Saturday , June 25 2022

The northern cod species face & # 39; & # 39 loss; spawning habitats if global warming exceeds 1.5 ° C



rapid climate change in the North & # 39; the Atlantic and the Arctic is a threat to some of the largest populations of & # 39; fish in the world. The impacts of warming and acidification can be made accessible through the & # 39; risk assessments based on the mechanism and the adequacy projections habitat in the future. We show that the acidification of the ocean causes reduction of embryonic thermal ranges, to identify the suitability of spawning habitats as a critical barrier life story for two abundant species & # 39; cod. Ranges & # 39; & # embryonic tolerance associated with 39; climate simulations show ever increasing CO2 emissions [Representative Concentration Pathway (RCP) 8.5] will deteriorate the suitability of & # 39; the current habitat & # 39; Reproduction both Atlantic cod (Gadus morhua) And Polar cod (Boreogadus saida) By 2100. The moderate heating (RCP4.5) can & # 39; avoid dangerous climate impacts on cod & # 39; Atlantic but still leaves a few areas & # 39; reproduction for the most vulnerable Polar cod, also lose the benefits of & # 39; ocean covered with ice. Emissions after RCP2.6, however, support the further suitability of habitat for these two species, suggesting that risks are minimized if the warming will be "below 2 ° C, if not 1.5 ° C "as promised by the & # 39; Paris Agreement.


The warming and acidification of the ocean (OWA), driven by unabated CO2 are expected to suppress the survival and reproduction of & # 39; many marine organisms (1). Existing knowledge implies that the physiological limits of the stages of the history of early life define species vulnerability to OWA (2). Studies scenarios & # 39; impact & # 39; the worst case is important to raise awareness of the risks and to achieve acceptance of society for & # 39; mitigation policy (3). However, more important is the identification of & # 39; paths & # 39; needed to minimize emission & # 39; be the impact risk and find potential habitats & # 39; refuge of & # 39; endangered species should receive priority in conservation13). However, risk assessments based mechanisms to integrate vulnerable life stages and their specific habitat in & # 39; context & # 39; scenario are not yet available, especially for marine species living in & # 39 ; Arctic regions (4, 5).

The Sub-Arctic seas and the Arctic across Europe & # 39; On (ie, the Iceland Sea, the Norwegian Sea, the East Greenland Sea and the Barents Sea) are expected to experience higher rates of & # 39; ocean warming, acidification and loss of6). These ocean regions previously called Waters & # 39; Norden (7) – are inhabited by populations & # 39; most productive fish, the majority of which carry annual migrations in & # 39; & # 39 specific locations; reproduction (4). The biophysical properties of suitable habitat laying support the survival of the early life stages as well as their spread to areas & # 39; suitable nurseries (8). As the fish embryos are often more sensitive to environmental change by subsequent life stages (2), Embryonic tolerance can & # 39; acts as a key constraint on the adequacy of generation habitat. For example, ranges of & # 39; thermal tolerance are narrower in fish embryos than in other stages of life may represent biogeographical restriction (8) And x & # 39; are likely explained by & # 39; & # 39 incomplete development, cardiovascular and other homeostatic systems (9). Acidification of & # 39; Ocean (OA) caused by elevated CO aquatic2 levels can worsen the disorder & # 39; homeostasis (10), B & # 39; thus reducing thermal spread (2, 11) And possibly reduce the adequacy of generation habitat by reducing the egg survival.

Both Atlantic cod and Polar cod are key members of the fauna of northern fish & # 39; high latitude, but they differ in & # 39; & # 39 terms; Thermal affinity and preference & # 39;4, 5). The cod & # 39; the Atlantic is "thermal ġeneristiku" occupying temperatures waters & # 39; Arctic between -1.5 ° and 20 ° C (12). B & # 39; contrast, the Polar cod is "thermal specialist", endemic to the High Arctic and rarely found in & # 39; temperatures of 3 ° C (13). Because the ranges of & # 39; temperatures overlapping & # 39; juvenile stages of life and & # 39; adults, two species co-exist during migrations & # 39;14). During the winter and spring, however, occurs at cheese & # 39; & # 39 b separate locations, temperatures & # 39; different water and sea ice conditions (Fig. 1). Since Atlantic cod prefers the warm waters (3-7 ° C) of the Polar cod (-1 to 2 ° C), the latter species is considered particularly vulnerable to climate change (5, 14). In addition, other indirect threat to cod reproduction & # 39; Polar is projected loss & # 39; sea ​​ice, which serves as habitat & # 39; nurseries for larvae and young during the spring and summer5).

Fig. 1 Models & # 39; cod distribution in the Atlantic and Polar cod in waters of & # 39; Norden.

(A) Cod in the Atlantic; (B) Polar Cod. The two species populations reproduce during winter and spring (Atlantic cod: from March to May; Cod Polar: from December to March) in & # 39; specific locations for species (ie habitat laying, cod : 3 to 7 ° C, open water; Cod Polar: -1 ° to 2 ° C, closed cover of sea ice). The green arrows indicate the dissemination of eggs and larvae driven surface currents prevalent. During the summer, feed (with green areas) of the two species overlap in part, for example, around Svalbard, which marks the limit of & # 39; North Atlantic cod distribution. The red symbols indicate animal origin (reproductive adults) used in & # 39; this study. The distribution maps were replaced after (4, 13, 33). NEW, the Northeast Water Polynya; FJL, Franz Joseph Land; NZ, Novaya Zemlya.

The spawning aggregations of Atlantic cod and Polar, that & # 39; often include many million individuals, are important resources for humans and other marine predators. For example, the Norwegian fishing Atlantic cod alone generates annual revenue & # 39; USD 800 million (15), While the Polar cod is an essential item of food for many birds and marine mammals (5). The assessment of changes in habitat suitability & # 39; reproduction for these species should therefore focus soċjoekoloġika high relevance (4). Functional responses & # 39; embryos for OWA incorporated into & # 39; model & # 39; habitats can help to identify risks and benefits in space & # 39; of & # 39; emission scenarios ranging, including the objective to limit global warming to 1.5 ° C & # 39; above pre-industrial levels16).

Here, embryonic address ranges & # 39; thermal tolerance under OA cod & # 39; Atlantic and Polar cod. Rates & # 39; & # 39 consumption; oxygen (MO2) Of & # 39; embryos in the eye and larva stage in morphometric vertebral hatch provide insight into energetic restrictions imposed by OWA. The adequacy of breeding habitat has been mapped across the Waters & # 39; Norden under different route Representatives Conference (RCPs) by linking data on egg survival with & # 39; climatic simulations Invoice 5 Interkomparjonali Model Project Contact (CMIP5). The RCPs assume or "no mitigation of greenhouse gases" (RCP8.5), "Interim Mitigation" (RCP4.5), or "strong mitigation" (RCP2.6). The latter scenario was developed with the aim of limiting the increase in global average surface temperature (average land and sea surface) to less than 2 ° C with & # 39; relationship period a & # 39; reference from 1850 to 1900 and is adapted to provide the first estimate for maintaining global warming to "well below 2 ° C, if not 1.5 ° C", as stated in the Agreement & # 39; Paris (16).


Consumption & # 39; embryonic oxygen (MO2) Increased by & # 39; increasing temperature but aside or fell in the warmer temperatures (cod & # 39; Atlantic: ≥9 ° C; Cod Polar: ≥4.5 ° C; Fig. 2, A and B), that is, along with & # 39; conditions (Figure 3), indicative of & # 39; severe heat stress. Embryos acclimated to lower temperatures (<9 ° / 4.5 ° C) and elevated Pco2 (Partial pressure of CO2) Consumed ~ 10% more oxygen compared to & # 39; farmed under control Pco2. This trend was reverse & # 39; back on heating, indicating that the additional oxygen and associated energy demands under conditions of OA can not be f & # 39; high temperatures b & # 39 ; critical way, which leads to reduce the higher thermal ceiling metabolic maintenance. Requirements & # 39; higher power under elevated Pco2 can & # 39; resulting from the cumulative costs & # 39; increased regulation & # 39; acidic base, protein turnover, and repair & # 39; injury (9, 10). The energy allocation functions to support life should receive priority over growth (17), As evidenced by CO2– and a reduction in heating caused by the larvae hatch size (Fig. 2, C to F, and fig. S2). The relative decline in the free area of ​​the body of the larvae due to the elevation sriel Pco2 10% average for cod & # 39; Atlantic (P < 0.001) and 13% for Polar cod (P < 0.001), with the smallest larvae hatched in the warmer temperature (Fig. 2, C and D, and Table S1). Reduction in the larval body size and dry weight (Fig. 2, E and F, and table S1) comply with CO2– entered the reallocation & # 39; energy & # 39; away from growth also observed in other species & # 39; fish (18).

Fig. 2 Effects & # 39; elevated Pco2 rates on & # 39; & # 39 consumption; Oxygen dependent on temperature (MO2) And growth of & # 39; embryos cod and Atlantic cod embryo Polar (right).

(A and B) MO2 was measured at & # 39; embrijoli at eye stage (image). Symbols are means (± SEM shown as bars, n = 6 or 4). The performance curves (lines) are based on n = 28 point data. Weaknesses dark and light indicating intervals of & # 39; & # 39 credible trust; Bayesi 90 and 95%, respectively. (C and D) Free from yellow body in Area larvae hatch was evaluated as an indicator of somatic growth and resource use (yellow). The box plots superimposed b & # 39; individual values ​​show the 25, 50 and 75th percentile; the whiskers forming intervals of & # 39; & # 39 confidence; 95%. (D) a sufficient sample size was available in & # 39; 6 ° C because many people have died or poorly hatched. (E and F) Offset between & # 39; regression lines (b & # 39; & # 39 intervals; confidence & # 39; 95%) indicating CO2related differences in the weight relations of the newly hatched larvae size (image). Subjects were grouped together on 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 indicated in black, while the orange ★ indicate significant CO2 long-temperature treatment (post hoc Tukey test, n = 6 or 4 per treatment). See Table S1 for details of statistical tests. N., unavailable.

Fig. 3 Effects & # 39; elevated Pco2 Egg survival dependent on the temperature in the Atlantic cod and Polar cod.

(A) Cod in the Atlantic; (B) Polar Cod. Symbols represent means (± SEM shown as bars, n = 6). The thermal performance curves (TPCs, lines) of & # 39; each species based on n = 36 data points. Weaknesses dark and light indicating intervals of & # 39; & # 39 credible trust; Bayesi 90 and 95%, respectively. The TPCs have been extrapolated in & # 39; side temperatures by incorporating limits & # 39; tolerance to freezing literature (Materials and Methods). Significant main effects of temperature, Pco2, Or their interaction (T * Pco2) ★ are indicated in black, while the orange ★ indicate significant CO2 long-temperature treatment (post hoc Tukey test, n = 6 or 4 per treatment). See Table S1 for details of statistical tests.

The egg survival has & # 39; outside the preferred temperatures of the Atlantic cod (and ≥9 ≤0 ° C) and Polar cod (≥3 ° C), particularly under Pco2 (Figure 3 and Table S1). Therefore, our results confirm that ranges & # 39; embryonic tolerance representing a tight restriction on the niche & # 39; Atlantic cod in thermal and Polar cod. CO2-MISSIONS of & # 39; deaths at the optimum temperature of & # 39; their reproduction were less pronounced for Atlantic cod (6 ° C, Fig. 3A) than cod Polar (0 to a 1.5 ° C, Fig. 3B). This observation corresponds to the variation in CO2 sensitivity reported by previous studies on early life stages of fish tested the effects of & # 39; OWA only under the best conditions & # 39; temperature (18). However, both species experienced similar CO2– related decrease in egg survival at their respective respective heat (-48% in & # 39; 9 ° C for Atlantic cod and -67% at 3 ° C for Polar cod). increased thermal sensitivity & # 39; embryos under projected Pco2 levels imply a reduction of the range of & # 39; their thermal tolerance and b & # 39; so the reproductive niche species (2). As a consequence, the geographical extent of habitat & # 39; thermally suitable for cod reproduction of Atlantic and Polar cod not only can & # 39; changed to higher latitudes as heating reaction but also because OWA contract.

Compared to & # 39; the contemporary cod sites (known) of Atlantic cod and polar cod in the area of ​​study (blue areas in & # 39; Figure 1, areas surrounded by yellow f & # 39 ; Figure 4), our basic simulations (1985-2004) suggest that the best thermal range & # 39; development & # 39; embryos [>90% potential egg survival (PES), Fig. 4]. However, the area & # 39; to produce thermally suitable habitat (PES> 90%) is greater than the area where the spawn occurs. For example, despite adequate temperatures, no generation of cod in the Atlantic is not currently observed in the North Sea & # 39; Barents (19), Indicating the suitability of spawning habitat also depends on factors other than temperature. Mechanisms to prevent certain areas as suitable for reproduction may include improperly spread of & # 39; eggs and larvae, conditions & # 39; unfavorable feed, and pressure & # 39; predation (8, 19).

Fig. 4 The adequacy of the current cod habitat (baseline) for cod and Atlantic cod in Polar Waters & # 39; Norden.

(A) Cod in the Atlantic; (B) Polar Cod. The adequacy of Spawning habitat is expressed as PSE (% PSE, coded color) by combining experimental data & # 39; survival (Fig. 3) b & # 39; WOA13 temperatures (1 ° x 1 °, 50 m & # 39; on & # 39; marine shelf) for the period 1984-2005 base. The values ​​are programmed on spawning seasons (cod Atlantic: from March to May; Cod Polar: December to March) and Referrals against places where the shipment was documented[Żonimdawrablyellow([Yellowdashedareas([żonimdawrabl-isfar([yellowdashedareas(13, 33)]. The spatial extension of & # 39; habitat & # 39; Reproduction (PES> 90%) suitable thermal is typically greater than that of "committed habitat & # 39; reproduction" because other limiting factors are not considered. The Magenta dotted lines indicate the respective positions of seasonal sea edge (defined as areas with & # 39; ice concentrations> 70% noted that a few sea ice edge among species laying seasons because specific species.

By 2100, the unabated OWA (RCP8.5) is projected to cause a substantial reduction in & # 39; PES f & # 39; main sites & # 39; reproduction in both species (Fig. 5, A to C ). For cod in the Atlantic, PES is projected to decline around Iceland (-10 to -40%) and Faroe Islands (-20 to -60%) and all along the Norwegian coast (-20 to -60 %), a & # 39; breeding sites in the archipelago & # 39; Lofoten (f & # 39; 68 ° N, Fig. 5A). In turn, the extensive shelf regions & # 39; outside Svalbard and the North Sea & # 39; Barents become more adapted (PES, +10 to + 60%) due to heating and reducing the coverage of sea ice. However, the potential gains in northern habitats are constrained by reduced cold tolerance of Atlantic cod embryo under conditions OA and, possibly, unknown constraining factors (see above). Under RCP4.5, reduction in & # 39; cod in Atlantic PES & # 39; some southern laying sites (eg. The Faroe Islands: -10 to -40%) are generally overcome by thermal benefits ( PES, +20 to + 60%) in (between Svalbard, Franz Josef Land and Novaya Zemlya; Fig. 5, D and F).

Fig. 5 Change in habitat suitable thermally cod Atlantic cod (left) and Polar cod (right) in Norden Waters under RCPs.

(A to C) RCP8.5: OWA unabated. (D to F) RCP4.5: intermediate heating (no acidification is considered). (G to I) RCP2.6: Less than 2 ° C global warming (no acidification is considered). Maps showing the change between period PES & # 39; reference (1985-2004; season of Atlantic cod cod: March to May, Polar cod season from December to March, see Fig. 3) and the median & # 39; multimodel CMIP5 projections based on seasonal temperature of the sea surface, from 0 to 50 m; see Materials and Methods) for this century (2081-2100). The black shaded type indicates areas (cells, 1 ° × 1 °) b & # 39; high uncertainty (ie, the change in & # 39; PES f & # 39; that the cell is smaller than the CMIP5 ensemble range; see Materials and methods). The magenta dotted lines represent the ice edge positions marine specific specific grain season for the species (defined as areas with & # 39; ice concentrations> 70%). (C, F, and I) For each chart, the values ​​(change PES) of & # 39; individual cells are summarized under the core density estimates, with the width & # 39; corresponding to the relative occurrence of & # 39; values. The box plots show the 25, 50 and 75th percentile; the ends of the whiskers mark the intervals & # 39; 95%.

The polar cod x & # 39; likely to experience the most dramatic loss of & # 39; spawning habitat south & # 39; Svalbard and Novaya Zemlya (PES, -40 to -80%; RCP8.5; Fig. 5B). In addition, the Polar cod will lose most of its habitat under water except for a small refuge on the eastern shelf of Greenland (Figure 5B). Even warming effects without OA (RCP4.5; Fig. 5, E and F) will substantially reduce the adequacy of & # 39; important spawning habitats for cod from Svalbard Polar (PES -20 to -60%) and Novaya Zemlya (PES, -10 to -40%). The widespread loss of sea ice under RCP8.5 RCP4.5 scenarios and can & # 39; indirectly affect the reproductive success of Polar cod, because snow protects adults lay eggs and predation serves as habitat & # 39; feed for early stages (5). To limit global warming to around 1.5 ° C & # 39; above pre-industrial levels (ie, the median temperature & # 39; RCP2.6) you & # 39; not only reduce reductions in & # 39 ; PES in existing core areas & # 39; reproduction of both species to less than 10% (Fig. 5, G to I) but also keep some sea ice cover.


Our projections suggest that the impacts driven OWA on egg survival and consequent changes in the suitability of habitat layers can be decisive primary & # 39; restrictions dependent on the climate on -merluzz Atlantic and Polar cod. The present findings are consistent with the hypothesis that the thermal ranges of tolerance and embryonic both species habitats are compressed progressive OWA (2). Our results also corroborate the idea that climate change is not imitigat represents an existential threat to species adapted to cold like Polar cod (20), But identified some cold refuge for this species in the High Arctic. The cod in the Atlantic can & # 39; follow the poleward displacement of the thermal top, possibly leading to the establishment of & # 39; this commercially important species in & # 39; regions that are currently dominated by Polar cod. The parallel decline in soil suitability & # 39; outside Iceland and the Norwegian coast (under RCP8.5) implies that, by 2100, south of the Arctic Circle wine (eg. In south of Lofoten) may not be possible for Atlantic cod. The potential displacements of & # 39; & # 39 stocks; fish are commercially important in managing borders and exclusive economic zones pose major challenges not only for national fishermen and conservationists (5) But also international bodies and regulations, which intend to avoid overexploitation, resource conflicts, and degradation of & # 39; pristine ecosystems in the Arctic (4, 21).

However, if global warming is limited to 1.5 ° C & # 39; above pre-industrial levels, then x & # 39; likely that changes in thermal suitability of current habitat laying do not exceed the critical limits Atlantic cod and Polar cod. The residual risk can be further reduced because the two species could potentially adapt to climate change, responding either (i) by & # 39; changes in time and / or place lay in current regions (22) Or (ii) by & # 39; generational processes that enhance physiological tolerance (23). The uncertainties in our results also relate to & # 39; (iii) the reliability and the climate projections resolution CMIP5 (24).

Firstly, the temporary window for spawning north is limited to spring late winter due to the extreme seasonality of primary production of light and associated (food for planktonic larvae) in & # 39; high latitude (> 60 ° N)22). significant changes in the phenology of & # 39; reproduction are therefore likely to occur in & # 39; this region. Instead, North expansions & # 39; & # 39 during nesting periods; Historical and ongoing warming are well documented, especially for Atlantic cod, which extended the activity & # 39; reproducing at West Svalbard in their thirties (25). However, central & # 39; spawning areas (eg., The Lofoten archipelago for the Barents Sea population) have always been busy over the past centuries, possibly due to favorable combinations of & # 39; biotic and abiotic factors maximizing recruitment success8, 22). After breeding, the spreading of eggs and larvae to areas & # 39; suitable nurseries, sometimes with & # 39; over one hundred & # 39; kilometers – plays an important role in & # 39; terms & # 39; connectivity of the life cycle and population replenishment8). Leaks in & # 39; alternative locations (as required under RCP8.5 both species and under RCP4.5 for Polar cod) can & # 39; interfere with the connectivity and thus increases the risk of & # 39; loss & # 39; advocacy and failure & # 39; recruitment (8). Therefore, setting b & # 39; success & # 39; new habitats laying depends heavily on a number of & # 39; factors other than egg survival (i.e., availability of prey, pressure & # 39; predation and connectivity), all of which are currently difficult to predict2, 22).

Second, our results assume that the ranges of & # 39; embryonic tolerance are constantly in & # 39; different populations and generations (i.e., no change evolutionary f & # 39; this century). These assumptions are supported by experimental data[Eżottimata&#39;temperaturasimiligħall-iżvilupptal-bajdfostpopolazzjonijietdifferentita&#39;merluzzflAtlantic([EgsimilartemperatureoptimaforeggdevelopmentamongdifferentAtlanticcodpopulations([eżottimata'temperaturasimiligħall-iżvilupptal-bajdfostpopolazzjonijietdifferentita'merluzzfl-Atlantiku([egsimilartemperatureoptimaforeggdevelopmentamongdifferentAtlanticcodpopulations(26) see also fig. S1], As well as observations on the spot[Eżbidlakonsistentilejnit-tramuntanatal-attivitàtal-merluzztal-merluzzbħalareazzjonigħat-tisħinpreċedenti/continuous([Egconsistentnorthwardshiftofcodspawningactivityinresponsetoprevious/ongoingwarming([eżbidlakonsistentilejnit-tramuntanatal-attivitàtal-merluzztal-merluzzbħalareazzjonigħat-tisħinpreċedenti/kontinwu([egconsistentnorthwardshiftofcodspawningactivityinresponsetoprevious/ongoingwarming(17)]and phylogenetic analysis & # 39; the evolution of the thermal tolerance of marine fish[Eg<01°Cbidlafit-tolleranzatermaligħalkullmiljunsena([Eg<01°Cchangeinthermaltoleranceper1millionyears([eż<01°Cbidlafit-tolleranzatermaligħalkullmiljunsena([eg<01°Cchangeinthermaltoleranceper1millionyears(27)]. The generational plasticity (TGP) you & # 39; to promote short-term adaptation to environmental change through & # 39; nongoġeniku heritage (eg., maternal transmission) (23). However, b & # 39; in contrast to the theory & # 39; TGP, the Atlantic cod experiments suggest that egg viability is weakened in similar degrees & # 39; Heating if women are exposed to heat during the maturing of the gonad (28). This example & # 39; negative TGP correspond to the majority (57%) of & # 39; TGP studies in & # 39; fish observed neutral responses (33%) or negative (24%) (29). Due to the limited capacity for short-term adaptation, x & # 39; likely that the species must abandon their traditional habitats as exceeding the physiological limits (2). Therefore, our results identify not only areas with & # 39; high-risk but potentially & # 39; refuge habitats should receive priority regarding the implementation of marine reserves.

Third, the climate forecasting CMIP5 include uncertainties (24). To some extent, these uncertainties can be reduced and assessed taking into account the results multimodel (see Materials and Methods). The habitats of the coast are poorly represented in the current global climate models (24). The confidence climate impact projections for these areas can & # 39; improved in future studies, mostly b & # 39; elegant way through & # 39; global ocean models multiresolli b & # 39; unstructured mesh (30).

Given & # 39; embryonic intolerance OWA, we show that b & # 39; & # 39 emissions; gas emissions & # 39; effect & # 39; greenhouse unabated, large areas currently used for production will become less suitable for recruitment of Atlantic cod and polar cod, possibly leading to impacts sharp on nets Food-Arctic and associated ecosystem services4, 5). However, our results also highlight that & # 39; mitigation measures, as promised by the Agreement & # 39; Paris, can reduce the effects of climate change in both species. Because the current CO2 trajectories & # 39; emissions giving a chance & # 39; 1% to limit global warming to 1.5 ° C & # 39; above pre-industrial levels (31), Our results require immediate cuts & # 39; emissions after heating compatible with scenarios b & # 39; 1.5 ° C to avoid irreversible damage to the ecosystem in the Arctic and elsewhere.



The cod & # 39; Atlantic caught by & # 39; Fishing with south lines of the Barents Sea (Tromsøflaket: 70 ° 28 & # 39; 00 'N, 18 ° 00 & # 39; 00' E) in & # 39; March 2014 mature fish transported to the Center for Marine -Akwakultura (Nofima AS, Tromso, Norway) and maintained in & # 39; flow tank (25 m3) Under ambient light, salinity [34 practical salinity units (PSU)], And temperature conditions (5 ° ± 0.5 ° C). The polar cod caught in & # 39; Kongsfjorden (West Svalbard: 78 ° 95 & # 39; 02 'N, 11 ° 99 & # 39; 84' E) from trawling in & # 39; January 2014. selected Fish kept in & # 39; tanks to pass through (0.5 m3) And transferred to the Aquaculture Research Station in & # 39; Karvikå (NOFIMA, The Arctic University of Norway ITU, Tromsø). At the station, the fish was kept at & # 39; flow tank (2 m3) F & # 39; water temperature & # 39; 3 ° ± 0.3 ° C (34 PSU) and complete darkness. In both experiments, the gametes used for in vitro fertilization obtained from a strip spawn n = 13 (Polar cod: 12) and men n = 6 women (table S2).

Protocol fertilization

All fertilization made within 30 min after shaving. Each egg batch was divided into & # 39; middle and fertilized using the & # 39; seawater sterilized (34 PSU) filtered and ultraviolet (UV) adjusted before temperature to keep the broodstock (cod Atlantic : 5 ° C; Cod Polar: 3 ° C) Pco2 conditions[control[control[kontroll[controlPco2: 400 μatm, pH(Free Scale) 8:15; high Pco2: 1100 μatm, pHF 7.77]. standardized protocol & # 39; dry fertilization with milt from aliquots n = 3 men used to maximize fertilization success (32).

The fertilization success

The fertilization success was evaluated at & # 39; sub-samples (3 × 100 eggs per batch and Pco2 treatment), which were incubated in a petri products sealed up the stage & # 39; 8/16 cells (Atlantic Cod: 12 hours, 5 ° C; Cod Polar: 24 hours, 3 ° C) photographed under sterjomikroskopju for subsequent evaluation (table S3). These images were also used to determine the average egg diameter & # 39; lot of eggs (30 eggs per batch, table S3).

Setup & # 39; incubation

According to different seasons & # 39; reproduction, two experiments can be conducted with & # 39; consecutively in the same experimental setup as in 2014 (Polar cod: February to April; Atlantic cod from April to May). Eggs fertilized in previously & # 39; one of the control or high Pco2 kept in the respective CO2 trattament u inkubat sakemm jitfaqqas f&#39;ħames temperaturi differenti (merluzz fl-Atlantiku: 0 °, 3 °, 6 °, 9 ° u 12 ° C; Merluzz Polar: 0 °, 1.5 °, 3 °, 4.5 ° u 6 ° C) . Il-firxiet tat-temperatura ġew magħżula biex ikopru l-preferenzi ta &#39;riproduzzjoni tal-merluzz ta&#39; l-Atlantiku (3 sa 7 ° C) (33) u l-merluzz Polar (≤2 ° C) (13) u xenarji ta &#39;tisħin proġettati għar-reġjun rispettiv. Kull grupp ta &#39;trattament ta&#39; lott tal-bajd ġie suddiviż f&#39;żewġ inkubaturi staġnati (20 inkubatur għal kull mara, 120 f&#39;kull esperiment). Biex tevita l-istimi tas-sopravivenza, wieħed biss miż-żewġ inkubaturi ntuża biex jevalwa s-sopravivenza tal-bajd (u l-morfometriċi tal-larva fil-bokkaporti), filwaqt li sotto-kampjuni meħtieġa għal embrijoniċi MO2 ittieħdu miŜuri mit-tieni inkubatur.

Inizjalment, l-inkubaturi kollha (volum, 1000 ml) ġew mimlija b&#39;ilma tal-ilma (34 PSU) iffiltrat (0.2 μm) u sterilizzat bl-UV aġġustat għat-trattament rispettiv tal-fertilizzazzjoni u maħżun b&#39;libs pożittiv. Fir-rigward tal-forniment tal-ossiġnu f&#39;inkubatur staġnat, huwa importanti li jiġi żgurat li l-bajd għandu biżżejjed spazju biex jirranġa ruħhom f&#39;saff wieħed taħt il-wiċċ tal-ilma. Għalhekk aġġustaw l-ammont ta &#39;bajd għal kull inkubatur (Merluzz Atlantiku: ~ 300 sa 500; Merluzz Polar: ~ 200 sa 300) skond differenzi fid-daqs tal-bajd bejn il-merluzz Atlantiku (~ 1.45 mm) u l-Polar cod (~ 1.65 mm). L-inkubaturi mgħobbija kienu mbagħad lokalizzati f&#39;banek tal-baħar tal-baħar termostatati b&#39;mod differenti (volum, 400 litru) biex jiżguraw bidla fit-temperatura bla xkiel ġewwa l-inkubatur. L-inkubaturi trasparenti u l-isfel tal-ponta ġew issiġillati b&#39;kopertura ta &#39;Styrofoam biex tevita l-CO2 outgassing u ċaqliq fit-temperatura. Skond ir-reġimi tad-dawl naturali, il-bajd tal-merluzz fl-Atlantiku rċieva dawl ħafif b&#39;ritmu ta &#39;kuljum ta&#39; 8 sigħat dawl / 16-il siegħa dlam, u bajd tal-merluzz Polar inżammu fid-dlam ħlief għal espożizzjoni ħafifa waqt l-immaniġġjar. Kull 24 siegħa, 90% tal-volum tal-ilma ta &#39;kull inkubatur ġie sostitwit b&#39;ilma tal-baħar iffiltrat (0.2 μm) u sterilizzat bl-UV sabiex jiġi evitat it-tnaqqis tal-ossiġnu. Valv ta &#39;l-iżbokk ġie mmuntat fil-qiegħ ta&#39; l-inkubaturi biex jitbattal l-ilma baħar bil-bajd mejjet, li jitilfu l-kapaċità li jżommu f&#39;wiċċ l-ilma u jinżlu lejn il-qiegħ. Kull banju ta &#39;l-ilma baħar kien fih żewġ tankijiet ta&#39; reservoir ta &#39;60 litru, li kienu wżati biex jiffrankaw minn qabel l-ilma tal-baħar għat-temperatura korrispondenti u Pco2 kundizzjonijiet. It-temperaturi ta &#39;l-ilma ġewwa l-banjijiet ta&#39; l-ilma kienu kkontrollati minn termostats u rreġistrati awtomatikament kull 15-il minuta (± 0.1 ° C) permezz ta &#39;kompjuter ta&#39; akkwarju b&#39;aktar minn kanal wieħed (IKS-Aquastar, IKS Systems, il-Ġermanja). Futur Pco2 il-kundizzjonijiet ġew stabbiliti b&#39;injezzjoni ta &#39;CO pur2 gass ​​fit-tankijiet tal-ġibjuni ta &#39;60 litru mgħaddsa f&#39;kull temperatura. Ġiet użata sistema ta &#39;rispons b&#39;ħafna kanali (IKS-Aquastar), imqabbad ma&#39; sondi individwali tal-pH (IKS-Aquastar) u valvoli tas-solenojdi biex tikkontrolla l-pH tal-ilma u Pco2 valuri. the – Pco2 tat-tankijiet tal-kontenitur ġie mkejjel in situ qabel kull skambju ta &#39;l-ilma b&#39;infraġun ta&#39; l-infra-aħmar Pco2 sonda (Vaisala GMP 343, kumpens manwali tat-temperatura, preċiżjoni ta &#39;± 5 μatm; Vaisala, il-Finlandja). Is-sonda kienet mgħammra b&#39;tagħmir tal-Qari MI70 u pompa ta &#39;aspirazzjoni, li kienet imqabbda ma&#39; membrana ta &#39;degassing (G541, Liqui-Cel, 3M, USA) biex tkejjel Pco2 fl-arja ekwilibrata għal gassijiet ta &#39;l-ilma maħlula (34). Il-kalibrazzjoni tal-fabbrika kienet ikkonfermata bil-kejl ta &#39;l-ilma baħar li qabel kien imbexxex b&#39;taħlita ta&#39; gass tekniku (1000 μatm CO2 fl-arja, Air Liquide, il-Ġermanja). Qabel l-iskambju tal-ilma ta &#39;kuljum, il-valuri tal-pH tat-tankijiet tal-ġibjun ġew imkejla b&#39;elettrodu tal-pH tal-laboratorju sa tliet punti deċimali (Mettler Toledo InLab Routine Pt 1000 b&#39;kumpens ta&#39; temperatura, Mettler Toledo, Isvizzera), li kien imqabbad ma &#39;pH WTW 3310 metru. Kien hemm kalibrazzjoni b&#39;żewġ punti ma &#39;buffers tal-BNS (National Bureau of Standards) fuq bażi ta&#39; day. Biex taqleb l-NBS għall-iskala ta &#39;konċentrazzjoni ta&#39; proton libera għall-pH tal-baħar (35), l-elettrodu ġie kkalibrat bil-baffers tat-tris-HCl għall-ilma baħar (36), li kienu akklimatizzati mat-temperatura tal-inkubazzjoni korrispondenti qabel kull kejl. Il-valuri tal-pH tal-ilma baħar jirreferu għall-iskala tal-pH ħielsa (pHF) matul dan il-manuskritt. Il-parametri ta &#39;l-ilma baħar huma mqassra fil-fig. S3.

Sopravivenza tal-bajd

Il-mortalità tal-bajd ġiet irreġistrata fuq bażi ta &#39;24 siegħa sakemm l-individwi kollha ġewwa inkubatur kienu mietu jew imfaqqsa (fig. S4). Ladarba tfaqqas il-bidu, larva għall-għawm liberu inġabret filgħodu, ewtjenizzati b&#39;doża eċċessiva ta &#39;tricaine methanesulfonate (MS-222), u magħduda wara eżami viżwali għal deformitajiet morfoloġiċi taħt sterjomikroskopju. L-inċidenza ta &#39;deformitajiet larvali kienet ikkwantifikata bħala l-perċentwal ta&#39; trapjaturi li juru deformazzjonijiet severi tas-sġla tal-isfar, kranju, jew kolonna vertebrali. Is-sopravivenza tal-bajd ġiet definita bħala l-perċentwali ta &#39;larva vijabbli mhux formali, li nfetħu min-numru inizjali ta&#39; bajd fertilizzat (fig. S5). Il-proporzjon ta &#39;bajd fertilizzat f&#39;inkubatur kien stmat mis-suċċess medju tal-fertilizzazzjoni tal-lott tal-bajd rispettiv (tabella S3).


Rati ta &#39;konsum ta&#39; ossiġnu (MO2) ta &#39;embriji fl-istadju eyed (f&#39;50% pigmentazzjoni tal-għajnejn, fig. S4) kienu mkejla f&#39;kamra magħluqa ta&#39; respirazzjoni kkontrollata mit-temperatura (OXY0 41 A, Collotec Meßtechnik GmbH, il-Ġermanja). L-kmamar b&#39;ħitan doppji ġew imqabbda ma &#39;termostat li jgħaddi mill-fluss biex tiġi aġġustata t-temperatura tal-kamra tar-respirazzjoni għat-temperatura ta&#39; inkubazzjoni korrispondenti tal-bajd. Il-kejl sar fi tliet kopji bi 10 sa 20 bajda ta &#39;kull mara u kombinazzjoni ta&#39; treatment. Il-bajd tqiegħed fil-kamra b&#39;volum ta &#39;1 ml ta&#39; ilma baħar sterilizzat aġġustat għall-korrispondenti Pco2 treatment. Ġie mqiegħed microrostirrer manjetiku (3 mm) taħt il-bajd li jżomm f&#39;wiċċ l-ilma biex tiġi evitata l-istratifikazzjoni ta &#39;l-ossiġnu fil-kompartiment tar-respirazzjoni. 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).

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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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