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Northern cod species face damage to spawning habitats if global warming exceeds 1.5 ° C


Rapid climate change in the Northeast Atlantic and Arctic poses a threat to some of the largest fish populations in the world. The impact of heating and acidification can be easily accessed through mechanism-based risk assessment and future habitat suitability projections. We show that ocean acidification causes a narrowing of the embryonic thermal range, which identifies the suitability of spawning habitats as barriers to critical life history for two abundant species of cod. Embryo tolerance related to climate simulations reveals that CO is increasing2 emission [Representative Concentration Pathway (RCP) 8.5] will worsen the suitability of the current spawning habitat for both Atlantic cod (Gadus morhua) and Polar cod (Boreogadus saida) in 2100. Moderate heating (RCP4.5) can prevent dangerous climate impacts on Atlantic cod but still leaves some spawning areas for more vulnerable Pole cod, which also loses the benefits of ice-covered oceans. Emissions following RCP2.6, however, support unchanging habitat suitability for both species, suggesting that risks are minimized if heating is held "below 2 ° C, if not 1.5 ° C," as promised by the Paris Agreement.


Ocean heating and acidification (OWA), driven by unstable CO2 emissions, expected to limit the survival and reproduction of many marine organisms (1) Existing knowledge implies that the physiological limits of the early stages of life history define species susceptibility to OWA (2) The worst-impact scenario studies are important for raising risk awareness and gaining community acceptance of mitigation policies (3) However, even more important is the identification of the emission paths needed to minimize the risk of impacts and to find potential protection habitats of endangered species that must be prioritized in conservation (13) However, a mechanism-based risk assessment that integrates vulnerable life stages and their specific habitat needs into the context of the scenario is hardly available, especially for marine species inhabiting the Arctic region (4, 5)

Subarctic and Arctic seas around Northern Europe (i.e., Iceland Sea, Norwegian Sea, East Greenland Sea, and Barents Sea) are projected to experience higher levels of ocean warming, acidification and loss of sea ice than most other marine areas on Earth (6) This sea area – formerly called the Norden Sea (7) – inhabited by highly productive fish populations, most of whom make annual migrations to special spawning locations (4) Suitable biophysical features of spawning habitats support the survival of the early stages of life and their spread to suitable nursery areas (8) Given that fish embryos are often more sensitive to environmental changes than later life stages (2), embryonic tolerance can act as a fundamental obstacle to the suitability of spawning habitats. For example, a narrower thermal tolerance range in fish embryos than in other life stages can represent biogeographic constraints (8) and may be explained by the incomplete development of the cardiovascular and homeostatic systems (9) Ocean acidification (OA) caused by an increase in water CO2 levels can worsen homeostasis disorders (10), thus narrowing the thermal range (2, 11) and may reduce the suitability of spawning habitats by damaging the survival of eggs.

Both Atlantic cod and Polar cod are key members of North latitude fish fauna, but they differ in terms of thermal affinity and spawning preferences (4, 5) The Atlantic Cod is a "thermal generalist" that occupies moderate waters to the Arctic between ,51.5 ° and 20 ° C (12) Instead, Polar cod is a "thermal specialist," endemic to the High Arctic and rarely found at temperatures above 3 ° C (13) Because of the overlapping temperature ranges of the stages of adolescent and adult life, both species coexist during their summer feeding migrations (14) During winter and spring, however, spawning occurs in separate locations with different water temperatures and sea ice conditions (Figure 1). Given that Atlantic cod prefers warm water (3 ° to 7 ° C) than Polar cod (−1 ° to 2 ° C), the latter species are considered highly vulnerable to climate change (5, 14) In addition, another indirect threat to reproduction of Polar cod is the loss of projected sea ice, which serves as a nursery habitat for larvae and adolescents during the spring and summer (5)

Picture. 1 Pattern of distribution of Atlantic cod and Polar cod in the Norden Ocean.

(A) Atlantic cod; (B) Polar cod. Populations of both species reproduce during winter and spring (Atlantic cod: March to May; polar cod: December to March) at species-specific locations (ie spawning habitats, blue shaded regions) with characteristic temperatures and ice sea conditions (Atlantic cod : 3 ° to 7 ° C, open water, cod poles: −1 ° to 2 ° C, closed sea ice caps). Green arrows show the spread of eggs and larvae driven by the prevailing surface currents. During the summer, eating places (green shaded areas) of both species overlap, for example, around Svalbard, which marks the northernmost distribution limit of Atlantic cod. The red symbol shows the origin of animals (adult spawning) used in this study. Distribution map redrawn after (4, 13, 33) NEW, the Northeast Water Poly; FJL, Franz-Joseph-Land; NZ, Novaya Zemlya.

The aggregation of spawning Atlantic and Polar cod – often made up of millions of individuals – is an important resource for humans and other marine predators. For example, Norway's Atlantic cod fisheries alone generate annual revenues of US $ 800 million (15), whereas polar cod is an important food for many seabirds and mammals (5) Estimating changes in spawning habitat suitability for this focal species because it has high socioecological relevance (4) Embryo functional responses to OWA incorporated into habitat models can help identify spatial risks and benefits in various emissions scenarios, including the goal of limiting global warming to 1.5 ° C above pre-industrial levels (16)

Here, we assess the thermal tolerance range of embryos below OA in Atlantic cod and Polar cod. Level of oxygen consumption (MHI2) Spy embryos and larval morphometrics in hatches provide insight into the energetic constraints imposed by OWA. Suitability of spawning habitats was mapped in the Norden Ocean under different Pathway of Concentration Representation (RCP) by linking egg survival data with the Phase 5 Combined Interconnection Model Project climate simulation (CMIP5). RCP considers "no greenhouse gas mitigation" (RCP8.5), "intermediate mitigation" (RCP4.5), or "strong mitigation" (RCP2.6). The final scenario was developed with the aim of limiting the increase in global average surface temperature (mean above ground and sea level) to below 2 ° C relative to the 1850-1900 reference period and suitable for providing first estimates for the consequences of maintaining global warming to "Well below 2 ° C, if not 1.5 ° C," as stated in the Paris Agreement (16)


Embryonic oxygen consumption (MHI2) increases with temperature but flattens or decreases at the hottest temperatures (Atlantic cod: ≥9 ° C; Polar cod: ≥4.5 ° C; Figure 2, A and B), which, in combination with increased mortality under these conditions (Figure 3), shows severe heat pressure. The embryo adjusts to lower temperatures (<9 ° / 4.5 ° C) and increases Ptogether2 (partial pressure CO2) consumed ~ 10% more oxygen than those kept under control Ptogether2. This trend is reversed after heating, indicating that additional oxygen and related energy requirements under OA conditions cannot be met at very high temperatures, causing the thermal upper limit of metabolic maintenance to decrease. Higher energy requirements under elevated Ptogether2 can result from cumulative costs of increasing acid-base regulation, protein turnover, and damage repair (9, 10) Energy allocation for life-sustaining functions must be given priority over growth (17), as evidenced by CO2– and the reduction caused by heating in larval size when hatching (Fig. 2, C to F, and picture S2). Relative decrease in the orphan free body area due to increased larvae Ptogether2 on average 10% for Atlantic cod (P < 0.001) and 13% for Polar cod (P < 0.001), with the smallest larvae hatching at the hottest temperature (Fig. 2, C and D, and table S1). Decreases in larval body size and dry weight (Figures 2, E and F, and table S1) are in line with CO2reallocation-induced energy away from growth is also seen in other fish species (18)

Fig. 2 Increase effect Ptogether2 at the level of oxygen consumption depending on temperature (MHI2) and growth of Atlantic cod embryos and polar cod embryos (right).

(A and B) MHI2 measured in edged embryos (images). Symbols are means (± SEM are described as bars, n = 6 or 4). The performance curve (line) is based on n = 28 data points. The dark and light shade shows 90 and 95% credible Bayesian confidence intervals, respectively. (C and D) The mushroom-free body area of ​​the larvae in the hatch was assessed as an indicator of somatic growth and resource utilization (yellow). Placed box plots with individual values ​​indicate the 25th, 50th, and 75th percentiles; mustache marks 95% confidence interval. (D) Adequate sample sizes are not available at 6 ° C because most individuals die or hatch defects. (E and F) Offset between regression lines (with 95% confidence intervals) indicates CO2-related differences in the relationship between the weight size of newly hatched larvae (images). Individuals are collected throughout the treatment temperature (E: 0 ° to 12 ° C, F: 0 ° to 3 ° C). (A to F) Significant major effects of temperature, Ptogether2or their interactions (T * Ptogether2) shown by ★ black, while orange ★ shows significant CO2 effects in temperature care (Tukey post hoc test, n = 6 or 4 per treatment). See table S1 for details on statistical tests. N.a., not available.

Figure 3 Increase effect Ptogether2 on egg survival depends on temperature in Atlantic cod and Polar cod.

(A) Atlantic cod; (B) Polar cod. Symbols represent means (± SEM are described as bars, n = 6). The thermal performance curve (TPC, line) of each species is based on n = 36 data points. The dark and light shade shows 90 and 95% credible Bayesian confidence intervals, respectively. TPC was extrapolated to subzero temperatures by including freezing tolerance limits from the literature (Materials and Methods). The main effects of temperature are significant, Ptogether2or their interactions (T * Ptogether2) shown by ★ black, while orange ★ shows significant CO2 effects in temperature care (Tukey post hoc test, n = 6 or 4 per treatment). See table S1 for details on statistical tests.

Egg survival decreases beyond the preferred spawning temperature of Atlantic cod (≤0 ° and ≥9 ° C) and Polar cod (≥3 ° C), especially under the influence of increase Ptogether2 (Figure 3 and table S1). Thus, our results confirm that the embryo tolerance range is a strict constraint on thermal laying eggs of Atlantic cod and Polar cod. TOGETHER2Deaths induced at their optimal spawning temperatures are less clear for Atlantic cod (6 ° C, Fig. 3A) than for Polar cod (0 ° to 1.5 ° C, Fig. 3B). This observation is in accordance with variations in CO2 the sensitivity reported by previous research in the early stages of fish life tested for the OWA effect is only under optimum temperature conditions (18) However, both species experienced similar CO2Related decreases in egg survival on the threshold of warmth respectively (−48% at 9 ° C for Atlantic cod and −67% at 3 ° C for Polar cod). Increased thermal sensitivity of the embryo below the projection Ptogether2 the level implies a narrowing of their thermal tolerance range and thus from the species reproduction niche (2) As a result, the spatial level of thermally suitable spawning habitats for Atlantic cod and Polar cod may not only shift to higher latitudes in response to warming but also contracts due to OWA.

Compared to the Atlantic and Polar cod spawning sites in the study area (the blue area in Fig. 1; the yellow dotted area in Figure 4), our basic simulation (1985–2004) shows that spawning occurs exclusively within the optimum range thermal embryo development [>90% potential egg survival (PES), Fig. 4]. However, the area of ​​thermally suitable spawning habitat (PES> 90%) is greater than the area where spawning actually occurs. For example, despite the appropriate temperature, there is no spawning of Atlantic cod currently observed in the northeast Barents Sea (19), indicating that the suitability of the spawning habitat also depends on factors other than temperature. Mechanisms that block certain areas suitable for spawning may include the spread of deviant eggs and larvae, unfavorable feeding conditions, and predatory pressure (8, 19)

Picture. 4 Compatibility of the current spawning habitat (baseline) for Atlantic cod and Polar cod in the Norden Sea.

(A) Atlantic cod; (B) Polar cod. Suitability of spawning habitats is expressed as PES (% PES, color code) by combining experimental survival data (Figure 3) with the WOA13 temperature field (1 ° × 1 °, 50 m over the shelf sea) for the 1984–2005 baseline period. The average value above the spawning season (Atlantic cod: March to May; polar cod: December to March) and referenced to locations where spawning has been documented[brokenareayellow([yellowdashedareas([daerahputus-putuskuning([yellowdashedareas(13, 33)]. The spatial distance of thermally suitable spawning habitats (PES> 90%) is usually greater than that of "realized spawning habitats" because other limiting factors are not considered. The magenta dotted line shows the position of the edge of seasonal sea ice (defined as an area with an ice concentration of> 70%; note that the edge of the sea ice differs slightly between species due to various spawning seasons of certain species).

In 2100, the untreated OWA (RCP8.5) is projected to cause a substantial reduction in PES in the main spawning locations of the two species (Figures 5, A to C). For Atlantic cod, PES is projected to decline around Iceland (−10 to −40%) and the Faroe Islands (−20 to −60%) and along the entire coast of Norway (−20 to −60%), including the most important spawning sites in Lofoten islands (at 68 ° N, Fig. 5A). In turn, the extensive shelf area of ​​Svalbard and across the northeastern Barents Sea will be more suitable (PES, +10 to + 60%) due to warming and decreasing sea ice. However, the potential benefit of habitat in the North is constrained by reduced cold tolerance in Atlantic cod embryos under OA conditions and, perhaps, unknown inhibiting factors (see above). Under RCP4.5, decreases in Atlantic cod PES in several southern spawning locations (for example, the Faroe Islands: −10 to −40%) are largely compared to thermal benefits (PES, +20 to + 60%) in the northeast Barents Sea (between Svalbard, Franz Josef Land, and Novaya Zemlya; Fig. 5, D and F).

Picture. 5 Changes in thermally suitable spawning habitats of Atlantic cod (left) and Polar cod (right) on the Norden Sea under RCPs.

(A for C) RCP8.5: OWA Doesn't Move. (D for F) RCP4.5: Medium heating (not acidified). (G for I) RCP2.6: Less than 2 ° C global warming (not acidified). Maps show a PES shift between the baseline period (1985-2004; spawning season for Atlantic cod: March to May; Pole cod spawning season: December to March; see Figure 3) and multimodel based CMIP5 median (seasonal sea surface temperature, 0 to 50 m ; see Materials and Methods) for the end of this century (2081-2100). Black shading shows the area (cell, 1 ° × 1 °) with high uncertainty (i.e., the PES shift in the cell is smaller than the CMIP5 ensemble spread; see Materials and Methods). The magenta dotted line represents the position of the edge of sea ice from the specific spawning season of each species (defined as an area with an ice concentration of> 70%). (C, F, and I) For each map, values ​​(changes in PES) of individual cells are summarized by estimates of kernel density, with widths corresponding to the emergence of relative values. The box plot shows the 25th, 50th and 75th percentiles; mustache marks the 95% interval.

The polar pole is likely to suffer the most dramatic losses from spawning habitats south of Svalbard and Novaya Zemlya (PES, −40 to −80%; RCP8.5; Fig. 5B). In addition, Polar cod will lose most of its ice habitat except for small protection on the East Greenland shelf (Figure 5B). Even OA-free heating (RCP4.5; Fig. 5, E and F) will substantially reduce the suitability of important spawning habitats for polar cod from Svalbard (PES, −20 to −60%) and Novaya Zemlya (PES, −10 to −40%). The loss of sea ice area under the scenario RCP8.5 and RCP4.5 can indirectly influence the success of reproduction of Pole cod, because ice protects adult spawning from predation and serves as a feeding habitat for the early life stages (5) Limiting global warming to around 1.5 ° C above the pre-industrial level (average temperature of RCP2.6) may not only minimize PES reduction in the current core spawning area of ​​both species to less than 10% (Fig. 5 , G). for I) but also maintains several layers of sea ice.


Our projections show that the impact of OWA on egg survival and consequent changes in spawning spawning habitats may be the main determinant of climate-dependent constraints on Atlantic cod and Polar cod. This finding is in line with the hypothesis that thermal range tolerance and embryonic habitat of both species are compressed by progressive OWA (2) Our results also reinforce the notion that climate change does not mean representing an existential threat for cold-adapted species such as polar cod (20), although we identified some cold displacement for this species in the North Pole. The Atlantic Cod can follow polar displacement from its optimum thermal, possibly leading to the formation of commercially important species in areas currently dominated by Polar cod. A parallel decline in habitat suitability from Iceland and the coast of Norway (below RCP8.5) implies that, by 2100, spawning in the southern Arctic Circle (for example, south of Lofoten) may no longer be possible for Atlantic cod. The potential for the transfer of important fish stocks commercially across management boundaries and exclusive economic zones poses major challenges not only for national fishermen and environmentalists (5) but also for international bodies and regulations, which aim to avoid over-exploitation, resource conflicts, and degradation of native ecosystems in the Arctic (4, 21)

However, if global warming is limited to 1.5 ° C above pre-industrial levels, then changes in thermal suitability of spawning habitats are currently unlikely to exceed the critical threshold of Atlantic cod and Polar cod. Residual risk can be further reduced because both species have the potential to adapt to climate change, responding well (i) through a shift in the time and / or location of spawning in this region (22) or (ii) through a transgeneration process that increases physiological tolerance (23) Uncertainty in our results also relates to (iii) the reliability and resolution of CMIP5 climate projections (24)

First, the temporal window for spawning in the North is limited to late winter due to extreme light seasons and associated primary production (food for planktonic larvae) at high latitudes (> 60 ° N) (22) Significant changes in spawning phenology are therefore not possible in this region. In contrast, the expansion of spawning in the north during the historic and sustained warm-up period was well documented, especially for Atlantic cod, which extended its spawning activity to West Svalbard in the 1930s (25) However, core spawning areas (for example, the Lofoten archipelago for the Barents Sea population) have always been occupied during the past centuries, probably because of the favorable combination of biotic and abiotic factors that maximize the success of recruitment (8, 22) After spawning, the spread of eggs and larvae to suitable nursery areas – sometimes more than hundreds of kilometers – plays an important role in relation to the conformation of the life cycle and filling the population (8) Spawning in alternative locales (as required by RCP8.5 for both species and under RCP4.5 for Pole cod) can interfere with connectivity and therefore increase the risk of recruitment losses and failures (8) Thus, the success of the formation of new spawning habitats will depend greatly on a number of factors besides the survival of eggs (ie prey availability, predation pressure, and connectivity), all of which are currently difficult to predict (2, 22)

Second, our results assume that the range of embryo tolerance is constant across different populations and generations (that is, there are no evolutionary changes in this century). These assumptions are supported by experimental data[forexampletheoptimaltemperatureforthedevelopmentofthebridgeinadifferentpopulationofAtlanticArt([egsimilartemperatureoptimaforeggdevelopmentamongdifferentAttanticpodations([misalnyaoptimasuhuyangserupauntukpengembangantelurdiantarapopulasicodAtlantikyangberbeda([egsimilartemperatureoptimaforeggdevelopmentamongdifferentAtlanticcodpopulations(26); see also fig. S1], and with field observations[forexamplethechangeintheactivityofthescaffoldersisconsistentwiththedirectionoftheairresponsetothepreviousheat/ongoingprocess([egconsistencyoftheshiftfromthemodalactivityofresponsenon-explanatory/ongoingfarming([misalnyaperubahanaktivitaspemijahancodsecarakonsistenkearahutarasebagairesponsterhadappemanasansebelumnya/yangsedangberlangsung([egconsistentnorthwardshiftofcodspawningactivityinresponsetoprevious/ongoingwarming(17)]and phylogenetic analysis of the evolution of thermal tolerance in marine fish[eg<01°Cchangesintolerancetodermalper1millionyears([eg<01°Cchangeinthermaltoleranceper1millionyears([mis<01°Cberubahdalamtoleransitermalper1jutatahun([eg<01°Cchangeinthermaltoleranceper1millionyears(27)]. Transgeneity plasticity (TGP) can promote short-term adaptation to environmental changes through nongenetic inheritance (for example, mother transmission) (23) However, in contrast to the TGP theory, experiments on Atlantic cod show that the viability of eggs is disrupted during the same degree of warming if the female is exposed to heat during gonadal maturation (28) This example of negative TGP corresponds to the majority (57%) of studies on TGP in fish that observed a neutral (33%) or negative response (24%) (29) Given the limited capacity for short-term adaptation, it is likely that species must leave their traditional habitat as soon as the physiological limit is exceeded (2) Thus, our results identify not only high-risk areas but also potential protection habitats that must be prioritized in connection with the implementation of marine reserves.

Third, CMIP5 climate projections include uncertainty (24) To a certain extent, this uncertainty can be reduced and assessed by considering multimodel results (see Materials and Methods). Near-coastal habitats are not represented in the current global climate model (24) Beliefs in climate impact projections for these fields can be enhanced in future studies, most elegantly using the global multiresolution sea model with unstructured nets (30)

Given embryonic intolerance to OWA, we show that with immeasurable greenhouse gas emissions, large areas currently used for spawning will be less suitable for recruitment of cod and Atlantic Pole cod, which may cause a reduction in the impact on Arctic food networks and related ecosystem services (4, 5) However, our results also emphasize that mitigation measures, as promised by the Paris Agreement, can improve the effects of climate change on both species. Given that CO is currently2 emission trajectory produces a 1% chance to limit global warming to 1.5 ° C above pre-industrial levels (31), our results call for cutting emissions immediately after a scenario compatible with heating of 1.5 ° C to prevent damage to irreversible ecosystems in the Arctic and elsewhere.



Atlantic cod is captured by longlining in the southern Barents Sea (Tromsøflaket: 70 ° 28′00 ″ N, 18 ° 00′00 ″ E) in March 2014. Adult fish are transported to the Marine Cultivation Center (Nofima AS, Tromso, Norway) and held in flow-through tanks (25 m3) under ambient light, salinity [34 practical salinity units (PSU)], and temperature conditions (5 ° ± 0.5 ° C). The polar pole was captured in Kongsfjorden (West Svalbard: 78 ° 95′02 ″ N, 11 ° 99′84 ″ E) by trawling in January 2014. The selected fish was held in a flow-through tank (0.5 m)3) and transferred to the Aquaculture Research Station in Karvikå (NOFIMA, Norwegian Arctic University UiT, Tromso). At the station, the fish are stored in a flow-through tank (2 m)3) at 3 ° ± 0.3 ° C water temperature (34 PSU) and complete darkness. In both experiments, gametes used for in vitro fertilization were obtained by spawning strips from n = 13 (Pole cod: 12) male and n = 6 women (table S2).

Fertilization protocol

All fertilization is carried out within 30 minutes after stripping. Each batch of eggs was divided into two and fertilized using purified sea water and ultraviolet (UV) (34 PSU) which was previously adjusted to the holding temperature of the parent (Atlantic Cod: 5 ° C; Polar cod: 3 ° C) and two different Ptogether2 condition[control[control[kontrol[controlPtogether2: 400 μatm, pH(Free Scale) 8.15; high Ptogether2: 1100 μatm, pHF 7.77]. Dry fertilization protocol standardized with millin aliquots from n = 3 men are used to maximize the success of conception (32)

Fertilization success

Successful fertility was assessed in subsamples (3 × 100 eggs per batch and Ptogether2 treatment), which was incubated in a closed petri dish until stage 8-16-cell (Atlantic cod: 12 hours, 5 ° C; Polar cod: 24 hours, 3 ° C) and photographed under the stereomicroscope for further evaluation (S3 table)) . These images are also used to determine the average egg diameter from a batch of eggs (30 eggs per batch, table S3).

Incubation settings

According to different spawning seasons, the two trials can be carried out sequentially with the same experimental setting in 2014 (Polar cod: February to April; Atlantic cod: April to May). Previously fertilized eggs are either in control or high Ptogether2 maintained in each CO2 treatment and incubated until hatching at five different temperatures (Atlantic cod: 0 °, 3 °, 6 °, 9 °, and 12 ° C; Polar cod: 0 °, 1.5 °, 3 °, 4.5 °, and 6 ° C). The temperature range is chosen to cover spawning preferences of Atlantic cod (3 ° to 7 ° C) (33) and Polar cod (≤2 ° C) (13) and warming scenarios projected for each region. Each treatment group from the batch of eggs was divided into two stagnant incubators (20 incubators per woman, 120 in each experiment). To not estimate survival, only one of the two incubators was used to evaluate the survival of the eggs (and morphometric larvae at hatching), while the subsamples were needed for embryos. MHI2 measurements taken from the second incubator.

Initially, all incubators (volume, 1000 ml) were filled with filtration (0.2 μm) and sterile UV sea water (34 PSU) which was adjusted to each fertilizing treatment and stocked with positive floating eggs. Regarding the stagnant supply of oxygen in the incubator, it is important to ensure that eggs have enough space to regulate themselves in one layer below the surface of the water. We therefore adjusted the number of eggs per incubator (Atlantic cod: ~ 300 to 500; Polar cod: ~ 200 to 300) according to differences in egg size between Atlantic cod (~ 1.45 mm) and Polar cod (~ 1.65 mm ) The incubator loaded is then placed in a different thermostylated sea water bath (volume, 400 liters) to ensure a smooth temperature change in the incubator. The transparent, tapered bottom tapered is sealed with a Styrofoam cover to prevent CO2 outgassing and temperature fluctuations. According to the natural light regime, Atlantic cod eggs receive dim light with a daily rhythm of 8 hours of light / 16 hours of darkness, and cod egg Poles are stored in darkness except for dim light exposures during handling. Every 24 hours, 90% of the water volume of each incubator is replaced by a filter (0.2 μm) and UV sterilized seawater to avoid oxygen depletion. The outlet valve is installed at the bottom of the incubator to drain sea water with dead eggs, which lose buoyancy and drop down. Each seawater bath contains two reservoir tanks of 60 liters, which are used to regulate seawater to the appropriate temperature and Ptogether2 condition. The water temperature inside the water bath is controlled by a thermostat and recorded automatically every 15 minutes (± 0.1 ° C) through a multichannel aquarium computer (IKS-Aquastar, IKS Systems, Germany). Future Ptogether2 conditions are formed by injection of pure CO2 gas into a reservoir tank of 60 liters is submerged at each temperature. The multi-channel feedback system (IKS-Aquastar), connected to individual pH probes (IKS-Aquastar) and solenoid valves, is used to control the pH of the water and Ptogether2 values. That Ptogether2 The reservoir tank is measured in situ before each exchange of water with infrared Ptogether2 probes (Vaisala GMP 343, manual temperature compensation, accuracy ± 5 μatm; Vaisala, Finland). The probe is equipped with an MI70 Reading device and an aspiration pump, which is connected to membrane degassing (G541, Liqui-Cel, 3M, USA) to measure Ptogether2 in the air balanced to dissolved water gas (34) Factory calibration was confirmed by seawater measurements previously inflated with a technical gas mixture (1000 μatm CO2 in the air, Air Liquide, Germany). Before daily water exchange, the pH value of the reservoir tank was measured by laboratory level pH electrodes of up to three decimals (Mettler Toledo InLab Routine Pt 1000 with temperature compensation, Mettler Toledo, Switzerland), which was connected to a WTW 3310 meter pH. Two-point calibration with NBS buffers (National Bureau of Standards) is carried out every day. To convert NBS to a concentration scale protons are free for pH of sea water (35), electrodes calibrated with tris-HCl sea water buffer (36), which adjusts to the appropriate incubation temperature before each measurement. The pH value of seawater refers to the scale of the free pH (pHF) throughout this text. The seawater parameters are summarized in the figure. S3.

Survival of eggs

Kematian telur dicatat secara 24 jam sampai semua individu dalam inkubator meninggal atau menetas (gbr. S4). Setelah menetas dimulai, larva berenang bebas dikumpulkan di pagi hari, di-eutanasia dengan overdosis dari tricaine methanesulfonate (MS-222), dan dihitung setelah pemeriksaan visual untuk kelainan morfologi di bawah stereomicroscope. Insiden cacat larva dihitung sebagai persentase dari tukik menunjukkan deformasi parah kantung kuning telur, kranium, atau kolom vertebral. Kelangsungan hidup telur didefinisikan sebagai persentase larva nonmalforma, hidup yang menetas dari jumlah awal telur yang dibuahi (gambar S5). Proporsi telur dibuahi dalam inkubator diperkirakan dari keberhasilan pembuahan rata-rata dari batch telur masing-masing (tabel S3).


Tingkat konsumsi oksigen (MHI2) Embrio bermata (pada 50% pigmentasi mata, gambar. S4) diukur dalam ruang respirasi yang dikontrol suhu tertutup (OXY0 41 A, Collotec Meßtechnik GmbH, Jerman). Ruang berdinding ganda terhubung ke termostat aliran-melalui untuk menyesuaikan suhu ruang respirasi ke suhu inkubasi yang sesuai dari telur. Pengukuran dilakukan dalam rangkap tiga dengan 10 hingga 20 telur dari setiap kombinasi wanita dan pengobatan. Telur ditempatkan ke dalam ruangan dengan volume 1 ml air laut yang disterilkan disesuaikan dengan yang sesuai Ptogether2 pengobatan. Sebuah microstirrer magnetik (3 mm) ditempatkan di bawah telur mengambang untuk menghindari stratifikasi oksigen di dalam ruang respirasi. 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 MHI2. In each case, we treated different levels of temperature and Ptogether2 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 Ptogether2 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 MHI2. 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 Ptogether2 on thermal sensitivity. “Betar” and “Gaussian” error distributions were used for egg survival and MHI2 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 Ptogether2 = 400 μatm. The effect of elevated Ptogether2 (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 Ptogether2 on daily mortality rates of Atlantic cod and Polar cod.

Fig. S5. Effects of temperature and Ptogether2 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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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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