Nathalie Morata

Emma Michaud
email: emma.michaud@univ-brest.fr

Marie-Aude Poullaouec

Jérémy Devesa

Manon Le Goff

Rudolph Corvaisier

Paul E Renaud

Climate change and diminishing seasonality in Arctic benthic processes

Keywords: bioturbation, Kongsfjorden, nutrient fluxes, phytodetritus, respiration, Svalbard

de niveau recherche, publiés ou non, émanant des établissements d'enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

INTRODUCTION

One of the dominant concepts guiding current understanding of the functioning of Arctic marine ecosystems is the overriding role of dramatic seasonality in physical drivers. Indeed, intense but short-lived algal blooms characterize many Arctic areas and are coupled to the return of sunlight, melting of sea ice, and stratification of the water column. These blooms fuel both pelagic and benthic food-webs, and sustain migratory fish, seabirds, and mammals during the short summer. The lack of primary production during the long polar night has resulted in an assumption of dormancy in many ecosystem elements [START_REF] Berge | Unexpected Levels of Biological Activity during the Polar Night Offer New Perspectives on a Warming Arctic[END_REF], but this has recently been challenged by evidence of active functioning throughout the ecosystem [START_REF] Berge | In the dark: A review of ecosystem processes during the Arctic polar night[END_REF][START_REF] Berge | POLAR NIGHT Marine Ecology: Life and Light in the Dead of Night[END_REF], including by seafloor communities [START_REF] Renaud | Benthic Communities in the Polar Night[END_REF].

For Arctic seafloor communities, generally presumed to be limited by labile carbon [START_REF] Piepenburg | Recent research on Arctic benthos: common notions need to be revised[END_REF], ecological functioning shows strong spatial [START_REF] Clough | Infaunal density, biomass and bioturbation in the sediments of the Arctic Ocean[END_REF][START_REF] Oleszczuk | Benthic macrofaunal bioturbation activities from shelf to deep basin in spring to summer transition in the Arctic Ocean[END_REF] and seasonal [START_REF] Bourgeois | Organic matter remineralization in marine sediments: A Pan-Arctic synthesis[END_REF][START_REF] Grant | Sediment properties and benthic-pelagic coupling in the North Water[END_REF][START_REF] Link | Spring-to-summer changes and regional variability of benthic processes in the western Canadian Arctic[END_REF][START_REF] Renaud | Seasonal variation in benthic community oxygen demand: A response to an ice algal bloom in the Beaufort Sea[END_REF][START_REF] Rysgaard | Seasonal carbon and nutrient mineralization in a high-Arctic coastal marine sediment, Young Sound, Northeast Greenland[END_REF] variability linked to patterns of food availability. In spring and summer, intense pulses of fresh material can reach the seafloor, such as ice-derived material or phytodetritus [START_REF] Boetius | Export of Algal Biomass from the Melting Arctic Sea Ice[END_REF][START_REF] Morata | A multiple biomarker approach to tracking the fate of an ice algal bloom to the sea floor[END_REF], upon which benthic communities react in both field and experimental studies by quickly increasing respiration and bioturbation rates [START_REF] Renaud | Seasonal variation in benthic community oxygen demand: A response to an ice algal bloom in the Beaufort Sea[END_REF][START_REF] Morata | Impact of early food input on the Arctic benthos activities during the polar night[END_REF]. These findings are consistent with the paradigm of pelagic-benthic coupling, which posits that stocks and processes in seafloor communities generally mirror spatial and temporal patterns in pelagic production and flux [START_REF] Graf | Benthic-pelagic coupling: a benthic view[END_REF]17].

Such coupling has been suggested to be more pronounced in high-latitude environments due in large part to the pulsed or spatially discrete nature of food arrival on the seafloor [START_REF] Petersen | Differences in energy flow through major components of subarctic, temperate and tropical marine sheif ecosystems[END_REF]. Many of the pioneering studies of these processes, however, have been conducted on open shelves and areas with considerable sea-ice cover.

Climatic change has led to strong declines in sea-ice cover, thickness, and the length of the sea-ice season over the past decades [START_REF] Onarheim | Seasonal and Regional Manifestation of Arctic Sea Ice Loss[END_REF], and has resulted in changes in phenology and composition of phytoplankton blooms and flux patterns [START_REF] Wassmann | Future Arctic Ocean Seasonal Ice Zones and Implications for Pelagic-Benthic Coupling[END_REF][START_REF] Leu | Arctic spring awakening -Steering principles behind the phenology of vernal ice algal blooms[END_REF]. Further, increased temperature and light availability (due to reduced ice cover) result in increased benthic algal production in nearshore regions [START_REF] Krause-Jensen | Seasonal sea ice cover as principal driver of spatial and temporal variation in depth extension and annual production of kelp in Greenland[END_REF], with predictions of larger inputs of (macro-) algal detritus to benthic systems in a warmer Arctic. How predicted and observed changes in amount and seasonality of labile carbon will affect Arctic seafloor communities is unclear, but their processes are vital to regenerating nutrients in these otherwise oligo-to meso-trophic systems. Furthermore, fjords are sites of disproportionately high carbon sequestration on a global scale [START_REF] Smith | High rates of organic carbon burial in fjord sediments globally[END_REF], and climate-driven changes in cycling may have implications for climate feedback processes. Kongsfjorden, a high Arctic fjord on the west coast of Svalbard, has observed a dramatic reduction in seasonal ice-cover, and except for inner bays, has been largely ice free in winter since 2006 [START_REF] Pavlova | Changes in Sea-Ice Extent and Thickness in Kongsfjorden, Svalbard (2003-2016)[END_REF]. The fjord still exhibits strong seasonality in primary production and vertical fluxes to the seafloor [START_REF] Lalande | Spatial and temporal variability in export fluxes of biogenic matter in Kongsfjorden[END_REF][START_REF] Hegseth | Phytoplankton Seasonal Dynamics in Kongsfjorden, Svalbard and the Adjacent Shelf[END_REF] but little seasonal variability in infaunal community structure [START_REF] Włodarska-Kowalczuk | Do benthic meiofaunal and macrofaunal communities respond to seasonality in pelagial processes in an Arctic fjord (Kongsfjorden, Spitsbergen)?[END_REF][START_REF] Mazurkiewicz | Seasonal constancy (summer vs. winter) of benthic size spectra in an Arctic fjord[END_REF]. Sediment processes, such as oxygen and nutrient fluxes and bioturbation rates, have not been investigated but are critical to understanding ecosystem functioning in rapidly changing Arctic environments.

In this study, we quantify seasonal differences in (1) sediment properties, (2) bioturbation and biogeochemical-cycling rates at three locations in Kongsfjorden with different ice-cover and infaunacommunity composition, and (3) identify mechanisms linking environmental drivers and ecological processes.

Results offer insight into the response of benthic communities to a changing Arctic, and how current paradigms of ecosystem functioning may be challenged over the coming decades.

MATERIAL AND METHODS

Study area

Kongsfjorden (79°N and 12°E) is 27 km long, 10 km wide, and is located on the Northwestern part of Spitsbergen Island in the Svalbard Archipelago (Figure 1). Because of its open connection to Fram Strait, it is largely influenced by advection of transformed Atlantic waters [START_REF] Cottier | Arctic fjords: a review of the oceanographic environment and dominant physical processes[END_REF]. In the past, the fjord was regularly covered by sea ice, but because of increased advection of Atlantic water, it experiences variable and reduced sea-ice, with mostly ice-free years since 2005/2006 [START_REF] Cottier | Arctic fjords: a review of the oceanographic environment and dominant physical processes[END_REF]. The inner part of the fjord is still rather "Arctic" because of the influence of four large tidal glaciers. Three sampling stations were selected along a gradient from the inner part of the fjord, to the fjord opening: the inner-fjord station (78°54 N, 12°28 E, 80 m deep, Station A) was located at 1.4 km from the head of the fjord under the direct influence of the tidal glacier inputs; the middle-fjord station (78°567 N, 11°56E, 295 m deep, Station B) was located midway between the tidal glacier and the ocean; and the outer station (78°59 N, 11°32 E, 305 m deep, Station C) was located 24 km from the head of the fjord, near the fjord mouth. All stations were visited in May, August and October 2012, and in August 2014 and January 2015. However, due to technical difficulties, it was not possible to perform sediment cores incubations in May and August 2012 at the inner station. The middle and outer stations were also visited in January 2013 period.

Field sampling

During each field campaign, nine sediment cores (12.7 cm diameter, 10 cm height) were collected from each station with a HAPS corer (KC Denmark), except in January 2013 where the sediment cores were collected using a box corer (45 cm x 45 cm). The top 2 cm of sediment from three cores were sliced after collection for determination of the sedimentary organic matter quantity and quality (e.g., chlorophyll and phaeopigments; total organic carbon and total nitrogen contents: TOC, TN). Sediments were gently homogenized and frozen (-20°C) for further analyses. The six remaining cores were kept in a dark cold room at 2°C for benthic processes measurements.

Sediment core incubation for benthic fluxes and bioturbation activities measurements

Sediment cores were filled (~1L) with recently collected bottom water (2-3 °C, 35 ‰, [START_REF] Calleja | Effects of increase glacier discharge on phytoplankton bloom dynamics and pelagic geochemistry in a high Arctic fjord[END_REF]) and aerated to keep oxygen saturation. The cores were acclimated in the cold room for 24 h (2-3 °C), where upon overlying water was changed to remove the released metabolites, and 5 g of fluorescent luminophores (red, 63-90 µm) were homogeneously introduced to the overlying water to quantify biological sediment reworking activity [START_REF] Oleszczuk | Benthic macrofaunal bioturbation activities from shelf to deep basin in spring to summer transition in the Arctic Ocean[END_REF]. In order to measure nutrient fluxes and sediment oxygen demand (SOD), cores were then sealed using tops that provided constant stirring of the overlying water [START_REF] Morata | Impact of early food input on the Arctic benthos activities during the polar night[END_REF]. Oxygen concentrations were monitored every 4 to 6 h using spot sensors (Presens A/S; Germany) [START_REF] Morata | Impact of early food input on the Arctic benthos activities during the polar night[END_REF]. Incubations were terminated after 24 h when 15-20 % of the oxygen had been consumed and SOD was measured as the (negative) slope of the regression line between oxygen concentration and time [START_REF] Morata | Impact of early food input on the Arctic benthos activities during the polar night[END_REF]. Sixty milliliters of overlying waters were sampled with a syringe at the beginning and at the end of the 24h incubation for nutrient analyses. Nutrient fluxes were measured as a difference in nutrient concentration between the two sampling times [START_REF] Morata | Impact of early food input on the Arctic benthos activities during the polar night[END_REF]. Water samples for nitrate + nitrite (NO3 -+ NO2 -), ammonium (NH4 + ) and phosphate (PO4 3-) were filtered (0.2 µm) and directly frozen for future analyses, while filtered samples for silicate (Si(OH)4 -) were kept at +4°C. Cores were then reopened and kept with constant aeration by bubbling and by renewing overlying water every three days. Cores were incubated in those conditions with the luminophores for 10 days [START_REF] Oleszczuk | Benthic macrofaunal bioturbation activities from shelf to deep basin in spring to summer transition in the Arctic Ocean[END_REF]. At the end of the experiment, the sediment cores were sliced into 0.5-cm layers from 0 to 5 cm depth, 1-cm layers from 5 to 10 cm depth and 2-cm layers from 10 to 18 cm depth. Each slice was carefully homogenized and kept for luminophores quantification.

Laboratory analyses

2.4.1: Bulk sediment analyses

At the laboratory, sediments were freeze-dried and gently crushed to powder and homogenized for bulk sediment analyses. Dry bulk sediment density (δ) was determined for each sample by using the known sediment volume. Pigments (chlorophyll a (chla) and phaeopigments (phaeo)) were analyzed fluorometrically [START_REF] Morata | Impact of early food input on the Arctic benthos activities during the polar night[END_REF]. Organic matter (OM) content was measured as loss on ignition (450°C, 4 h). Total organic carbon (TOC) and total nitrogen (TN) contents were measured by the Thermo Quest Flash EA 1112 CHN analyser [START_REF] Morata | Impact of early food input on the Arctic benthos activities during the polar night[END_REF].

Biomass of TOC and pigments contents was calculated (TOCbm, chlabm, and phaeobm) as ratios (Chla/phaeo; C-Chla/TOC) over the 0-2 cm sediment layer.

2.4.2: Nutrient fluxes

Nitrate + nitrite, silicate, and phosphate were analyzed by colorimetry on a Bran+Luebbe Autoanalyzer 3, and ammonium was analyzed by fluorometry [START_REF] Morata | Impact of early food input on the Arctic benthos activities during the polar night[END_REF]. Analytical precision for nutrient analyses was 0.05 µM. Fluxes were calculated from the slopes of the linear regressions of nutrient concentrations against time.

2.4.3: Bioturbation measurements

Luminophore detection and counting for quantification of the tracer transport modes were made following to [START_REF] Oleszczuk | Benthic macrofaunal bioturbation activities from shelf to deep basin in spring to summer transition in the Arctic Ocean[END_REF]. This model simultaneous quantifies the biodiffusion-like transport (Db coefficient; cm 2 .y -1 ) and the nonlocal transport of the tracers (r coefficient; y -1 ). It adjusts a theoretical curve of the tracer distribution with depth on experimental data. The best fit between the observed and modeled tracer distribution is estimated by the least squares method and produces the best Db and r coefficients.

Phil. Trans. R. Soc. A.

Data analyses

The influences of time and location on biogeochemical fluxes, sediment variables and bioturbation coefficients were tested using a two-way analysis of variance with season (January, May, August, October from 2012 to 2015) and stations (inner, middle, outer) as fixed factors. To satisfy homoscedasticity and normality requirements, oxygen and silicate fluxes were log(x+1) and square-roots transformed, respectively. Parametric analyses (ANOVA) and pairwise comparison tests (Tukey's HSD) were then applied to these variables and to TOC and TN. Differences in other parameters (C/N, TOCbiom, Chlabiom, Phaeobiom, C-Chla/TOC, Chla/Phaeo, ammonia, nitrate+nitrite, and phosphate fluxes, Db and r coefficients) were tested using the non-parametric two-way analysis of variances (Sheirer-Ray-Hare test) followed by the Wilcoxon pairwise comparison test with Bonferroni corrections, due to the non-homoscedasticity of the data and the unbalanced design [START_REF] Sokal | Biometry. The principles and practice of statistics in biological research[END_REF].

In order to determine which biogeochemical variables, benthic fluxes, and bioturbation coefficients explained most variability among studied stations between 2012 and 2015, a principle components analysis (PCA) was performed using the "factomine" Rstudio package [START_REF] Lê | FactoMineR: An R Package for Multivariate Analysis[END_REF]. Data were normalized prior to analysis.

Correlation analyses were then used to quantify the relatedness between variables using the non-parametric Spearman coefficient after data normality verification.

RESULTS

Sediment organic matter and pigments

OM (9%), TOC (1.6%) and TN (0.2%) were significantly higher at outer Station "C", followed by the middle Station "B" and the inner station "A" (Table 1, supplementary figure 1,S1). No temporal changes in % OM, TOC and TN were observed at Station A. In the outer station, OM, TOC and TN contents were significantly higher in January 2015 than in August 2014 and October 2012 (table 1, Suppl. Material. 1). OM followed the same trends in the middle station, but TOC was lower there in January 2015 than in August 2012, 2014 and May 2012 (Table 1, supplementary figure 1,S1). Significantly lower biomass of TOC (TOCbm ~ 50-100 mg m -²) was found at Station A compared to the two other stations for each date (Table 1, Figure 2a, supplementary figure 1, S1). Seasonal decreasing of TOCbm was only statistically significant at Station B in January 2015 (figure 2a). Biomass of Chl-a (Chlabm) was highest (60-70 mg m -²)) near the glacier in May and August 2012 (table 1, figure 2b). While the Chlabm remained stable over time at station B, it significantly decreased in January 2015 in stations A and C (10 mg m -²; figure 2b, table 1). Biomass of phaeopigments (Phaeobm) was significantly different between all station pairs, being significantly the lowest near the glacier (50 mg m -²), followed by the outer (~120 mg m -²) and middle (~150 mg m -²) stations (figure 2c). Phaeobm did not change seasonally at station B, but significantly decreased in January 2015 at the two other stations (table 1, figure 2c).

Chla:phaeo and C-Chla:TOC ratios were both significantly higher at the station near the glacier in May and August 2012, whereas it decreased significantly in January 2015. Chla:phaeo ratios and C-Chla:TOC ratios were consistent at the middle and outer stations for the entire sampling period. Pigment biomass and their respective ratios were highly variable in October between the sediment cores at station A (Table 1, Figure 2).

Bioturbation coefficients

The biodiffusion coefficient Db ranged from 0 to 3 cm 2 y -1 along the fjord; mean values were significantly higher in May 2012 (2-3 cm 2 y -1 ), than in August 2012, 2014, October 2012 and January 2015 (Db < 0.5 cm 2 y -1 ; p<0.00002) for middle and outer stations (table 1, figure 3). The non-local transport coefficient (r) ranged from 0 to 8 y -1 over the study area and was significantly lowest at the inner station in October 2012, August 2014 and January 2015 (table 1, figure 3). While the mean r remained stable over time at the middle station, it was significantly higher in October 2012 for the outer station (p<0.01) (table 1, figure 3).

Oxygen and nutrient fluxes

Station A presented no data (nd) in May, August 2012, and January 2013 since core incubation at this station was not possible during these months. SOD was lowest at the inner station in October 2012, August 2014 and in January 2015 (Figure 4a, Table 1) and remained stable over the three sampling periods (6-7 mmol O2 m -² d -1 ).

For the middle and outer stations, SOD was similar (10-12 mmol m -² d -1 ) and did not vary seasonally (p>0.12, Table 1), although SOD tended to be higher in the months of August 2012 and 2014 at the middle station.

Nutrient fluxes were measured at the middle and outer stations in May, August, October 2012, and January 2015 and during October 2012 and January 2015 at the inner station (Figure 4 b-e, Table 1). Silicate was always released from the sediment and significant highest rates were at the middle and outer stations (1.5 -2 mmol m - ² d -1 , p<0.05), mainly in August and October 2012 (Figure 4b, table 1). Ammonium uptake was significant and consistent at the outer station (-0.1 mmol m -² d -1 ; p<0.05, table 1, figure 4c). Low levels of ammonium release were measured in the middle station (0.1 mmol m -² d -1 ) with no significant seasonal change. At station A, ammonia fluxes were opposite with high ammonia release in October 2012 (0.4 mmol m -² d -1 ) and ammonia uptake in January 2015 (-0.5 mmol m -² d -1 ). Nitrate + nitrite showed a consistent pattern going from significant NO3+NO2 uptake in May 2012 (p<0.05, table 1) at stations B and C to release in October, August 2012 and January 2015 for all stations (Figure 4d). Net phosphate fluxes were quite low (< 0.04 mmol m -² d -1 ) and showed different significant seasonal patterns among the three stations (Figure 4e, Table 1, p<0.05).

Phosphate influxes were measured at station A in October 2012 and in January, and in station C in May and January (Figure 4d). Phosphate was released and significantly highest in October 2012 at the stations B and C (p<0.05, table 1).

Environmental variables

The PCA analysis explained 59% of the variability among sampling stations and dates: the first axis explained 37% and the second axis 22% (Figure 5, supplementary figure 2,S2). The most important variables (and their loadings) defining the first axis were TOCbm (0.89), silicate fluxes (0.80), r (0.76), phaeobm (0.75), PO4 3-fluxes (0.46), SOD (-0.54), NH4 + fluxes (-0.54), C-chla:TOC (-0.75), chla:phaeo (-0.83), while chlabm (0.96), chla (0.93), NH4 + fluxes (0.63), C-chla:TOC (0.60), phaeobm (0.51), and C:N (-0.46) defined the second axis. Stations were separated into two groups on the basis of PCA results: Station A alone and stations B and C together. Time points at Sta A are distributed along a gradient from lowest values of chla and NH4 + flux in January to highest in October. The opposite gradient was observed for C/N. Sampling date for stations B and C had little effect on station groupings, and these stations were characterized by the PCA as having high SOD, phaeobm, TOCbm , nitrate+nitrite, phosphate and silicate fluxes, and non-local bioturbation rates. Biogeochemical fluxes were significantly inter-correlated, SOD was positively correlated with ammonium uptake, and silicate and phosphate efflux to overlying waters as well as chla:phaeo and C-chla:TOC ratios (table 2). SOD was negatively correlated with phaeobm and non-local bioturbation (table 2). Chlabm was positively correlated with ammonium flux (table 2). Both biodiffusion and nitrate+nitrite fluxes were not correlated with any measured variables.

DISCUSSION

Spatial and temporal differences in sediment properties

In Kongsfjorden, previous studies have shown seasonal changes in pelagic production. In 2012, a mooring in mid-Kongsfjorden registered a strong diatom-dominated spring bloom from April to mid-May, with moderate Phil. Trans. R. Soc. A. fluorescence from mid-June until July [START_REF] Hegseth | Phytoplankton Seasonal Dynamics in Kongsfjorden, Svalbard and the Adjacent Shelf[END_REF]. A seasonal sediment-trap study conducted from 2012-2013 documented a sedimenting bloom in May as increased POC and chl a flux at all three stations, continuing into August at the glacier station (Station A) [START_REF] Lalande | Spatial and temporal variability in export fluxes of biogenic matter in Kongsfjorden[END_REF]. Another study [START_REF] Bourgeois | Glacier inputs influence organic matter composition and prokaryotic distribution in a high Arctic fjord (Kongsfjorden, Svalbard)[END_REF] found that the sediments near the glacier were lithogenic-dominant depleted in biopolymeric carbon (the sum of the main macromolecules: lipids, proteins and carbohydrates) compared to the entrance of the fjord and that the sedimentary isotopic signature showed different sources between the inner (fresh diatoms, lithogenic material with calcareous benthic foraminifers) and outer (faecal pellets, degraded phytoplankton cells) stations. Recently, non-pelagic sources of organic carbon have been suggested to be important for biogeochemical cycling in Kongsfjorden and many coastal sites in the Arctic. These other sources, including macroalgal detritus [START_REF] Renaud | Seasonal variation in benthic community oxygen demand: A response to an ice algal bloom in the Beaufort Sea[END_REF], terrestrially-derived carbon [START_REF] Kędra | The shallow benthic food web structure in the high Arctic does not follow seasonal changes in the surrounding environment[END_REF][START_REF] Harris | Do high Arctic coastal food webs rely on a terrestrial carbon subsidy?[END_REF], and microphytobenthos [START_REF] Woelfel | Microphytobenthos of Arctic Kongsfjorden (Svalbard, Norway): biomass and potential primary production along the shore line[END_REF], may be partly responsible for the higher sedimentary TOC at middle and outer Kongsfjorden stations, whereas the high inorganic sediment load at the glacier station dilutes any of these inputs resulting in consistently low TOC levels. These sources were not measured in this study, however.

It has been suggested that changes in the quality of the organic matter on the seafloor can be reflected in sedimentary TOC or pigments [START_REF] Morata | Spatial and seasonal variations in the pelagic-benthic coupling of the southeastern Beaufort Sea revealed by sedimentary biomarkers[END_REF]. Although sediment OM, TC, TN contents and TOCbiom were higher in the middle and outer stations in our study, biogenic silica and fecal-pellet carbon fluxes, indicating zooplankton grazing of diatoms at these same stations in May [START_REF] Lalande | Spatial and temporal variability in export fluxes of biogenic matter in Kongsfjorden[END_REF], likely explain the low chla/Phaeo and C-chl/TOC ratios in sediments at Stations B and C year-round. Low zooplankton grazing is suggested for Station A [START_REF] Lalande | Spatial and temporal variability in export fluxes of biogenic matter in Kongsfjorden[END_REF][START_REF] Bourgeois | Glacier inputs influence organic matter composition and prokaryotic distribution in a high Arctic fjord (Kongsfjorden, Svalbard)[END_REF], allowing fresher sedimenting material at this station.

Although temporal changes were not reflected in sediment organic parameters (OM, TC, TN, TOCbiom) at station A (glacier station), temporal decline in sediment pigments (chl a, phaeopigments, chla/Phaeo and Cchl/TOC ratios) were observed at this station. This is perhaps to be expected due to the seasonal sources of phytopigments relative to the larger pool of OC of mixed lability in the sediments. This shows that sediment pigment content and biomass are determined by the intensity of POC (grazed, faecal pellets) and phytoplankton (ungrazed) downward export fluxes over the year. Elevated export fluxes observed in May 2012 near the station result from the phytoplankton bloom and the release of particles from glacier melting, while during the important melt period in August the turbid waters likely dampen phytoplankton development [START_REF] Lalande | Spatial and temporal variability in export fluxes of biogenic matter in Kongsfjorden[END_REF]. This is more obvious in August 2014, which was a warm year for the Kongsfjorden with the inner section receiving warm Atlantic waters accelerating the glacier melt [START_REF] Luckman | Calving rates at tidewater glaciers vary strongly with ocean temperature[END_REF][START_REF] Promińska | Kongsfjorden and Hornsund hydrography -comparative study based on a multiyear survey in fjords of west Spitsbergen[END_REF][START_REF] Holmes | Relating ocean temperatures to frontal ablation rates at Svalbard tidewater glaciers: Insights from glacier proximal datasets[END_REF]. The month of January in this region is marked by a decline in the development of autotrophic organisms and in glacial melt both caused by the colder temperatures and polar night [START_REF] Lalande | Spatial and temporal variability in export fluxes of biogenic matter in Kongsfjorden[END_REF]. Once deposited at the sediment surface, fresh organic material (ungrazed) is slowly consumed over the following months since the benthic biomass and diversity [START_REF] Włodarska-Kowalczuk | Do benthic meiofaunal and macrofaunal communities respond to seasonality in pelagial processes in an Arctic fjord (Kongsfjorden, Spitsbergen)?[END_REF], and bioturbation activities (this study) remain low at this station. In contrast, the export fluxes observed in the middle and outer stations remained elevated and stable over time due to the continuous intrusion of warm Atlantic waters and associated phytoplankton communities until the mid-fjord [START_REF] Lalande | Spatial and temporal variability in export fluxes of biogenic matter in Kongsfjorden[END_REF][START_REF] Promińska | Kongsfjorden and Hornsund hydrography -comparative study based on a multiyear survey in fjords of west Spitsbergen[END_REF], favouring the match between phytoplankton bloom and copepod grazing, and POM fluxes. However, sedimenting OM does not accumulate at Stations B and C, suggesting it is consumed and processed rapidly by seafloor communities. These two stations have higher faunal abundance, species and functional diversity than Station A [START_REF] Włodarska-Kowalczuk | Do benthic meiofaunal and macrofaunal communities respond to seasonality in pelagial processes in an Arctic fjord (Kongsfjorden, Spitsbergen)?[END_REF]. Higher bioturbation rates at these stations than at Station A also suggest that benthic communities at these stations are more efficient at consuming material upon its arrival on the sediment surface. A similar finding was made in a study on the Beaufort shelf, where, despite strong seasonal signals in vertical flux and sediment community oxygen consumption, little change in sediment pigments was found [START_REF] Renaud | Seasonal variation in benthic community oxygen demand: A response to an ice algal bloom in the Beaufort Sea[END_REF].

Spatial and temporal differences in bioturbation activities

Bioturbation showed strong spatial variability in the fjord, with very low biodiffusion and non-local mixing at

Station A. This station has no deep burrowing polychaetes (e.g. maldanids) and is dominated by small surface-deposit feeders (cirratulid and cossurid polychaetes) throughout the year [START_REF] Włodarska-Kowalczuk | Do benthic meiofaunal and macrofaunal communities respond to seasonality in pelagial processes in an Arctic fjord (Kongsfjorden, Spitsbergen)?[END_REF]. Non-local mixing rates at Station A were similar to those for the deep stations (over 400 m) Barents Sea region dominated by small-sized organisms [START_REF] Oleszczuk | Benthic macrofaunal bioturbation activities from shelf to deep basin in spring to summer transition in the Arctic Ocean[END_REF]. The middle and outer stations showed similar rates of both biodiffusion and non-local mixing, and these rates were 2-4x those from previous studies in Arctic [START_REF] Oleszczuk | Benthic macrofaunal bioturbation activities from shelf to deep basin in spring to summer transition in the Arctic Ocean[END_REF]. Active burrowers and deepdwelling tubeworms were found at Stations B and C [START_REF] Włodarska-Kowalczuk | Do benthic meiofaunal and macrofaunal communities respond to seasonality in pelagial processes in an Arctic fjord (Kongsfjorden, Spitsbergen)?[END_REF], and organic content was 3-4 x higher at the middle and outer stations than at Station A (Figure 3).

There was little obvious seasonal change in non-local transport at any of the stations, and non-local transports are positively correlated to degraded sedimentary organic matter (phaeopigment biomass). This is consistent with the lack of accumulation of a pulse of phytopigments at the mid and outer stations (Figure 3), and the lower richness and abundance of burrowers at Station A [START_REF] Włodarska-Kowalczuk | Do benthic meiofaunal and macrofaunal communities respond to seasonality in pelagial processes in an Arctic fjord (Kongsfjorden, Spitsbergen)?[END_REF], particularly those most often involved in nonlocal mixing (oweniid and maldanid polychaetes). Biodiffusion was highest in May at Stations B and C and was a factor of >4 lower during the rest of the year. POC, chl a, biogenic silica, and fecal pellet fluxes, indicators of deposition of organic material, were considerably (2-15 x) higher in May than during other seasons at these stations [START_REF] Lalande | Spatial and temporal variability in export fluxes of biogenic matter in Kongsfjorden[END_REF], and likely led to enhanced biodiffusion activities, as observed in other studies [START_REF] Morata | Impact of early food input on the Arctic benthos activities during the polar night[END_REF][START_REF] Gerino | Comparison of Different Tracers and Methods Used to Quantify Bioturbation During a Spring Bloom: 234-Thorium, Luminophores and Chlorophylla[END_REF].

Diversity and size-structure of meio-and macrobenthic communities are similar through the year at each station [START_REF] Włodarska-Kowalczuk | Do benthic meiofaunal and macrofaunal communities respond to seasonality in pelagial processes in an Arctic fjord (Kongsfjorden, Spitsbergen)?[END_REF], probably due to sedimentary organic matter remaining available during a large part of the year. Thus, it is supposed here that communities at each station change their bioturbation behavior through the year depending on phytodetritus pulses and stock of degraded OM. Biodiffusion is dominant in May at the stations B&C but non-local (conveyer-like) mixing dominates from August to January. The quality of OM between May and August at the two stations may explain these changes, where sub-surface activities are dominant after rapid processing of the freshest phytodetritus.

Although we don't have bioturbation data in May and August at the Station A, bioturbation intensity there is lower than in stations B&C during the other seasons. This is caused by the impoverishment of benthic communities by conditions at the glacier front (hydrodynamics, erosion), although the sedimentary pigments are less degraded at this station from spring to fall. Stations B&C have more diverse benthic communities and higher functional-trait diversity and bioturbation. This can explain why the two modes of bioturbation are observed at these two stations.

Spatial and temporal differences in benthic fluxes

The remineralization of carbon and nutrients by Arctic seafloor communities has been shown to depend primarily on organic matter availability [START_REF] Gerino | Comparison of Different Tracers and Methods Used to Quantify Bioturbation During a Spring Bloom: 234-Thorium, Luminophores and Chlorophylla[END_REF][START_REF] Hulth | Arctic sediments (Svalbard): consumption and microdistribution of oxygen[END_REF][START_REF] Boetius | Benthic oxygen uptake, hydrolytic potentials and microbial biomass at the Arctic continental slope[END_REF][START_REF] Cathalot | Benthic Oxygen Uptake in the Arctic Ocean Margins -A Case Study at the Deep-Sea Observatory HAUSGARTEN (Fram Strait)[END_REF][START_REF] Kotwicki | Total benthic oxygen uptake in two Arctic fjords (Spitsbergen) with different hydrological regimes[END_REF]. At deep Arctic basin stations, depth is as important as pigment concentration [START_REF] Bourgeois | Glacier inputs influence organic matter composition and prokaryotic distribution in a high Arctic fjord (Kongsfjorden, Svalbard)[END_REF] but the depth range in this study was relatively narrow (80 -305 m). SOD measured in this study is similar to other measurements of SOD from Kongsfjorden [START_REF] Hulth | Arctic sediments (Svalbard): consumption and microdistribution of oxygen[END_REF][START_REF] Glud | Benthic mineralization and exchange in Arctic sediments (Svalbard, Norway)[END_REF], and generally higher than colder Svalbard fjords [START_REF] Morata | Impact of early food input on the Arctic benthos activities during the polar night[END_REF][START_REF] Kotwicki | Total benthic oxygen uptake in two Arctic fjords (Spitsbergen) with different hydrological regimes[END_REF][START_REF] Glud | Benthic mineralization and exchange in Arctic sediments (Svalbard, Norway)[END_REF] and deep-sea Arctic sediments [START_REF] Cathalot | Benthic Oxygen Uptake in the Arctic Ocean Margins -A Case Study at the Deep-Sea Observatory HAUSGARTEN (Fram Strait)[END_REF]. SOD, stable over the year at each station, was higher at Stations B&C where Phaeobm and TOCbm are highest, although chla was higher at Station A. The lack of significant seasonal variability in SOD at any of our stations is in direct contrast to findings in a number of empirical studies [START_REF] Bourgeois | Organic matter remineralization in marine sediments: A Pan-Arctic synthesis[END_REF][START_REF] Grant | Sediment properties and benthic-pelagic coupling in the North Water[END_REF][START_REF] Link | Spring-to-summer changes and regional variability of benthic processes in the western Canadian Arctic[END_REF][START_REF] Renaud | Seasonal variation in benthic community oxygen demand: A response to an ice algal bloom in the Beaufort Sea[END_REF] showing SOD was linked with seasonal cycles of pelagic production. Only in deep areas such as the central Arctic basin, where the seasonal pelagic signals is likely reduced due to great depths and generally lower primary production, was no seasonality in SOD identified [START_REF] Oleszczuk | Benthic macrofaunal bioturbation activities from shelf to deep basin in spring to summer transition in the Arctic Ocean[END_REF]. Response to pulsed food inputs can be realized in elevated SOD within days and persist for several weeks (e.g. [START_REF] Renaud | Seasonal variation in benthic community oxygen demand: A response to an ice algal bloom in the Beaufort Sea[END_REF]), and nutrient fluxes and bioturbation may respond at different time scales. Peak vertical flux of both POC and chl a in 2012 was in May [START_REF] Lalande | Spatial and temporal variability in export fluxes of biogenic matter in Kongsfjorden[END_REF], simultaneous with the sediment flux and bioturbation measurements, so we would have expected a peak in one or more of these parameters if there was a response to seasonal inputs. In the other studies cited, however, the timing of sampling relative to a food pulse may influence whether a response is observed.

Maintaining high SOD at stations throughout the year necessitates storage of organic material within sediments and/or significant presence of other labile carbon sources. The presence of a 'food bank' within the sediment that is available for use throughout the year was the explanation for little seasonality in SOD observed along the western Antarctic Peninsula [START_REF] Smith | A synthesis of bentho-pelagic coupling on the Antarctic shelf: Food banks, ecosystem inertia and global climate change[END_REF]. Alternately, more than 40% of carbon assimilation by soft-sediment benthos in another boreal, ice-free fjord in west Svalbard came from macroalgal detritus, even at depths up to 400 m [START_REF] Renaud | Macroalgal detritus and food-web subsidies along an Arctic fjord depth-gradient[END_REF], and an average of 60% of sediment organic carbon in Kongsfjorden comes from macroalgae [START_REF] Zaborska | Sedimentary organic matter sources, benthic consumption and burial in west Spitsbergen fjords -Signs of maturing of Arctic fjordic systems[END_REF]. We have no reason to exclude either of these possibilities and, indeed, both may contribute to the lack of seasonality in SOD.

Fauna associated with higher bioturbation rates at Stations B&C may also explain higher SOD [START_REF] Michaud | The functional group approach to bioturbation: The effects of biodiffusers and gallery-diffusers of the Macoma balthica community on sediment oxygen uptake[END_REF]. The correlation of SOD with non-local transport might result from intensification of microbial processes in subsurface sediments at Stations B&C caused by maldanid and spionid burrowing here [START_REF] Włodarska-Kowalczuk | Do benthic meiofaunal and macrofaunal communities respond to seasonality in pelagial processes in an Arctic fjord (Kongsfjorden, Spitsbergen)?[END_REF]. Change in bioturbation mode between May and August at Stations B&C is not perceptible in SOD. This may indicate either compensation in SOD between bioturbation functional groups and their associated microbial processes, or a dominance of maintenance respiration in fauna that overwhelms enhanced seasonal activities by diffusers or non-local mixers. Higher non-local transport in August likely stimulates the release of silicate to the overlying water and enhances sedimentary silicate dissolution [START_REF] Marinelli | Effects of polychaetes on silicate dynamics and fluxes in sediments: Importance of species, animal activity and polychaete effects on benthic diatoms[END_REF]. Silicate dissolution, usually most efficient on grazed OM [START_REF] Gallinari | Influence of seasonal phytodetritus deposition on biogenic silica dissolution in marine sediments-Potential effects on preservation[END_REF], is higher in stations with high Phaeobm and enriched in diatoms. Thus, sediment microbes can accelerate biogenic silica dissolution by colonizing and enzymatically degrading the organic coating of diatom frustules. . Nutrient fluxes (in the same range of values from the Svalbard area [START_REF] Glud | Benthic mineralization and exchange in Arctic sediments (Svalbard, Norway)[END_REF] and in the Canadian Arctic [START_REF] Link | Multivariate benthic ecosystem functioning in the Arctic – benthic fluxes explained by environmental parameters in the southeastern Beaufort Sea[END_REF]) indicate that fjord sediments are an important source of inorganic nutrients for driving primary production in the fjord. The seasonality of nutrient fluxes is further evidence of rapid processing of the sedimenting spring bloom/fecal pellet carbon. Higher NH4 + release at Station A might be the result of faster mineralization of the fresher sediment organic material, compared to at Stations B&C, where degraded organic matter slows microbial mineralization rates and perhaps leads to denitrification at the outer station.

Seasonality in a changing Arctic

Whereas strong seasonality of pelagic production and export of OM persists in a warmer, ice-free Kongsfjorden, the benthic system does not show a dramatic response. Such seasonality in Arctic benthic processes is most often observed in open shelf systems [START_REF] Bourgeois | Organic matter remineralization in marine sediments: A Pan-Arctic synthesis[END_REF]. In one of the very few seasonal studies of benthic processes performed in fjords [START_REF] Morata | Impact of early food input on the Arctic benthos activities during the polar night[END_REF] a strong response to experimental food addition was observed in a high-Arctic system with up to 8 months of ice cover per year. We argue that the results from Kongsfjorden may be a model for many areas on Arctic shelves undergoing loss of sea-ice and warming waters. Thus, it is important to explore potential mechanisms for this loss of strong seasonality in some processes, and possible consequences for Arctic benthic ecology.

There is considerable observational evidence that reductions in sea-ice and warming temperatures are strongly linked to increased macroalgal production due in large part to increased light availability [START_REF] Weslawski | Increase in biodiversity in the arctic rocky littoral, Sorkappland, Svalbard, after 20 years of climate warming[END_REF].

Macroalgae, particularly kelps, undergo seasonal growth and senescence cycles, generating considerable amounts of detritus [START_REF] Buchholz | Working on a baseline for the Kongsfjorden food web: production and properties of macroalgal particulate organic matter (POM)[END_REF]. Production of this detritus, however, is temporally distinct from pulses of pelagic phytodetritus as it arrives in autumn and winter due to natural senescence cycles and seasonal storms that detach living kelps from the sea floor. Increased light levels in a warming Arctic may also lead to enhanced growth of microphytobenthos, an as yet understudied source of organic matter to the coastal marine system [START_REF] Woelfel | Microphytobenthos of Arctic Kongsfjorden (Svalbard, Norway): biomass and potential primary production along the shore line[END_REF]. Additionally, inputs of terrestrial carbon via rivers, melting glaciers, and coastal erosion are also predicted to increase considerably as the Arctic and surrounding systems warm [START_REF] Parmentier | A synthesis of the arctic terrestrial and marine carbon cycles under pressure from a dwindling cryosphere[END_REF]. It is already clear that much of this carbon is labile and is processed rapidly when it reaches the marine system [START_REF] Harris | Do high Arctic coastal food webs rely on a terrestrial carbon subsidy?[END_REF], and is not restricted to coastal areas [START_REF] Magen | Origin and fate of particulate organic matter in the southern Beaufort Sea -Amundsen Gulf region, Canadian Arctic[END_REF]. Thus, elevated levels and processing of detrital material in warming, ice-free fjords relative to cold, seasonally ice-covered fjords [START_REF] Renaud | Macroalgal detritus and food-web subsidies along an Arctic fjord depth-gradient[END_REF][START_REF] Zaborska | Sedimentary organic matter sources, benthic consumption and burial in west Spitsbergen fjords -Signs of maturing of Arctic fjordic systems[END_REF] suggest sediment communities in the future Arctic may function differently than at present. How, then, will increased detritus content affect system functioning, aside from reduced seasonality? Detritus has been suggested to dampen seasonal fluctuations in carbon supply, leading to more stable food-chains and higher resilience to interannual variability in pelagic primary production [START_REF] Norkko | Trophic Structure of Coastal Antarctic Food Webs Associated with Changes in Sea Ice and Food Supply[END_REF]. Deposit-feeding taxa may be favored over suspension-feeders in many of these systems with potential implications for bioturbation modes and intensity, and at a longer time scales, decreasing functional traits diversity within benthic communities.

Monitoring programs could target these questions in detailed comparative studies. Such food-web shifts have not been well studied but could have strong consequences for sustenance of top predators, including subsistence human populations. Finally, fjords have been identified as sites of disproportionately high carbon burial [START_REF] Smith | High rates of organic carbon burial in fjord sediments globally[END_REF]. It is unclear whether increased detrital carbon and its impacts on seafloor processing will enhance or reduce this role. It is possible, however, that greater inputs of labile macroalgal detritus will enhance remineralization of more refractory sedimentary carbon that would otherwise be buried [START_REF] Aller | The Critical Role of Bioturbation for Particle Dynamics, Priming Potential, and Organic C Remineralization in Marine Sediments: Local and Basin Scales[END_REF]. This 'organic priming' can be promoted by bioturbation, enabling fresher material and oxidants to reach buried carbon, and such processes demand both observational and experimental attention.

Responses to pulsed pelagic inputs will continue to be strong and pelagic-benthic coupling can still be quite tight, but the addition of detrital carbon from macroalgae, benthic microalgae, and terrestrial sources can make it harder to track seasonality in benthic activity. Benthic processes may remain quite seasonal on oligotrophic shelves and ice covered coastal regions, but increases in organic matter inputs from terrestrial and coastal systems may change this over time. The interaction of processes, including changes in relative inputs of different carbon sources, declining seasonality in benthic activity, and potential changes in bioturbation functional traits and food-web structure (i.e., decoupling of separate energy channels by Tables Table 1:

  Differences in the bulk sediment variables, benthic fluxes and bioturbation coefficients at the three stations of Svalbard (Inner (A), Middle (B), Outer (C)) between 2012 (May, August, October), 2014 (August) and 2015 (January), after two-way ANOVAs (A; F and p values) or Sheirer-Ray-Hare (SRH; H and p values) tests. Significant differences (p<0.05) are indicated by asterisk (*). Last column indicates the pair wise comparisons between the three stations.

Figures captionsFigure 1 :

 1 Figures captions

Figure 2 :

 2 Figure 2: Mean biomass (mg m -2 ) of total organic carbon (TOC) (a), Chla (b), Phaeopigments (c) and mean

Figure 3 :

 3 Figure 3 : Mean biodiffusion (Db in cm² y -1 ) and non-local (r in y -1 ) transports measured at the three stations in

Figure 4 :

 4 Figure 4 : Mean oxygen (a) and nutrient net fluxes (b-e) (mmol m -² d -1 ) at the sediment-water interfaces at the

Figure 5 :

 5 Figure 5: Principal component analysis based on the sediment variables (C:N, Chla:phaeo and C-Chla:TOC

Figure 1 :

 1 Figure 1: Locations of the three stations at Inner (station A), Middle (station B), Outer (station C) in

Figure 2 :Figure 3 :Figure 4 :Figure 5 :

 2345 Figure 2: Mean biomass (mg m -2 ) of total organic carbon (TOC) (a), Chla (b), Phaeopigments (c) and mean

Table 2 :

 2 Spearman's rank correlation analyses between biogeochemical fluxes (O2, NO3 -+NO2 -, PO4 3-, NH4 + ), sediment biomarkers (C:N, C-Chla:TOC, Chla:Phaeo ratios, and biomass of TOC, chla and phaeopigments), and bioturbation variables (Db, r). Significant values are marked in bold (p < 0.05).

		Db	r	O 2 NO 3 -+NO 2 -Si(OH) 4 NH 4 +	PO 4 3-	C:N chla:phaeo C-Chla:TOC	TOC bm	chla bm	Phaeo bm
	Db	1.00	-0.20 -0.12	-0.27	-0.08 -0.43 -0.29 -0.18	-0.04	-0.16	0.34	-0.07	0.19
	r	-0.20	1.00 -0.86	0.49	0.94 -0.42 0.80 0.06	-0.72	-0.69	0.77	-0.30	0.76
	O2	-0.12	-0.86 1.00	-0.38	-0.94 0.59 -0.65 0.00	0.71	0.72	-0.92	0.24	-0.91
	NO 3 -+NO 2 -	-0.27	0.49 -0.38	1.00	0.45	0.08 0.15 -0.53	0.08	0.08	0.17	0.36	0.41
	Si(OH) 4	-0.08	0.94 -0.94	0.45	1.00 -0.47 0.80 0.01	-0.72	-0.71	0.83	-0.21	0.87
	NH 4 +	-0.43	-0.42 0.59	0.08	-0.47 1.00 -0.10 -0.37	0.82	0.86	-0.73	0.79	-0.36
	PO 4 3-	-0.29	0.80 -0.65	0.15	0.80 -0.10 1.00 0.18	-0.59	-0.51	0.59	-0.16	0.66
	C:N	-0.18	0.06 0.00	-0.53	0.01 -0.37 0.18 1.00	-0.48	-0.44	0.12	-0.71	-0.26
	chla:phaeo	-0.04	-0.72 0.71	0.08	-0.72 0.82 -0.59 -0.48	1.00	0.98	-0.79	0.81	-0.50
	C-Chla:TOC	-0.16	-0.69 0.72	0.08	-0.71 0.86 -0.51 -0.44	0.98	1.00	-0.82	0.80	-0.53
	TOC bm	0.34	0.77 -0.92	0.17	0.83 -0.73 0.59 0.12	-0.79	-0.82	1.00	-0.43	0.86
	chla bm	-0.07	-0.30 0.24	0.36	-0.21 0.79 -0.16 -0.71	0.81	0.80	-0.43	1.00	0.04
	Phaeo bm	0.19	0.76 -0.91	0.41	0.87 -0.36 0.66 -0.26	-0.50	-0.53	0.86	0.04	1.00

Phil. Trans. R. Soc. A.enhancing detrital food web[START_REF] Mcmeans | Food web structure of a coastal Arctic marine ecosystem and implications for stability[END_REF]), will likely result in ecosystem instability and in alteration of carbon cycling pathways. The potential consequences of fundamental changes in how organic matter is processed by Arctic benthos imply a need for development of biomarkers and experimental approaches to tease apart these interactions.

ACKNOWLEDGEMENTS

This study is a contribution to the projects ARCEx (NRC 228107), Marine Night (NRC 226417), WINBA (Arctic Field Grant), ESCOFAR (CNRS-EC2CO-DRIL&BIOHEFECT), IPEV (project #1132) and ECOTAB (ANR-11-PDOC-0018). We thank the crew of the MS Teisten, R/V Helmer Hanssen and the AWIPEV personnel in Ny-Ålesund for dedicated, professional assistance. We thank E. Amice, A. Aubert, J. Berge, S. Bourgeois, M.

Calleja, E. Courtecuisse, G. Duong, C. Gueguen, P. Kerhervé, F. Narcy, J. Richard, V. Rissone and J. Søreide for their help with field sampling. The authors thank the two anonymous referees for the reviewing process.

Data Accessibility

The datasets supporting this article have been uploaded as part of the Supplementary Material.

Competing Interests

We have no competing interests.

Authors' Contributions

Substantial contributions to conception and design (NM, EM, PR), acquisition of data (NM, RC, PR), analysis and interpretation of data (NM, EM, MAP, JD, MLG, RC, PR); 2) drafting the article or revising it critically for important intellectual content (NM, EM, PR); and 3) final approval of the version to be published (NM, EM, MAP, JD, MLG, RC, PR).