered (0.2 μm) and UV sterilization of seawater to avoid the reduction of oxygen. At the bottom of the incubator, a drainage drainage valve with dead eggs was installed, which lost the sailboat and descended to the bottom. Each sea-water bath contained two 60-liter reservoirs used to improve seawater at the right temperature and Pco2 conditions. The water temperatures within the water baths were controlled by the thermostats and automatically recorded every 15 min (± 0.1 ° C) using a multipurpose aquarium (IKS-Aquastar, IKS Systems, Germany). Future Pco2 conditions were established by injection of pure CO2 gas in the submerged reservoirs of the 60 liter fuel tank at each temperature. A multi-channel return system (IKS-Aquastar), coupled to single pH probes (IKS-Aquastar) and an electromagnetic valve, was used to control the water pH and Pco2 values. The Pco2 the tank reservoir was measured in situ before each exchange of water with an infrared color Pco2 probe (Vaisala GMP 343, manual temperature compensation, precision ± 5 μm, Vaisala, Finland). The probe is equipped with MI70 Reading and a discharge pump that is connected to the degassing membrane (G541, Liqui-Cel, 3M, USA) for measuring Pco2 in the air in equilibrium with dissolved aqueous gases (34). Factory calibration was confirmed by sea water measurements previously discharged with a technical gas mixture (1000 μm CO2 in the air, Air Liquide, Germany). Before daily water changes, the pH of the reservoir tank was measured with a laboratory pH electrode at three decimal places (Mettler Toledo InLab Routine Pt 1000 with temperature compensation, Mettler Toledo, Switzerland), which is connected to the WTW 3310 pH meter. Two-point calibration with the National Bureau of Standards was carried out on a daily basis. Convert NBS to a free proton scale concentration for pH of sea water (35), the electrode is calibrated using tris-HCl sea-water wells (36), which are applied to the appropriate incubation temperature before each measurement. PH values ​​of the mixture refer to the free pH scale (pHF) throughout the entire manuscript. The sea water parameters are summarized in Fig. S3.

Survival of eggs

Eat mortality was recorded at 24-hour level until all individuals in the incubator died or died (figure S4). When the exercise began, free-swallow larvae were collected in the morning, euthanized by excessive dosing of methansulphonate tritiine (MS-222) and counted after a visual examination for morphological deformations under the stereomicroscope. The frequency of larval deformities is quantified as a percentage of the spillage that shows severe deformity of the gallbladder, cranium, or vertebrate. Preživljavanje jaja definisano je kao procenat neformalnih, održivih larvi koje se izleglo od početnog broja oplođenih jaja (slika S5). Procenat oplođenih jaja u inkubatoru procijenjen je od srednjeg uspjeha đubrenja odgovarajuće serije jaja (tabela S3).


Stopa potrošnje kiseonika (MO2) očiju embriona očiju (kod 50% pigmentacije očiju, slika S4) merene su u zatvorenim, temperaturno kontrolisanim respiratornim komorama (OXY0 41 A, Collotec Meßtechnik GmbH, Nemačka). Komore sa dvostrukim zidovima bile su povezane sa protočnim termostatom kako bi se temperatura dihalne komore prilagodila odgovarajućoj temperaturi inkubacije jaja. Merenja su sprovedena u tri kopije sa 10 do 20 jaja svake ženske i kombinacijom lečenja. Jaja su postavljena u komoru sa zapreminom od 1 ml sterilisane morske vode prilagođene odgovarajućoj Pco2 liječenje. A magnetic microstirrer (3 mm) was placed underneath the floating eggs to avoid oxygen stratification within the respiration chamber. 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 MO2. In each case, we treated different levels of temperature and Pco2 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 Pco2 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 MO2. 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 Pco2 on thermal sensitivity. “Betar” and “Gaussian” error distributions were used for egg survival and MO2 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 Pco2 = 400 μatm. The effect of elevated Pco2 (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 Pco2 on daily mortality rates of Atlantic cod and Polar cod.

Fig. S5. Effects of temperature and Pco2 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).

References (4855)

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.


  1. H.-O. Pörtner et al., and Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge Univ. Press, 2014), pp. 411–484.

  2. O. Hoegh-Guldberg, R. Cai, E. S. Poloczanska, P. G. Brewer, S. Sundby, K. Hilmi, V. J. Fabry, S. Jung, The Ocean, in Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel of Climate Change, V. R. Barros, C. B. Field, D. J. Dokken, M. D. Mastrandrea, K. J. Mach, T. E. Bilir, M. Chatterjee, K. L. Ebi, Y. O. Estrada, R. C. Genova, B. Girma, E. S. Kissel, A. N. Levy, S. MacCracken, P. R. Mastrandrea, L. L. White, Eds. (Cambridge Univ. Press, 2014), chap. 30, pp. 1655–1731.

  3. J. Blindheim, The seas of Norden, in Norden: Man and Environment, U. Varjo, W. Tietze, Eds. (Gebrüder Borntraeger, 1987), pp. 20–32.

  4. A. M. Ajiad, H. Gjøsæter, in The Barents Sea. Ecosystem, Resources, Management. Half a Century of Russian-Norwegian Cooperation, T. Jakopsen, V. K. Ozhigin, Eds. (Tapir Academic Press, 2011), pp. 315–328.

  5. FAO, The State of World Fisheries and Aquaculture (SOFIA) (FAO Fisheries and Aquaculture Department, 2018).

  6. UNFCCC, Adoption of The Paris Agreement FCCC/CP/2015/L.9/Rev.1 (2015).

  7. K. Brander, Spawning and life history information for North Atlantic cod stocks, ICES Cooperative Research Report (2005).

  8. A. G. Dickson, C. L. Sabine, J. R. Christian, Guide to Best Practices for Ocean CO2Measurements (North Pacific Marine Science Organization, 2007).

  9. S. Wood, M. S. Wood, Package ‘mgcv’. R package version, 1.7-29 (2017).

  10. R. A. Locarnini, A. V. Mishonov, J. I. Antonov, T. P. Boyer, H. E. Garcia, O. K. Baranova, M. M. Zweng, C. R. Paver, J. R. Reagan, D. R. Johnson, M. Hamilton, D. Seidov, World Ocean Atlas 2013 (NOAA, 2013), vol. 1, pp. 73–44.

  11. R. M. Key, A. Olsen, S. van Heuven, S. K. Lauvset, A. Velo, X. Lin, C. Schirnick, A. Kozyr, T. Tanhua, M. Hoppema, S. Jutterström, R. Steinfeldt, E. Jeansson, M. Ishi, F. F. Perez, T. Suzuki, Global Ocean Data Analysis Project, Version 2 (GLODAPv2), ORNL/CDIAC-162, NDP-P093 (Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, 2015).

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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