Saturday , April 17 2021

If global warming exceeds 1.5 ° C, northern cod species are exposed to spawning habitat losses.


Rapid climate change in the Northeast Atlantic and Arctic regions is a threat to some of the world's largest fish populations. The effects of warming and acidification can be made accessible by mechanism-based risk assessments and projections of future habitat appropriateness. Ocean acidification shows that two abundant cod species cause narrowing of embryonic thermal intervals, which determines the appropriateness of ovulation habitats as a critical life history bottleneck. Embryonic tolerance ranges due to climate simulations reveal a continuously increasing CO.2nd emissions [Representative Concentration Pathway (RCP) 8.5] Disrupts the availability of the present spawning habitat for Atlantic cod (Gadus Morhuaand Polar cod (Boreogadus saidaUntil 2100. moderate warming (RCP4.5) can prevent dangerous climatic effects on Atlantic cod, but still leave several spawning areas for the more sensitive Polar cod, which loses the benefits of an ice-covered ocean. However, emissions following RCP2.6 support the largely unchanged habitat suitability for both species. This means that risks are minimized if the temperature is kept below 2 ° C if the warming is not below ur 1.5 ° C as promised by the Paris Agreement.


Ocean warming and acidification driven by reduced CO (OWA)2nd emissions are expected to limit the survival and proliferation of many marine organisms (one). The present information implies that the physiological boundaries of the early stages of life history define the vulnerability of species to OWA (2nd). The worst-case impact scenarios are important to increase risk awareness and to gain social acceptance for the reduction policy.3). However, more importantly, it is the identification of the emission paths required to minimize the impact risks and the presence of potential refuge habitats of endangered species that should prioritize protection.one3). However, for marine creatures living especially in the Arctic regions, it is not possible to assess risk-based mechanisms that integrate vulnerable life stages and special habitat needs in the context of a scenario.4, 5).

It is estimated that the Subarctic and Arctic seas around northern Europe (ie, the Icelandic Sea, the Norwegian Sea, the East Greenland Sea and the Barents Sea) will be subject to higher ocean warming, acidification and sea-ice loss rates than other marine areas on the Earth.6). These ocean areas – previously Norden Seas (7– where most productive fish populations live, most of them undertake annual transitions to specific migration areas (4). The biophysical characteristics of appropriate spawning habitats support the survival of early life stages and their distribution towards appropriate nursery areas.8). Considering that fish embryos are generally more sensitive than life cycle after environmental change (2ndembryonic tolerance can act as a basic restriction on the appropriateness of the spawning environment. For example, thermal tolerance ranges narrower than other stages of life in fish embryos may represent a biogeographic constraint (8and possibly the incomplete development of cardiovascular and other homeostatic systems (9). Ocean acidification caused by CO in high water (OA)2nd levels may exacerbate the discomfort of homeostasis (10), thus narrowing the thermal range (2nd, 11th) and will reduce the appropriateness of ovulation habitat by disrupting egg survival.

Both the Atlantic cod and the Polar cod are key members of the Northern high-latitude fish fauna, but differ in their thermal affinity and preference for ovulation (4, 5). Atlantic cod is a 51 thermal generalist Ar that passes moderate to Arctic waters between .51.5 ° and 20 ° C.12). On the contrary, the Polar cod is a; thermal expert in specific to the High Arctic and is rarely found at temperatures above 3 ° C.13). Because of the overlapping temperature ranges of juvenile and adult life stages, both species exist during summer migrations.14). However, in winter and spring, spawning occurs in separate places with different water temperatures and sea-ice conditions (Figure 1). Since the Atlantic cob prefers hotter waters (3 ° to 7 ° C) from Polar cod (-1 ° to 2 ° C), these species are considered particularly vulnerable to climate change (5, 14). Moreover, another indirect threat to the reproduction of Polar cod is the loss for marine ice, which serves as a nursery habitat for larvae and offspring in spring and summer.5).

Figure 1 Formation of Atlantic cod and Polar cod in Norden Seas.

(one) Atlantic cod; (BPolar cod. Populations of both species multiply in characteristic temperature and sea-ice conditions (species, spawning habitats, blue shaded areas) in winter and spring (Atlantic cod: from March to May; polar fish: December-March). cod: 3 ° to 7 ° C, open water, Polar code: kod1 ° to 2 ° C, closed sea-ice cover). Green arrows indicate spread of eggs and larval driven by diffuse surface currents. In summer, the feeding areas (green shaded areas) of both species partially overlap around Svalbard, which indicates, for example, the northernmost distribution border of Atlantic cod. The red symbols indicate the origin of the animals used in this study (ovulation adults). Distribution maps were redrawn (4, 13, 33). NEW, Northeast Water Polynesia; FJL, Franz-Joseph-Land; NZ, Novaya Zemlya.

The breeding clusters of the Atlantic and Polar cod (many millions) are important sources for humans and other marine hunters. For example, Norwegian Atlantic cod fishing alone brings annual income of $ 800 million.15), Polar cod is an important nutrient for many sea birds and mammals.5). Estimation of the appropriateness of the ovulation habitat for these focal species therefore has a high socio-economic interest (4). The functional responses of the embryos to OWA included in the habitat models can help identify spatial risks and benefits in varying 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 thermal tolerance under Atlantic cod and Polar cod under OA. Oxygen consumption rates (MSHE IS2ndMorphometry of the pupil stage embryos and capillary morphometry shed light on the energetic restrictions applied by OWA. The suitability of the ovulation habitat was mapped under different Representative Concentration Routes (RCPs) along the Norden Seas by associating egg survival data with Climate Simulations of the Coupled Model Intercomparison Project Phase 5 (CMIP5). RCPs assume no 2 greenhouse gas reduction ya (RCP8.5), azaltma intermediate reduction “(RCP4.5), or ı strong mitigation“ (RCP2.6). The final scenario is suitable for reducing the global average surface temperature (average land and sea surface) to <2 ° C below the reference period of 1850-1900 and providing the first estimate for the results. Keep global warming at i 1.5 ° C if not below 2 ° C C, as stated in the Paris Agreement16).


Embryonic oxygen consumption (MSHE IS2ndincreased with increasing temperatures, but increased or decreased at the highest temperatures (Atlantic cod: ≥9 ° C; Polar cod: ≥4.5 ° C; Fig. 2, A and B). conditions indicative of severe heat stress (Figure 3). Embryos are acclimated to low temperatures (<9 ° / 4,5 ° C) and height PAco2nd (CO partial pressure2ndconsumed ~ 10% more oxygen than those grown under control PAco2nd. This trend was reversed after warming and showed that under the conditions of OA, additional oxygen and associated energy demands could not be met at critical high temperatures and led to a reduction in the upper thermal limit of metabolic care. High energy requirements upgraded PAco2nd increased acid-base regulation may result from the cumulative costs of protein turnover and damage repair.9, 10). The allocation of energy to life-sustaining functions should take precedence over growth (17As evidenced by CO.)2nd– and reductions in the larval size of the lid (Figure 2, C to F and figure S2). Relative decrease in increased body area PAco2nd Average 10% for Atlantic codP < 0.001% for Polar cod and 13%P < With incubation of the smallest larvae at the smallest temperatures (Figure 2, C and D, and table S1). Larval size and dry weight reduction (Figure 2, E and F and S1 table) are consistent with CO.2ndThe energy seen in other fish species away from energy18).

FIG. 2nd Raised Effects PAco2nd temperature-dependent oxygen consumption (MSHE IS2ndand (right) growth of embryos and polar cod embryos in Atlantic cod.

(one and B) MSHE IS2nd in eye stage embryos (image). Symbols are tools (bars denoted as ± SEM & # 39; dir, n = 6 or 4). Based on performance curves (lines) n = 28 data points. Dark and light shadows show convincing confidence intervals of 90% and 95% respectively. (C and DThe larval unstable body area in the warehouse was evaluated as an indicator of somatic growth and source (yolk) use. The box drawings covered with separate values ​​indicate 25, 50 and 75 percentile; marks the 95% confidence intervals of the mustache. (D) Adequate sample sizes were not available at 6 ° C because most individuals were dead or hatched. (TO and FThe distances between the regression lines (with 95% confidence interval) indicate CO2ndDifferences related to size-weight relationships of newly screened larvae (images). Individuals were pooled in temperature treatments (E: 0 ° to 12 ° C, F: 0 ° to 3 ° C). (A & # 39; to F & # 39;) The main main effects of temperature, PAco2ndor their interaction (T * PAco2nd★ meaningful CO means orange ★ whereas black is indicated by ★2nd effects on temperature treatments (Tukey post hoc test, n = 6 or 4 per treatment). See table S1 & # 39; for details on statistical testing. N.a., not available.

Sec. 3 Raised Effects PAco2nd On temperature survival of eggs in Atlantic cod and polar cod.

(one) Atlantic cod; (BPolar cod. Symbols represent tools (bars are shown as ± SEM, n = 6). Thermal performance curves (TPCs, lines) of each species are taken as basis. n = 36 data points. Dark and light shadows show convincing confidence intervals of 90% and 95% respectively. TPCs were estimated at subzero temperatures by including freezing tolerance thresholds from the literature (Materials and Methods). Major main effects of temperature, PAco2ndor their interaction (T * PAco2nd★ meaningful CO means orange ★ whereas black is indicated by ★2nd effects on temperature treatments (Tukey post hoc test, n = 6 or 4 per treatment). See table S1 & # 39; for details on statistical testing.

Egg survival was reduced with Atlantic cod (isi0 ° and ≥9 ° C) and Polar cod (≥3 ° C), especially with the effect of elevation, except for preferred spawning temperatures. PAco2nd (Fig. 3 and table S1). Accordingly, our results confirm that embryonic tolerance intervals are a tight restriction on Atlantic cod and Polar cod thermal spawning niche. CO2ndThe mortality rates induced at optimal spawning temperatures were less pronounced compared to Polar cod (0 ° to 1.5 ° C, Figure 3B) for Atlantic cod (6 ° C, Fig. 3A). This observation corresponds to the variation in CO.2nd The sensitivity reported in previous studies on the early life stages of fish tested for OWA is effective only at optimum temperature conditions (18). However, both species experienced a similar CO.2ndegg survival rates, reduction in warmer thresholds (for Atlantic cod at 9 ° C – 48% and Polar cod at 3 ° C – 67%). Increased thermal sensitivity of projected embryos PAco2nd The levels refer to the narrowing of the thermal tolerance range and thus the breeding niches of the species.2nd). As a result, the spatial extent of thermally suitable spawning habitat for Atlantic cod and Polar cod not only shifts to higher latitudes in response to warming, but can also contract depending on OWA.

Compared to the Atlantic cod and Polar cod (Fig. 1 in the blue areas in Figure 1; Figure 1), our initial simulations (1985-2004) have shown Thermal optimum range of embryo development only [>90% potential egg survival (PES), Fig. 4]. However, the thermally suitable spawning habitat area (PES> 90%) is greater than the area where the spawning actually takes place. For example, despite suitable temperatures, it is not currently exposed to Atlantic cod in the northeast of the Barents Sea (19shows that the appropriateness of the ovulation habitat is also dependent on factors other than the temperature. Mechanisms that inhibit certain areas as appropriate for ovulation may include abnormal distribution of eggs and larvae, inappropriate feeding conditions, and predation pressure.8, 19).

Figure 4 Eligibility for present (start) spawning habitat for Atlantic cod and Polar cod in the Norden Seas.

(one) Atlantic cod; (BPolar cod. The suitability of the ovulation habitat is expressed as PES (% PES, color coded) by combining experimental survival data (Figure 3) with the WOA13 temperature areas (1 ° x 1 °, upper 50 m rack seas) for the base period between 1984 ,2005. The values ​​are averaged over the spawning seasons (Atlantic cod: March-May; polar cod: December-March) and references to where the ovulation is documented.[Sarıkesikalby([Yellowdashedareas([sarıkesikalanlar([yellowdashedareas(13, 33)]. The spatial size (PES> 90%) of the thermally suitable spawning habitat is typically greater than the “actual spawning habitat ansal because other limiting factors are not taken into account. Dotted purple lines indicate seasonal sea-ice position (ice concentrations are defined as areas of> 70%; note that, depending on species-specific spawning seasons, there are very few types of sea-ice edges between species).

By 2100, it was envisaged that the accelerated OWA (RCP8.5) would cause a significant reduction in PES in the key spawning areas of both species (Figs. 5, A to C). PES for Atlantic cod reduced to Iceland (−10 to −40%) and Faroe Islands (−20 to −60%) and all Norwegian coasts (;20 to ES60%) It is envisaged. Spawning areas in the Lofoten archipelago (68 ° N, Fig. 5A). The large shelf zones along the Svalbard and northeastern Barents Sea will be more appropriate due to the warming and decreasing sea-ice cover (PES, +10 to + 60%). However, potential habitat gains in the North are restricted by the reduced cold tolerance of Atlantic cod embryos under OA conditions and possibly under unknown restriction factors (see above). Under RCP4.5, in some southern spawning zones (eg Faroe Islands: Bar10 to azal40%) decreases in PES in Atlantic cod, with thermal benefits in the northeast Barents Sea (PES, +20 to + 60% ) largely outweighs. (Between Svalbard, Franz Josef Land and Novaya Zemlya; Fig. 5, D and F).

Figure 5 Change in thermally suitable spawning habitat of Atlantic cod (left) and Polar cod (right) in Norden Sea under RCPs.

(one for C) RCP8.5: OWA not accelerated. (D for FRCP4.5: Intermediate heating (acidification not taken into account). (G, for IRCP2.6: less than 2 ° C global warming (acidification not taken into account). The maps show the change in PES between the initial period (1985 #2004; the spawning season of Atlantic morons: from March to May; the spawning season of Polar morinata: December-March; see Figure 3) and the median of the CMIP5 multimodel-based projections. seasonal sea surface temperature, 0 to 50 m; for the end of this century (2081 Malzeme2100) see Materials and Methods). Black shading indicates areas of high uncertainty (cells, 1 ° x 1 °) (ie the slip in PES in this cell is smaller than the CMIP5 community propagation, see Materials and Methods). Dotted magenta lines represent the marine-ice edge positions of the species-specific spawning season (defined as areas with ice concentrations> 70%). (C, F and I) For each map, the values ​​of the individual cells (change in PES) are summarized by the estimates of the core density, the width corresponding to the relative occurrence of the values. Box drawings show 25, 50 and 75 percentile; The ends of the blade are marked at 95% intervals.

The polar cod will probably experience the most dramatic losses of the spawning habitat in the south of Svalbard and Novaya Zemlya (PES, #40 to -80%; RCP8.5; Figure 5B). Furthermore, the Polar cod will lose most of its ice-cold habitats outside a small bunker on the East Greenland shelf (Figure 5B). For indoor coding for heating even without OA effects (RCP4.5; Figures 5, E and F), Svalbard (PES, −20 to a60%) and Novaya Zemlya (PES, tır10) will significantly reduce the appropriateness of spawning habitats. – 40% & quot; a. Under RCP8.5 and RCP4.5 scenarios, the widespread loss of sea ice may indirectly affect the reproductive success of polar fish, since it protects ice spawning adults from predation and serves as a feeding environment for early life stages.5). Limiting global warming to about 1.5 ° C above the preindustrial levels (ie the median temperature of RCP2.6) can reduce the PES reduction in existing core spawning areas of both species to less than just 10% (Figure 5, G). I) but also protect some sea-ice cover.


Our projections suggest that changes in OWA-focused effects on egg survival and changes in habitat compatibility may be key determinants of climate-dependent constraints in Atlantic cod and Polar cod. The present findings are consistent with the hypothesis that the tolerance thermal ranges and embryonic habitats of both species are compressed by progressive OWA (2nd). Our results also support the idea that undisclosed climate change poses an existential threat to cold adapted species such as Polar cod (20Although, in spite of detecting some cold refugia for this kind of High Arctic. Atlantic cod could monitor the poleward displacement of its thermal optimum and possibly lead to the establishment of these commercially important species in the regions currently dominated by the Polar cod. The parallel decline in habitat conformity (under RCP8.5) on the coasts of Iceland and Norway indicates that it may no longer be possible for the Atlantic cod in 2100 to emerge in the south of the Arctic Circle (eg, south of Lofoten). The management limits of commercially important fish stocks and their potential displacement along the special economic zones lead to great difficulties, not only for national fishermen and conservatives.5and also to international bodies and regulations that attempt to lead to excessive exploitation, resource conflicts and the deterioration of unspoiled ecosystems in the Arctic (4, 21).

However, if global warming is limited to 1.5 ° C above preindustrial levels, then changes in the thermal suitability of available spawning habitats are unlikely to exceed critical thresholds of Atlantic cod and Polar cod. Remaining risks can be further reduced, as both types can potentially adapt to climatic changes: (i) through changes in timing and / or location of ovulation in existing areas.22or (ii) through transgenic processes that increase physiological tolerance (23). The uncertainties in our results also relate to (iii) the reliability and resolution of CMIP5 climate projections (24).

First, the temporary window for spawning in the North is limited to the last spring of winter due to the extreme seasonality of light at high latitudes (> 60 ° N) and the associated primary production (food for planktonic larvae).22). Significant changes in ovulation phenology are unlikely to occur in this region. Rather, it was documented for the north-west widening of western expansion in the historical and ongoing warming periods, especially for the Atlantic cod, which expanded its ovulation activity to the Western Svalbard in the 1930s.25). However, the core spawning areas (eg, the Lofoten archipelago for the population of the Barents Sea) have always been occupied in the past centuries, always due to the appropriate combinations of biotic and abiotic factors that will maximize the success of recruitment.8, 22). The spread of eggs and larvae to appropriate nursery areas (sometimes hundreds of kilometers) following ovulation plays an important role in life cycle connectivity and population renewal (8). In alternative locations, ovulation (as required under RCP8.5 for both species and under RCP4.5 for Polar cod) may disrupt the link and therefore increase the risk of damaging losses and recruitment failure (8). Accordingly, the successful establishment of new ovulation habitats is largely difficult to predict, in addition to egg survival, in addition to a number of factors (ie, the presence, prediction pressure, and linkage of the catch).2nd, 22).

Second, our results assume that embryonic tolerance intervals are constant over different populations and generations (ie there is no evolutionary change in this century). These assumptions are supported by experimental data[Örneğinfarklıatlantikmorinapopülasyonlarıarasındayumurtagelişimiiçinbenzersıcaklıkoptimizasyothe([Egsimilartemperatureoptimaforeggdevelopmentamongdifferentatlanticcodpopulations([örneğinfarklıAtlantikmorinapopülasyonlarıarasındayumurtagelişimiiçinbenzersıcaklıkoptimizasyonu([egsimilartemperatureoptimaforeggdevelopmentamongdifferentAtlanticcodpopulations(26); see also S1]as well as with field observations[Örönceon/devamedenısınmayayanıtolarakmorinayumurtlamaaktivitesinintutarlıkuzeyekaythe([Egconsistentnorthwardshiftofcodspawningactivityinresponsetoprevious/ongoingwarming([örönceki/devamedenısınmayayanıtolarakmorinayumurtlamaaktivitesinintutarlıkuzeyekayması([egconsistentnorthwardshiftofcodspawningactivityinresponsetoprevious/ongoingwarming(17)]and phylogenetic analysis of thermal tolerance evolution in marine fish[Inörneğin1milyonyıldatermaltolerans<01°C&#39;likdeğişI([Eg<01°Cchangeinthermaltoleranceper1millionyears([örneğin1milyonyıldatermaltoleransta<01°C'likdeğişim([eg<01°Cchangeinthermaltoleranceper1millionyears(27)]. Transgenous plasticity (TGP) may promote short-term adaptation through nongenetic inheritance resulting from environmental change (eg, Maternal transmission) (23). However, unlike the TGP theory, experiments on Atlantic cod suggest that egg viability is impaired when females are exposed during gonad maturation.28). This TGP sample corresponds to the majority (57%) of the studies on TGP in neutral (33%) or negative (24%) responses.29). Given the limited capacity for short-term adaptation, species are likely to have to abandon their traditional habitats as soon as their physiological limits are exceeded.2nd). Accordingly, our results define not only high-risk areas but also potential refuge habitats that should be prioritized for the implementation of marine reserves.

Third, CMIP5 climate projections include uncertainty (24). To some extent, these uncertainties can be reduced and evaluated by considering multi-model results (see Materials and Methods). Nearby habitats are underrepresented in current global climate models (24). The confidence of climate impact projections for these areas can be further enhanced in future studies with global multidisolution ocean models with unstructured network structures (30).

In light of embryonic intolerance against OWA, we have previously used large spawning greenhouse gas emissions, leading to cascading effects on the Arctic food networks and related ecosystem services, possibly leading to cascading effects on the Atlantic cod and Polar cod. show that it will become less suitable for recruitment.4, 5). However, our results emphasize that mitigation measures, as stated by the Paris Agreement, may affect climate change on both species. Valid CO given2nd Emission trajectories give a chance to limit global warming up to 1% above pre-industrial levels.31), our results require immediate emission cuts by following scenarios compatible with 1.5 ° C warming to prevent irreversible ecosystem damage in the Arctic and elsewhere.



Atlantic marines were captured in March 2014 in the southern Barents Sea (Tromsøflaket: 70 ° 28de00 39 N, 18 ° 00 Bar00; E). Mature fishes, Sea Water Products Center (Nofima AS, Tromsø, Norway) and a flow tank (25 m3) Under ambient light, salinity [34 practical salinity units (PSU)]and temperature conditions (5 ° ± 0.5 ° C). In the Kongsfjorden (West Svalbard: 78 ° 95 )02 ″ N, 11 ° 99 ,84 ″ E) in January 2014, troll-caught pole fish were caught. Selected fish in the flowing tanks (0.5 m.3and transferred to Aquaculture Research Station (NOFIMA, Norway UiT, Tromsø Arctic University) in Karvikå. At the station, fish were kept in a flowing tank (2 m33 ° ± 0.3 ° C at water temperature (34 PSU) and in full darkness. In both experiments, the strip from the gametes used for in vitro fertilization was obtained by ovulation. n = 13 (Polar cod: 12) male and n = 6 women (table S2).

Fertilization protocol

All fertilizers were performed within 30 minutes after stripping. Each egg mixture was halved and previously fertilized using rootstock holding temperature (Atlantic cod: 5 ° C; Polar cod: 3 ° C) and two different adjusted filtered and ultraviolet (UV) treated seawater (34 PSU). PAco2nd conditions[control[controller[kontrol[controlPAco2nd: 400 mm, pH(Free Scale) 8:15; high PAco2nd: 1100 μatm, pHF 7.77]. A standard dry fertilization protocol with milt aliquots n 3 men were used to maximize fertilization success.32).

Fertilization success

The fertilization success was evaluated in the samples (3 × 100 eggs per batch and PAco2nd incubated in closed petri dishes until the 8/16-cell stage (Atlantic cod: 12 hr, 5 ° C; Polar cod: 24 hr, 3 ° C) and photographed under a stereomicroscope for subsequent evaluation (table S3) . ). These images were also used to determine the average egg diameter of an egg set (30 eggs per batch, table S3).

Incubation installation

According to different spawning seasons, both experiments can be carried out sequentially with the same experimental setup in 2014 (Polar cod: from February to April; Atlantic cod: from April to May). Eggs pre-checked or fertilized at high PAco2nd in the relevant CO2nd and incubate at five different temperatures (Atlantic cod: 0 °, 3 °, 6 °, 9 ° and 12 ° C; Polar code: 0 °, 1.5 °, 3 °, 4.5 ° and 6 ° C). . The temperature ranges were selected to cover the spawning preferences of Atlantic cod (3 ° to 7 ° C) (33and Polar cod (≤2 ° C) (13and the heating zones foreseen for the zone concerned. Each treatment group of an egg group was divided into two stationary incubators (120 women in each experiment, 20 incubators). In order to avoid survival predictions, only one of the two incubators (and larval morphometry in the lid) to evaluate the use of eggs, sub-samples required for embryonic MSHE IS2nd measurements were taken from the second incubator.

Initially, all incubators (volume, 1000 ml) were filtered (0.2 ilgilim) and adjusted to fertilization treatment with UV-sterilized seawater (34 PSU) and filled with positive floating eggs. With respect to the oxygen supply in a stationary incubator, it is important to ensure that the eggs have sufficient space to arrange themselves as a single layer below the water surface. Therefore, we adjusted the amount 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). Installed incubators were then placed in different thermostat sea water baths (volume, 400 liters) to ensure a uniform temperature change in the incubator. Transparent, bottom conical incubators are sealed with a Styrofoam lid to prevent CO.2nd Outgassing and temperature fluctuations. Doğal ışık rejimlerine göre, Atlantik morina yumurtaları, 8 saatlik ışık / 16 saat karanlık günlük ritim ile loş ışık aldı ve işlem sırasında loş ışık maruziyeti dışında Polar morina yumurtaları karanlıkta tutuldu. Her 24 saatte, her bir inkübatörün su hacminin% 90&#39;ı, oksijen tükenmesini önlemek için filtrelenmiş (0.2 um) ve UV-sterilize deniz suyu ile değiştirilmiştir. Deniz suyunu ölü deniz ile boşaltmak için yüzdürme kabiliyetini azaltan ve dibe inen inkübatörlerin altına bir çıkış valfi monte edilmiştir. Her deniz suyu banyosu, deniz suyunu karşılık gelen sıcaklığa getirmek için kullanılan iki adet 60 litrelik rezervuar tankını içeriyordu. PAko2nd koşullar. Su banyoları içindeki su sıcaklıkları termostatlarla kontrol edildi ve her 15 dakikada bir (± 0.1 ° C) çok kanallı bir akvaryum bilgisayarı (IKS-Aquastar, IKS Systems, Almanya) aracılığıyla otomatik olarak kaydedildi. gelecek PAko2nd koşullar saf CO enjeksiyonu ile kuruldu2nd Her sıcaklıkta batırılmış 60 litrelik rezervuar tanklarına gaz verin. Su pH&#39;sini kontrol etmek için bireysel pH problarına (IKS-Aquastar) ve solenoid valflere bağlı çok kanallı bir geri bildirim sistemi (IKS-Aquastar) kullanıldı. PAko2nd değerler. PAko2nd rezervuar tanklarının her bir su değişiminden önce kızılötesi ile in situ ölçülmüştür. PAko2nd sonda (Vaisala GMP 343, manüel sıcaklık kompanzasyonu, ± 5 μmik doğruluk; Vaisala, Finlandiya). Prob, ölçülmek üzere bir gaz giderme membranına (G541, Liqui-Cel, 3M, ABD) bağlanan bir MI70 Okuma cihazı ve bir aspirasyon pompası ile donatılmıştır. PAko2nd havada çözünmüş su gazlarına dengelenmiştir (34). Fabrika kalibrasyonu, daha önce bir teknik gaz karışımı (1000 μatm CO) ile kabarmış deniz suyu ölçümleri ile doğrulandı.2nd havada, Air Liquide, Almanya). Günlük su değişiminden önce, rezervuar tanklarının pH değerleri, bir WTW 3310 pH&#39;ına bağlanan üç ondalık basamak (Mettler Toledo InLab Routine Pt 1000 sıcaklık telafili, Mettler Toledo, İsviçre) ile laboratuvar dereceli bir pH elektrodu ile ölçülmüştür. metre. Günlük olarak NBS (Ulusal Standartlar Bürosu) tamponlarıyla iki noktalı bir kalibrasyon gerçekleştirilmiştir. Deniz suyu pH&#39;sı için NBS&#39;yi serbest proton konsantrasyon ölçeğine dönüştürmek (35), elektrot tris-HCl deniz suyu tamponları ile kalibre edildi (36Her ölçümden önce karşılık gelen inkübasyon sıcaklığına alıştırılmış olan). Deniz suyu pH değerleri serbest pH ölçeğine (pH) karşılık gelirFBu yazı boyunca. Deniz suyu parametreleri şekil l&#39;de özetlenmiştir. S3.

Yumurta sağkalım

Yumurta ölüm oranı, bir inkübatördeki tüm bireyler ölene veya yumurtadan çıkana kadar 24 saat esasına göre kaydedilmiştir (Şekil S4). Kuluçkalama başladıktan sonra, sabahları serbest-yüzme larvaları toplandı, aşırı dozda tricaine metansülfonat (MS-222) ile ötanazi yapıldı ve bir stereomikroskop altında morfolojik deformiteler için görsel incelemeden sonra sayıldı. Larva deformitelerinin insidansı, yumurta sarısı, kafatası veya vertebral kolonun ağır deformasyonlarını gösteren yavruların yüzdesi olarak ölçülmüştür. Yumurta sağkalımı, döllenmiş yumurtanın ilk sayısından taranmış olan, biçimsiz, yaşayabilir larvaların yüzdesi olarak tanımlanmıştır (Şekil S5). Kuluçka makinesindeki döllenmiş yumurtaların oranı, ilgili yumurta kümesinin ortalama döllenme başarısından tahmin edilmiştir (tablo S3).


Oksijen tüketim oranları (MSHE IS2ndgözbebeği aşamalı embriyoların (% 50 göz pigmentasyonunda, şekil S4) kapalı, sıcaklık kontrollü solunum odalarında (OXY0 41 A, Collotec Meßtechnik GmbH, Almanya) ölçüldü. Çift duvarlı hazneler, solunum odasının sıcaklığını, yumurtaların karşılık gelen inkübasyon sıcaklığına ayarlamak için bir akış termostatına bağlanmıştır. Ölçümler, her dişi ve tedavi kombinasyonundan 10 ila 20 yumurta ile üç kopya halinde gerçekleştirilmiştir. Eggs were placed into the chamber with a volume of 1 ml of sterilized seawater adjusted to the corresponding PAco2nd treatment. 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[nmolO2nd (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 MSHE IS2nd. In each case, we treated different levels of temperature and PAco2nd 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 PAco2nd 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 (PA values were adjusted according to Tukey’s post hoc test method). All data are presented as means (± SEM) and statistical tests with PA < 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 MSHE IS2nd. 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 PAco2nd on thermal sensitivity. “Betar” and “Gaussian” error distributions were used for egg survival and MSHE IS2nd 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 PAco2nd = 400 μatm. The effect of elevated PAco2nd (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 PAco2nd on daily mortality rates of Atlantic cod and Polar cod.

Fig. S5. Effects of temperature and PAco2nd 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 not 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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