Temporal patterns in multiple stressors shape the vulnerability of overwintering Arctic zooplankton.

The Arctic polar nights bring extreme environmental conditions characterised by cold and darkness, which challenge the survival of organisms in the Arctic. Additionally, multiple anthropogenic stressors can amplify the pressure on the fragile Arctic ecosystems during this period. Determining how multiple anthropogenic stressors may affect the survival of Arctic life is crucial for ecological risk assessments and management, but this topic is understudied. For the first time, our study investigates the complex interactions of multiple stressors, exploring stressor temporal dynamics and exposure duration on a key Arctic copepod Calanus glacialis during the polar nights. We conducted experiments with pulse (intermittent) and press (continuous) exposure scenarios, involving microplastics, pyrene and warming in a fully factorial design. We observed significant effects on copepod survival, with pronounced impacts during later stressor phases. We also detected two-way interactions between microplastics and pyrene, as well as pyrene and warming, further intensified with the presence of a third stressor. Continuous stressor exposure for 9 days (press-temporal scenario) led to greater reductions in copepod survival compared to the pulse-temporal scenario, characterised by two 3-day stressor exposure phases. Notably, the inclusion of recovery phases, free from stressor exposure, positively influenced copepod survival, highlighting the importance of temporal exposure dynamics. We did not find behaviour to be affected by the different treatments. Our findings underscore the intricate interactions amongst multiple stressors and their temporal patterns in shaping the vulnerability of overwintering Arctic copepods with crucial implications for managing Arctic aquatic ecosystems under the fastest rate of ongoing climate change on earth.

Seasonal environmental transitions and metabolic plasticity in a sea-ice alga from an individual cell perspective.

Sea-ice microalgae are a key source of energy and nutrient supply to polar marine food webs, particularly during spring, prior to open-water phytoplankton blooms. The nutritional quality of microalgae as a food source depends on their biomolecular (lipid:protein:carbohydrate) composition. In this study, we used synchrotron-based Fourier transform infra-red microspectroscopy (s-FTIR) to measure the biomolecular content of a dominant sea-ice taxa, Nitzschia frigida, from natural land-fast ice communities throughout the Arctic spring season. Repeated sampling over six weeks from an inner (relatively stable) and an outer (relatively dynamic) fjord site revealed high intra-specific variability in biomolecular content, elucidating the plasticity of N. frigida to adjust to the dynamic sea ice and water conditions. Environmental triggers indicating the end of productivity in the ice and onset of ice melt, including nitrogen limitation and increased water temperature, drove an increase in lipid and fatty acids stores, and a decline in protein and carbohydrate content. In the context of climate change and the predicted Atlantification of the Arctic, dynamic mixing and abrupt warmer water advection could truncate these important end-of-season environmental shifts, causing the algae to be released from the ice prior to adequate lipid storage, influencing carbon transfer through the polar marine system.

Biomolecular profiles of Arctic sea-ice diatoms highlight the role of under-ice light in cellular energy allocation.

Arctic sea-ice diatoms fuel polar marine food webs as they emerge from winter darkness into spring. Through their photosynthetic activity they manufacture the nutrients and energy that underpin secondary production. Sea-ice diatom abundance and biomolecular composition vary in space and time. With climate change causing short-term extremes and long-term shifts in environmental conditions, understanding how and in what way diatoms adjust biomolecular stores with environmental perturbation is important to gain insight into future ecosystem energy production and nutrient transfer. Using synchrotron-based Fourier transform infrared microspectroscopy, we examined the biomolecular composition of five dominant sea-ice diatom taxa from landfast ice communities covering a range of under-ice light conditions during spring, in Svalbard, Norway. In all five taxa, we saw a doubling of lipid and fatty acid content when light transmitted to the ice-water interface was >5% but <15% (85%-95% attenuation through snow and ice). We determined a threshold around 15% light transmittance after which biomolecular synthesis plateaued, likely because of photoinhibitory effects, except for Navicula spp., which continued to accumulate lipids. Increasing under-ice light availability led to increased energy allocation towards carbohydrates, but this was secondary to lipid synthesis, whereas protein content remained stable. It is predicted that under-ice light availability will change in the Arctic, increasing because of sea-ice thinning and potentially decreasing with higher snowfall. Our findings show that the nutritional content of sea-ice diatoms is taxon-specific and linked to these changes, highlighting potential implications for future energy and nutrient supply for the polar marine food web.

Is Glacial Meltwater a Secondary Source of Legacy Contaminants to Arctic Coastal Food Webs?

Climate change-driven increases in air and sea temperatures are rapidly thawing the Arctic cryosphere with potential for remobilization and accumulation of legacy persistent organic pollutants (POPs) in adjacent coastal food webs. Here, we present concentrations of selected POPs in zooplankton (spatially and seasonally), as well as zoobenthos and sculpin (spatially) from Isfjorden, Svalbard. Herbivorous zooplankton contaminant concentrations were highest in May [e.g., ∑polychlorinated biphenyls (8PCB); 4.43, 95% CI: 2.72-6.3 ng/g lipid weight], coinciding with the final stages of the spring phytoplankton bloom, and lowest in August (∑8PCB; 1.6, 95% CI: 1.29-1.92 ng/g lipid weight) when zooplankton lipid content was highest, and the fjord was heavily impacted by sediment-laden terrestrial inputs. Slightly increasing concentrations of α-hexachlorocyclohexane (α-HCH) in zooplankton from June (1.18, 95% CI: 1.06-1.29 ng/g lipid weight) to August (1.57, 95% CI: 1.44-1.71 ng/g lipid weight), alongside a higher percentage of α-HCH enantiomeric fractions closer to racemic ranges, indicate that glacial meltwater is a secondary source of α-HCH to fjord zooplankton in late summer. Except for α-HCH, terrestrial inputs were generally associated with reduced POP concentrations in zooplankton, suggesting that increased glacial melt is not likely to significantly increase exposure of legacy POPs in coastal fauna.

Phenology of Oithona similis demonstrates that ecological flexibility may be a winning trait in the warming Arctic.

Rapidly warming Arctic is facing significant shifts in the zooplankton size-spectra manifested as increasing numbers of the small-sized copepod Oithona similis. Here we present a unique continuous data set covering 22 months, on its copepodite structure along with environmental drivers in the Atlantic-influenced high Arctic fjord Isfjorden (Spitsbergen). Abundance maxima of O. similis were observed in September when the highest seawater temperature was recorded. A high concentration of the indicator species of Atlantification Oithona atlantica was also observed at that time. The clear dominance of O. similis in the zooplankton community during the dark, theoretically unproductive season emphasizes its substantial role in sustaining a continuous carbon flow, when most of the large herbivorous copepods fall into sleeping state. The high sex ratio observed twice in both years during periods of high primary production suggests two main reproductive events per year. O. similis reproduced even in very low temperatures (< 0 °C) previously thought to limit their fecundity, which proves its unique thermal tolerance. Our study provides a new insight on ecology of this key copepod of marine ecosystems across the globe, and thus confirm the Climatic Variability Hypothesis assuming that natural selection favour species with such flexible adaptive traits as O. similis.

Seasonal dynamics and life histories of three sympatric species of Pseudocalanus in two Svalbard fjords.

Small copepods are the most diverse and numerous group in high-latitude zooplankton, yet our knowledge of important species remains poor because of the difficulties involved in correct species identification. In this study, we use a molecular method of identification, a species-specific polymerase chain reaction, to provide the first description of the seasonal dynamics and life histories of the important genus Pseudocalanus in two Svalbard fjords with contrasting environments. We conducted monthly investigations in the relatively warm and ice-free Adventfjorden, supplemented with seasonal samples from the colder, seasonally ice-covered Billefjorden. We found three species of Pseudocalanus (the Arctic P. acuspes and P. minutus, and the boreal P. moultoni). Pseudocalanus acuspes had a distinct annual life cycle and dominated during summer, when it actively reproduced. Surprisingly, the boreal P. moultoni was present year-round in both fjords and was the dominant species during winter; the presence of all life stages of this species throughout the year suggests a more continuous reproduction. The Arctic P. minutus was the rarest of the three species and was likely able to complete its life cycle in Billefjorden but not in Adventfjorden. Our study demonstrates that closely related species may have different life strategies and environmental preferences, which presumably make high-latitude zooplankton communities more resilient to climate change impacts on genus but not necessarily on species level.

Seasonal variability in non-consumptive mortality of Arctic zooplankton.

Recent observations from high-latitude marine ecosystems indicate that non-consumptive mortality may be particularly high in Arctic zooplankton during the polar night. Here we have estimated the contribution of dead organisms to the mesozooplankton community in the high Arctic (Svalbard 78-81oN) during the polar night (January), in spring (May) and in late summer (end of August). To identify in situ dead organisms, we used Neutral Red Stain. The dead zooplankton fraction consisted mainly of copepods, while the contribution of dead non-copepods was low in all seasons. The absolute abundance of dead copepods varied little between seasons; however, the relative contribution of dead copepods was highest in January with 11-35% of the copepods classified as dead, in contrast to 2-12% in spring and summer. Furthermore, there were species-specific differences: copepods of the genus Calanus contributed more to the dead fraction of the copepod community during the polar night compared to spring and summer, leading to a higher "dead" biomass in winter. We conclude that non-consumptive winter mortality is considerable in calanoid copepods in the Arctic and an important but so far neglected component of the passive carbon flux, providing carbon in larger portions for higher trophic level consumers during the low-productive winter.

Effects of oil spill response technologies on the physiological performance of the Arctic copepod Calanus glacialis.

A mesocosm study with oil in ice was performed in Van Mijenfjorden in Svalbard to compare effects of the oil spill responses (OSR) in situ burning, chemical dispersion and natural attenuation on the physiological performance of the Arctic copepod Calanus glacialis. Seawater collected from the mesocosms in winter and spring was used in laboratory incubation experiments, where effects on fecal pellet production, egg production and hatching success were investigated over a period of 14 days. Polycyclic aromatic hydrocarbon (PAH) seawater concentrations were lowest in winter. Brine channel formation in spring resulted in an 18 times increase in PAH concentration in the chemical dispersion treatment (1.67 µg L-1), and a 3 fold increase in the natural attenuation (0.36 µg L-1) and in situ burning (0.04 µg L-1) treatments. The physiological performance of female C. glacialis was unaffected by the PAH seawater concentrations. However, a higher mortality and deformity of nauplii was observed in the chemical dispersion treatment, highlighting the importance of considering secondary effects on next generation in future environmental risk assessment of OSR. This study shows that during the ice-covered period, chemical dispersion of oil spills leads to higher PAH exposure than natural attenuation and in situ burning, with potential consequences for recruitment of Arctic copepods.

Sea ice meiofauna distribution on local to pan-Arctic scales.

Arctic sea ice provides microhabitats for biota that inhabit the liquid-filled network of brine channels and the ice-water interface. We used meta-analysis of 23 published and unpublished datasets comprising 721 ice cores to synthesize the variability in composition and abundance of sea ice meiofauna at spatial scales ranging from within a single ice core to pan-Arctic and seasonal scales. Two-thirds of meiofauna individuals occurred in the bottom 10 cm of the ice. Locally, replicate cores taken within meters of each other were broadly similar in meiofauna composition and abundance, while those a few km apart varied more; 75% of variation was explained by station. At the regional scale (Bering Sea first-year ice), meiofauna abundance varied over two orders of magnitude. At the pan-Arctic scale, the same phyla were found across the region, with taxa that have resting stages or tolerance to extreme conditions (e.g., nematodes and rotifers) dominating abundances. Meroplankton, however, was restricted to nearshore locations and landfast sea ice. Light availability, ice thickness, and distance from land were significant predictor variables for community composition on different scales. On a seasonal scale, abundances varied broadly for all taxa and in relation to the annual ice algal bloom cycle in both landfast and pack ice. Documentation of ice biota composition, abundance, and natural variability is critical for evaluating responses to decline in Arctic sea ice. Consistent methodology and protocols must be established for comparability of meiofauna monitoring across the Arctic. We recommend to (1) increase taxonomic resolution of sea ice meiofauna, (2) focus sampling on times of peak abundance when seasonal sampling is impossible, (3) include the bottom 30 cm of ice cores rather than only bottom 10 cm, (4) preserve specimens for molecular analysis to improve taxonomic resolution, and (5) formulate a trait-based framework that relates to ecosystem functioning.

Contrasting physiological responses to future ocean acidification among Arctic copepod populations.

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 pHT 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.

Genetics redraws pelagic biogeography of Calanus.

Planktonic copepods of the genus Calanus play a central role in North Atlantic/Arctic marine food webs. Here, using molecular markers, we redrew the distributional ranges of Calanus species inhabiting the North Atlantic and Arctic Oceans and revealed much wider and more broadly overlapping distributions than previously described. The Arctic shelf species, C. glacialis, dominated the zooplankton assemblage of many Norwegian fjords, where only C. finmarchicus has been reported previously. In these fjords, high occurrences of the Arctic species C. hyperboreus were also found. Molecular markers revealed that the most common method of species identification, prosome length, cannot reliably discriminate the species in Norwegian fjords. Differences in degree of genetic differentiation among fjord populations of the two species suggested that C. glacialis is a more permanent resident of the fjords than C. finmarchicus We found no evidence of hybridization between the species. Our results indicate a critical need for the wider use of molecular markers to reliably identify and discriminate these morphologically similar copepod species, which serve as important indicators of climate responses.

Arctic complexity: a case study on diel vertical migration of zooplankton.

Diel vertical migration (DVM) of zooplankton is a global phenomenon, characteristic of both marine and limnic environments. At high latitudes, patterns of DVM have been documented, but rather little knowledge exists regarding which species perform this ecologically important behaviour. Also, in the Arctic, the vertically migrating components of the zooplankton community are usually regarded as a single sound scattering layer (SSL) performing synchronized patterns of migration directly controlled by ambient light. Here, we present evidence for hitherto unknown complexity of Arctic marine systems, where zooplankton form multiple aggregations through the water column seen via acoustics as distinct SSLs. We show that while the initiation of DVM during the autumnal equinox is light mediated, the vertical positioning of the migrants during day is linked more to the thermal characteristics of water masses than to irradiance. During night, phytoplankton biomass is shown to be the most important factor determining the vertical positioning of all migrating taxa. Further, we develop a novel way of representing acoustic data in the form of a Sound Image (SI) that enables a direct comparison of the relative importance of each potential scatterer based upon the theoretical contribution of their backscatter. Based on our comparison of locations with contrasting hydrography, we conclude that a continued warming of the Arctic is likely to result in more complex ecotones across the Arctic marine system.

Lipid sac area as a proxy for individual lipid content of arctic calanoid copepods.

We present an accurate, fast, simple and non-destructive photographic method to estimate wax ester and lipid content in single individuals of the calanoid copepod genus Calanus and test this method against gas-chromatographic lipid measurements.