Widespread ocean acidification (OA) is modifying the chemistry of the global ocean, and the Arctic is recognized as the region where the changes will progress at the fastest rate. Moreover, Arctic species show lower capacity for cellular homeostasis and acid-base regulation rendering them particularly vulnerable to OA. In the present study, we found physiological differences in OA response across geographically separated populations of the keystone Arctic copepod Calanus glacialis. In copepodites stage CIV, measured reaction norms of ingestion rate and metabolic rate showed severe reductions in ingestion and increased metabolic expenses in two populations from Svalbard (Kongsfjord and Billefjord) whereas no effects were observed in a population from the Disko Bay, West Greenland. At pH T 7.87, which has been predicted for the Svalbard west coast by year 2100, these changes resulted in reductions in scope for growth of 19% in the Kongsfjord and a staggering 50% in the Billefjord. Interestingly, these effects were not observed in stage CV copepodites from any of the three locations. It seems that CVs may be more tolerant to OA perhaps due to a general physiological reorganization to meet low intracellular pH during hibernation. Needless to say, the observed changes in the CIV stage will have serious implications for the C. glacialis population health status and growth around Svalbard. However, OA tolerant populations such as the one in the Disko Bay could help to alleviate severe effects in C. glacialis as a species. K E Y W O R D SArctic, ingestion rate, metabolic rate, ocean acidification, pCO2, pH, reaction norm, zooplankton
IntroductionGenetic variation underlies the populations’ potential to adapt to and persist in a changing environment, while phenotypic plasticity can play a key role in buffering the negative impacts of such change at the individual level.MethodsWe investigated the role of genetic variation in the thermal response of the northern shrimp Pandalus borealis, an ectotherm species distributed in the Arctic and North Atlantic Oceans. More specifically, we estimated the proportion transcriptomic responses explained by genetic variance of female shrimp from three origins after 30 days of exposure to three temperature treatments.ResultsWe characterized the P. borealis transcriptome (170,377 transcripts, of which 27.48% were functionally annotated) and then detected a total of 1,607 and 907 differentially expressed transcripts between temperatures and origins, respectively. Shrimp from different origins displayed high but similar level of transcriptomic plasticity in response to elevated temperatures. Differences in transcript expression among origins were not correlated to population genetic differentiation or diversity but to environmental conditions at origin during sampling.DiscussionThe lack of genetic variation explaining thermal plasticity suggests limited adaptability in this species’ response to future environmental changes. These results together with higher mortality observed at the highest temperature indicate that the thermal niche of P. borealis will likely be restricted to higher latitudes in the future. This prediction concurs with current decreases in abundance observed at the southern edge of this species geographical distribution, as it is for other cold-adapted crustaceans.
Inter‐individual variation in phenotypic traits has long been considered as “noise” rather than meaningful phenotypic variation, with biological studies almost exclusively generating and reporting average responses for populations and species’ average responses. Here, we compare the use of an individual approach in the investigation of extracellular acid–base regulation by the purple sea urchin Paracentrotus lividus challenged with elevated p CO 2 and temperature conditions, with a more traditional approach which generates and formally compares mean values. We detected a high level of inter‐individual variation in acid–base regulation parameters both within and between treatments. Comparing individual and mean values for the first (apparent) dissociation constant of the coelomic fluid for individual sea urchins resulted in substantially different (calculated) acid–base parameters, and models with stronger statistical support. While the approach using means showed that coelomic p CO 2 was influenced by seawater p CO 2 and temperature combined, the individual approach indicated that it was in fact seawater temperature in isolation that had a significant effect on coelomic p CO 2 . On the other hand, coelomic [HCO 3 − ] appeared to be primarily affected by seawater p CO 2 , and less by seawater temperature, irrespective of the approach adopted. As a consequence, we suggest that individual variation in physiological traits needs to be considered, and where appropriate taken into account, in global change biology studies. It could be argued that an approach reliant on mean values is a “procedural error.” It produces an artefact, that is, a population's mean phenotype. While this may allow us to conduct relatively simple statistical analyses, it will not in all cases reflect, or take into account, the degree of (physiological) diversity present in natural populations.
Widespread ocean acidification (OA) is transforming the chemistry of the global ocean, and the Arctic is recognised as a region where the earliest and strongest impacts of OA are expected. In the present study, metabolic effects of OA and its interaction with food availability was investigated in Calanus glacialis from the Kongsfjord, West Spitsbergen. We measured metabolic rates and RNA/DNA ratios (an indicator of biosynthesis) concurrently in fed and unfed individuals of copepodite stages CII-CIII and CV subjected to two different pH levels representative of present day and the “business as usual” IPCC scenario (RCP8.5) prediction for the year 2100. The copepods responded more strongly to changes in food level than to decreasing pH, both with respect to metabolic rate and RNA/DNA ratio. However, significant interactions between effects of pH and food level showed that effects of pH and food level act in synergy in copepodites of C. glacialis. While metabolic rates in copepodites stage CII-CIII increased by 78% as a response to food under present day conditions (high pH), the increase was 195% in CII-CIIIs kept at low pH—a 2.5 times greater increase. This interaction was absent for RNA/DNA, so the increase in metabolic rates were clearly not a reaction to changing biosynthesis at low pH per se but rather a reaction to increased metabolic costs per unit of biosynthesis. Interestingly, we did not observe this difference in costs of growth in stage CV. A 2.5 times increase in metabolic costs of growth will leave the copepodites with much less energy for growth. This may infer significant changes to the C. glacialis population during future OA.
Nutritional and organoleptic qualities (taste, smell, texture, appearance) are key characteristics of seafood when it comes to defining consumer choices. These qualities, which are determined by the biochemical properties of the seafood, can be altered by environmental conditions, such as those imposed by ongoing global ocean change. However, these effects have rarely been studied despite their potential important economic and dietary implications: many human communities depend upon seafood as a primary source of nutrition and/or income from the associated seafood industry. The Northern shrimp, Pandalus borealis, makes the 3rd most valuable fishery in Eastern Canada, and figures among the most important fisheries in the NorthEastern Atlantic. This study aimed to determine the impact of combined ocean warming, acidification and hypoxia on (a) muscle mineral content as proxy for nutritional quality, and (b) the taste, smell, texture, and appearance as proxies for organoleptic quality of this commercially important species. These proxies were determined after an exposure of 30 days under laboratory conditions to different ocean global change scenarios of temperature (2, 6, and 10 • C), pH (7.75 and 7.4) and oxygen (100 and 35% relative to air saturation), in isolation and in combination. Shrimp survival was significantly lower (68%) for shrimp exposed to warming and low pH, and even lower (37%) when hypoxia was superimposed, compared to an average survival of 88% for all other treatments. Mineral contents were globally higher in shrimp exposed to the highest temperature, while organoleptic attributes were comparable across all scenarios tested. Thus, while we do not expect nutritional value and organoleptic quality of shrimp, broadly speaking, to be altered by global changes even in areas where conditions will correspond to our warmest (10 • C) and lowest pH (7.4) scenarios, the lower survival rate we report could negatively impact the viability of shrimp populations and consequently the shrimp industry. This may be particularly true for areas that are currently becoming or are expected to become hypoxic.
Species with a wide distribution can experience regionally a wide range of environmental conditions, to which they can acclimatize or adapt. Consequently, the geographic origin of an organism can influence its responses to environmental changes, and therefore its sensitivity to combined global change drivers. This study aimed at determining the physiological responses of the northern shrimp Pandalus borealis, at different levels of biological organization and from four different geographic origins, exposed to elevated temperature and low pH to define its sensitivity to future ocean warming (OW) and acidification (OA). Shrimp sampled within the northwest Atlantic, were exposed for 30 days to combinations of three temperature (2, 6 or 10 °C) and two pH levels (7.75 or 7.40). Survival, metabolic rates, whole-organism aerobic performance and cellular energetic capacity were assessed at the end of the exposure. Our results show that shrimp survival was negatively affected by temperature above 6 °C and low pH, regardless of their origin. Additionally, shrimp from different origins show overall similar whole-organism performances: aerobic scope increasing with increasing temperature and decreasing with decreasing pH. Finally, the stability of aerobic metabolism appears to be related to cellular adjustments specific to shrimp origin. Our results show that the level of intraspecific variation differs among levels of biological organization: different cellular capacities lead to similar individual performances. Thus, the northern shrimp sensitivity to OW and OA is overall comparable among origins. Nonetheless, shrimp vulnerability to predicted global change scenarios for 2100 could differ among origins due to different regional environmental conditions.
Using a targeted metabolomic approach we investigated the effects of low seawater pH on energy metabolism in two late copepodite stages (CIV and CV) of the keystone Arctic copepod species Calanus glacialis. Exposure to decreasing seawater pH (from 8.0 to 7.0) caused increased ATP, ADP and NAD+ and decreased AMP concentrations in stage CIV, and increased ATP and phospho-L-arginine and decreased AMP concentrations in stage CV. Metabolic pathway enrichment analysis showed enrichment of the TCA cycle and a range of amino acid metabolic pathways in both stages. Concentrations of lactate, malate, fumarate and alpha-ketoglutarate (all involved in the TCA cycle) increased in stage CIV, whereas only alpha-ketoglutarate increased in stage CV. Based on the pattern of concentration changes in glucose, pyruvate, TCA cycle metabolites, and free amino acids, we hypothesise that ocean acidification will lead to a shift in energy production from carbohydrate metabolism in the glycolysis toward amino acid metabolism in the TCA cycle and oxidative phosphorylation in stage CIV. In stage CV, concentrations of most of the analysed free fatty acids increased, suggesting in particular that ocean acidification increases the metabolism of stored wax esters in this stage. Moreover, aminoacyl-tRNA biosynthesis was enriched in both stages indicating increased enzyme production to handle low pH stress.
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