Horizon scanning of potential threats to high-Arctic biodiversity, human health and the economy from marine invasive alien species: A Svalbard case study.

The high Arctic is considered a pristine environment compared with many other regions in the northern hemisphere. It is becoming increasingly vulnerable to invasion by invasive alien species (IAS), however, as climate change leads to rapid loss of sea ice, changes in ocean temperature and salinity, and enhanced human activities. These changes are likely to increase the incidence of arrival and the potential for establishment of IAS in the region. To predict the impact of IAS, a group of experts in taxonomy, invasion biology and Arctic ecology carried out a horizon scanning exercise using the Svalbard archipelago as a case study, to identify the species that present the highest risk to biodiversity, human health and the economy within the next 10 years. A total of 114 species, currently absent from Svalbard, recorded once and/or identified only from environmental DNA samples, were initially identified as relevant for review. Seven species were found to present a high invasion risk and to potentially cause a significant negative impact on biodiversity and five species had the potential to have an economic impact on Svalbard. Decapod crabs, ascidians and barnacles dominated the list of highest risk marine IAS. Potential pathways of invasion were also researched, the most common were found associated with vessel traffic. We recommend (i) use of this approach as a key tool within the application of biosecurity measures in the wider high Arctic, (ii) the addition of this tool to early warning systems for strengthening existing surveillance measures; and (iii) that this approach is used to identify high-risk terrestrial and freshwater IAS to understand the overall threat facing the high Arctic. Without the application of biosecurity measures, including horizon scanning, there is a greater risk that marine IAS invasions will increase, leading to unforeseen changes in the environment and economy of the high Arctic.

Photophysiological cycles in Arctic krill are entrained by weak midday twilight during the Polar Night.

Light plays a fundamental role in the ecology of organisms in nearly all habitats on Earth and is central for processes such as vision and the entrainment of the circadian clock. The poles represent extreme light regimes with an annual light cycle including periods of Midnight Sun and Polar Night. The Arctic Ocean extends to the North Pole, and marine light extremes reach their maximum extent in this habitat. During the Polar Night, traditional definitions of day and night and seasonal photoperiod become irrelevant since there are only "twilight" periods defined by the sun's elevation below the horizon at midday; we term this "midday twilight." Here, we characterize light across a latitudinal gradient (76.5° N to 81° N) during Polar Night in January. Our light measurements demonstrate that the classical solar diel light cycle dominant at lower latitudes is modulated during Arctic Polar Night by lunar and auroral components. We therefore question whether this particular ambient light environment is relevant to behavioral and visual processes. We reveal from acoustic field observations that the zooplankton community is undergoing diel vertical migration (DVM) behavior. Furthermore, using electroretinogram (ERG) recording under constant darkness, we show that the main migratory species, Arctic krill (Thysanoessa inermis) show endogenous increases in visual sensitivity during the subjective night. This change in sensitivity is comparable to that under exogenous dim light acclimations, although differences in speed of vision suggest separate mechanisms. We conclude that the extremely weak midday twilight experienced by krill at high latitudes during the darkest parts of the year has physiological and ecological relevance.

A marine zooplankton community vertically structured by light across diel to interannual timescales.

The predation risk of many aquatic taxa is dominated by visually searching predators, commonly a function of ambient light. Several studies propose that changes in visual predation will become a major climate-change impact on polar marine ecosystems. The High Arctic experiences extreme seasonality in the light environment, from 24 h light to 24 h darkness, and therefore provides a natural laboratory for studying light and predation risk over diel to seasonal timescales. Here, we show that zooplankton (observed using acoustics) in an Arctic fjord position themselves vertically in relation to light. A single isolume (depth-varying line of constant light intensity, the value of which is set at the lower limit of photobehaviour reponses of Calanus spp. and krill) forms a ceiling on zooplankton distribution. The vertical distribution is structured by light across timescales, from the deepening of zooplankton populations at midday as the sun rises in spring, to the depth to which zooplankton ascend to feed during diel vertical migration. These results suggest that zooplankton might already follow a foraging strategy that will keep visual predation risk roughly constant under changing light conditions, such as those caused by the reduction of sea ice, but likely with energetic costs such as lost feeding opportunities as a result of altered habitat use.

Nitrate supply and uptake in the Atlantic Arctic sea ice zone: seasonal cycle, mechanisms and drivers.

Nutrient supply to the surface ocean is a key factor regulating primary production in the Arctic Ocean under current conditions and with ongoing warming and sea ice losses. Here we present seasonal nitrate concentration and hydrographic data from two oceanographic moorings on the northern Barents shelf between autumn 2017 and summer 2018. The eastern mooring was sea ice-covered to varying degrees during autumn, winter and spring, and was characterized by more Arctic-like oceanographic conditions, while the western mooring was ice-free year-round and showed a greater influence of Atlantic water masses. The seasonal cycle in nitrate dynamics was similar under ice-influenced and ice-free conditions, with biological nitrate uptake beginning near-synchronously in early May, but important differences between the moorings were observed. Nitrate supply to the surface ocean preceding and during the period of rapid drawdown was greater at the ice-free more Atlantic-like western mooring, and nitrate drawdown occurred more slowly over a longer period of time. This suggests that with ongoing sea ice losses and Atlantification, the expected shift from more Arctic-like ice-influenced conditions to more Atlantic-like ice-free conditions is likely to increase nutrient availability and the duration of seasonal drawdown in this Arctic shelf region. The extent to which this increased nutrient availability and longer drawdown periods will lead to increases in total nitrate uptake, and support the projected increases in primary production, will depend on changes in upper ocean stratification and their effect on light availability to phytoplankton as changes in climate and the physical environment proceed. This article is part of the theme issue 'The changing Arctic Ocean: consequences for biological communities, biogeochemical processes and ecosystem functioning'.

Seafloor warm water temperature anomalies impact benthic macrofauna communities of a high-Arctic cold-water fjord.

Amid the alarming atmospheric and oceanic warming rates taking place in the Arctic, western fjords around the Svalbard archipelago are experiencing an increased frequency of warm water intrusions in recent decades, causing ecological shifts in their ecosystems. However, hardly anything is known about their potential impacts on the until recently considered stable and colder northern fjords. We analyzed macrobenthic fauna from four locations in Rijpfjorden (a high-Arctic fjord in the north of Svalbard) along its axis, sampled intermittently in the years 2003, 2007, 2010, 2013 and 2017. After a strong seafloor warm water temperature anomaly (SfWWTA) in 2006, the abundance of individuals and species richness dropped significantly across the entire fjord in 2007, together with diversity declines at the outer parts (reflected in Shannon index drops) and increases in beta diversity between inner and outer parts of the fjord. After a period of three years with stable water temperatures and higher sea-ice cover, communities recovered through recolonization processes by 2010, leading to homogenization in community composition across the fjord and less beta diversity. For the last two periods (2010-2013 and 2013-2017), beta diversity between the inner and outer parts gradually increased again, and both the inner and outer sites started to re-assemble in different directions. A few taxa began to dominate the fjord from 2010 onwards at the outer parts, translating into evenness and diversity drops. The inner basin, however, although experiencing strong shifts in abundances, was partially protected by a fjordic sill from impacts of these temperature anomalies and remained comparatively more stable regarding community diversity after the disturbance event. Our results indicate that although shifts in abundances were behind important spatio-temporal community fluctuations, beta diversity variations were also driven by the occurrence-based macrofauna data, suggesting an important role of rare taxa. This is the first multidecadal time series of soft-bottom macrobenthic communities for a high-Arctic fjord, indicating that potential periodic marine heatwaves might drive shifts in community structure, either through direct effects from thermal stress on the communities or through changes in environmental regimes led by temperature fluctuations (i.e. sea ice cover and glacial runoff, which could lead to shifts in primary production and food supply to the benthos). Although high-Arctic macrobenthic communities might be resilient to some extent, sustained warm water anomalies could lead to permanent changes in cold-water fjordic benthic systems.

Environmental niche overlap in sibling planktonic species Calanus finmarchicus and C. glacialis in Arctic fjords.

Knowledge of environmental preferences of the key planktonic species, such as Calanus copepods in the Arctic, is crucial to understand ecosystem function and its future under climate change. Here, we assessed the environmental conditions influencing the development stages of Atlantic Calanus finmarchicus and Arctic Calanus glacialis, and we quantified the extent to which their niches overlap by incorporating multiple environmental data. We based our analysis on a 3-year seasonal collection of zooplankton by sediment traps, located on moorings in two contrasting Svalbard fjords: the Arctic Rijpfjorden and the Atlantic-influenced Kongsfjorden. Despite large differences in water temperature between the fjords, local realized ecological niches of the sibling Calanus species overlapped almost perfectly. The exception was the earliest copepodites of C. glacialis in Rijpfjorden, which probably utilized the local ice algal bloom in spring. However, during periods with no sea ice, like in Kongsfjorden, the siblings of both Calanus species showed high synchronization in the population structure. Interestingly, differences in temperature preferences of C. finmarchicus and C. glacialis were much higher between the studied fjords than between the species. Our analysis confirmed the high plasticity of Calanus copepods and their abilities to adapt to highly variable environmental settings, not only on an interannual basis but also in a climate warming context, indicating some resilience in the Calanus community.

Can a key boreal Calanus copepod species now complete its life-cycle in the Arctic? Evidence and implications for Arctic food-webs.

The changing Arctic environment is affecting zooplankton that support its abundant wildlife. We examined how these changes are influencing a key zooplankton species, Calanus finmarchicus, principally found in the North Atlantic but expatriated to the Arctic. Close to the ice-edge in the Fram Strait, we identified areas that, since the 1980s, are increasingly favourable to C. finmarchicus. Field-sampling revealed part of the population there to be capable of amassing enough reserves to overwinter. Early developmental stages were also present in early summer, suggesting successful local recruitment. This extension to suitable C. finmarchicus habitat is most likely facilitated by the long-term retreat of the ice-edge, allowing phytoplankton to bloom earlier and for longer and through higher temperatures increasing copepod developmental rates. The increased capacity for this species to complete its life-cycle and prosper in the Fram Strait can change community structure, with large consequences to regional food-webs.

Shine a light: Under-ice light and its ecological implications in a changing Arctic Ocean.

The Arctic marine ecosystem is shaped by the seasonality of the solar cycle, spanning from 24-h light at the sea surface in summer to 24-h darkness in winter. The amount of light available for under-ice ecosystems is the result of different physical and biological processes that affect its path through atmosphere, snow, sea ice and water. In this article, we review the present state of knowledge of the abiotic (clouds, sea ice, snow, suspended matter) and biotic (sea ice algae and phytoplankton) controls on the underwater light field. We focus on how the available light affects the seasonal cycle of primary production (sympagic and pelagic) and discuss the sensitivity of ecosystems to changes in the light field based on model simulations. Lastly, we discuss predicted future changes in under-ice light as a consequence of climate change and their potential ecological implications, with the aim of providing a guide for future research.

Zooplankton and sediment fluxes in two contrasting fjords reveal Atlantification of the Arctic.

Svalbard fjords are facing a significant increase in Atlantic water inflow, which influences all ecosystem components, thus the objective of this study was to assess how recent Atlantification impacts the functioning of zooplankton community. For this purpose, two year-round operating sediment traps and associated hydrographic instruments, providing continuous time series of zooplankton and sediment fluxes, were deployed in the Atlantic-influenced Kongsfjorden and the typical high Arctic fjord Rijpfjorden. We used multivariate statistical methods to analyze how environmental variables, including the sediment fluxes, influence the zooplankton communities in the fjords. We found out that sedimentation rates were an order of magnitude higher in Kongsfjorden (reaching 39.7 g m-2 d-1 in December) and increased in autumn, while in Rijpfjorden, they peaked in late winter - early spring (2.9 g m-2 d-1 in February). Such sediment flux patterns might result from the redeposition of sediments from shallower, subtidal areas and were probably connected to autumn/winter storms. According to multivariate analyses, zooplankton in Kongsfjorden were significantly influenced by water temperature, which explained 22% of their variation, and the flux of organic and mineral sediments explaining 15% and 7.8%, respectively; while in Rijpfjorden, it was sea ice (25.3%), water temperature (16.2%), salinity (8.1%), and mineral sedimentation (6.3%). The structure of zooplankton communities in both fjords was similar in winter; in Kongsfjorden, zooplankton kept developing through spring and summer, while in the Arctic Rijpfjorden, the community paused until the onset of phytoplankton bloom and sea ice break-up in summer, to finally achieve, in autumn, a similar species and development stage structure as summer in the Atlantic-influenced fjord. Our study demonstrates how integrating multiple pieces of information can provide key insights into the relations between Atlantification, sediment flux, and zooplankton community, thus helping to assess the functioning of high Arctic ecosystems under climate change conditions.

Implications of increasing Atlantic influence for Arctic microbial community structure.

Increasing influence of Atlantic water in the Arctic Ocean has the potential to significantly impact regional water temperature and salinity. Here we use a rDNA barcoding approach to reveal how microbial communities are partitioned into distinct assemblages across a gradient of Atlantic-Polar Water influence in the Norwegian Sea. Data suggest that temperate adapted bacteria may replace cold water taxa under a future scenario of increasing Atlantic influence, but the eukaryote response is more complex. Some abundant eukaryotic cold water taxa could persist, while less abundant eukaryotic taxa may be replaced by warmer adapted temperate species. Furthermore, within lineages, different taxa display evidence of increased relative abundance in reaction to favourable conditions and we observed that rare microbial taxa are sample site rather than region specific. Our findings have significant implications for the vulnerability of polar associated community assemblages, which may change, impacting the ecosystem services they provide, under predicted increases of Atlantic mixing and warming within the Arctic region.

Artificial light during the polar night disrupts Arctic fish and zooplankton behaviour down to 200 m depth.

For organisms that remain active in one of the last undisturbed and pristine dark environments on the planet-the Arctic Polar Night-the moon, stars and aurora borealis may provide important cues to guide distribution and behaviours, including predator-prey interactions. With a changing climate and increased human activities in the Arctic, such natural light sources will in many places be masked by the much stronger illumination from artificial light. Here we show that normal working-light from a ship may disrupt fish and zooplankton behaviour down to at least 200 m depth across an area of >0.125 km2 around the ship. Both the quantitative and qualitative nature of the disturbance differed between the examined regions. We conclude that biological surveys in the dark from illuminated ships may introduce biases on biological sampling, bioacoustic surveys, and possibly stock assessments of commercial and non-commercial species.

The advective origin of an under-ice spring bloom in the Arctic Ocean using multiple observational platforms.

Under-ice blooms of phytoplankton in the Chukchi Sea have been observed, with strong implications for our understanding of the production regimes in the Arctic Ocean. Using a combination of satellite remote sensing of phytoplankton biomass, in situ observations under sea ice from an autonomous underwater vehicle (AUV), and in vivo photophysiology, we examined the composition, magnitude and origin of a bloom detected beneath the sea ice Northwest of Svalbard (Southern Yermak Plateau) in May 2010. In situ concentration of up to 20 mg chlorophyll a [Chl a] m-3, were dominated by the northern planktonic spring species of diatoms, Thalassiosira nordenskioeldii, T. antarctica var. borealis, Chaetoceros socialis species complex and Fragilariopsis oceanica. These species were also found south of the marginal ice zone (MIZ). Cells in the water column under the sea ice were typically high-light acclimated, with a mean light saturation index (E k ) of 138 µmol photons m-2 s-1 and a ratio between photoprotective carotenoids (PPC) and Chl a (w:w) of 0.2. Remotely sensed data of [Chl a] showed a 32,000 km2 bloom developing south of the MIZ. In effect, our data suggest that the observed under-ice bloom was in fact a bloom developed in open waters south of the ice edge, and that a combination of northward-flowing water masses and southward drifting sea ice effectively positioned the bloom under the sea ice. This have implications for our general understanding of under-ice blooms, suggesting that their origin and connection with open water may be different in different regions of the Arctic.

Moonlight Drives Ocean-Scale Mass Vertical Migration of Zooplankton during the Arctic Winter.

In extreme high-latitude marine environments that are without solar illumination in winter, light-mediated patterns of biological migration have historically been considered non-existent [1]. However, diel vertical migration (DVM) of zooplankton has been shown to occur even during the darkest part of the polar night, when illumination levels are exceptionally low [2, 3]. This paradox is, as yet, unexplained. Here, we present evidence of an unexpected uniform behavior across the entire Arctic, in fjord, shelf, slope and open sea, where vertical migrations of zooplankton are driven by lunar illumination. A shift from solar-day (24-hr period) to lunar-day (24.8-hr period) vertical migration takes place in winter when the moon rises above the horizon. Further, mass sinking of zooplankton from the surface waters and accumulation at a depth of ∼50 m occurs every 29.5 days in winter, coincident with the periods of full moon. Moonlight may enable predation of zooplankton by carnivorous zooplankters, fish, and birds now known to feed during the polar night [4]. Although primary production is almost nil at this time, lunar vertical migration (LVM) may facilitate monthly pulses of carbon remineralization, as they occur continuously in illuminated mesopelagic systems [5], due to community respiration of carnivorous and detritivorous zooplankton. The extent of LVM during the winter suggests that the behavior is highly conserved and adaptive and therefore needs to be considered as "baseline" zooplankton activity in a changing Arctic ocean [6-9]. VIDEO ABSTRACT.

Calving rates at tidewater glaciers vary strongly with ocean temperature.

Rates of ice mass loss at the calving margins of tidewater glaciers (frontal ablation rates) are a key uncertainty in sea level rise projections. Measurements are difficult because mass lost is replaced by ice flow at variable rates, and frontal ablation incorporates sub-aerial calving, and submarine melt and calving. Here we derive frontal ablation rates for three dynamically contrasting glaciers in Svalbard from an unusually dense series of satellite images. We combine ocean data, ice-front position and terminus velocity to investigate controls on frontal ablation. We find that frontal ablation is not dependent on ice dynamics, nor reduced by glacier surface freeze-up, but varies strongly with sub-surface water temperature. We conclude that calving proceeds by melt undercutting and ice-front collapse, a process that may dominate frontal ablation where submarine melt can outpace ice flow. Our findings illustrate the potential for deriving simple models of tidewater glacier response to oceanographic forcing.

Is Ambient Light during the High Arctic Polar Night Sufficient to Act as a Visual Cue for Zooplankton?

The light regime is an ecologically important factor in pelagic habitats, influencing a range of biological processes. However, the availability and importance of light to these processes in high Arctic zooplankton communities during periods of 'complete' darkness (polar night) are poorly studied. Here we characterized the ambient light regime throughout the diel cycle during the high Arctic polar night, and ask whether visual systems of Arctic zooplankton can detect the low levels of irradiance available at this time. To this end, light measurements with a purpose-built irradiance sensor and coupled all-sky digital photographs were used to characterize diel skylight irradiance patterns over 24 hours at 79°N in January 2014 and 2015. Subsequent skylight spectral irradiance and in-water optical property measurements were used to model the underwater light field as a function of depth, which was then weighted by the electrophysiologically determined visual spectral sensitivity of a dominant high Arctic zooplankter, Thysanoessa inermis. Irradiance in air ranged between 1-1.5 x 10-5 µmol photons m-2 s-1 (400-700 nm) in clear weather conditions at noon and with the moon below the horizon, hence values reflect only solar illumination. Radiative transfer modelling generated underwater light fields with peak transmission at blue-green wavelengths, with a 465 nm transmission maximum in shallow water shifting to 485 nm with depth. To the eye of a zooplankter, light from the surface to 75 m exhibits a maximum at 485 nm, with longer wavelengths (>600 nm) being of little visual significance. Our data are the first quantitative characterisation, including absolute intensities, spectral composition and photoperiod of biologically relevant solar ambient light in the high Arctic during the polar night, and indicate that some species of Arctic zooplankton are able to detect and utilize ambient light down to 20-30m depth during the Arctic polar night.

Unexpected Levels of Biological Activity during the Polar Night Offer New Perspectives on a Warming Arctic.

The current understanding of Arctic ecosystems is deeply rooted in the classical view of a bottom-up controlled system with strong physical forcing and seasonality in primary-production regimes. Consequently, the Arctic polar night is commonly disregarded as a time of year when biological activities are reduced to a minimum due to a reduced food supply. Here, based upon a multidisciplinary ecosystem-scale study from the polar night at 79°N, we present an entirely different view. Instead of an ecosystem that has entered a resting state, we document a system with high activity levels and biological interactions across most trophic levels. In some habitats, biological diversity and presence of juvenile stages were elevated in winter months compared to the more productive and sunlit periods. Ultimately, our results suggest a different perspective regarding ecosystem function that will be of importance for future environmental management and decision making, especially at a time when Arctic regions are experiencing accelerated environmental change [1].

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.

Diel vertical migration of Arctic zooplankton during the polar night.

High-latitude environments show extreme seasonal variation in physical and biological variables. The classic paradigm of Arctic marine ecosystems holds that most biological processes slow down or cease during the polar night. One key process that is generally assumed to cease during winter is diel vertical migration (DVM) of zooplankton. DVM constitutes the largest synchronized movement of biomass on the planet, and is of paramount importance for marine ecosystem function and carbon cycling. Here we present acoustic data that demonstrate a synchronized DVM behaviour of zooplankton that continues throughout the Arctic winter, in both open and ice-covered waters. We argue that even during the polar night, DVM is regulated by diel variations in solar and lunar illumination, which are at intensities far below the threshold of human perception. We also demonstrate that winter DVM is stronger in open waters compared with ice-covered waters. This suggests that the biologically mediated vertical flux of carbon will increase if there is a continued retreat of the Arctic winter sea ice cover.