Introduction

The Northern Svalbard Continental Margin represents a transitional zone in the high Arctic, where the northward-flowing Atlantic Water (salinity ≥ 34.9 PSU, temperature > 0 °C), transported by the West Spitsbergen Current, subducts beneath the fresher Polar Water layer (salinity ∼31–34 PSU) and surrounding Arctic water masses1, 2, 3. Due to rising heat advection of Atlantic Water, the inflow regions (eastern Barents Sea and north of Svalbard) experience earlier and more extensive sea-ice retreat, which in turn leads to increased primary production in the area4. Over the past decades, the progressively earlier retreat of sea ice north of Svalbard has led to a prolongation of the phytoplankton growing season, an expansion of under-ice blooms, and Phaeocystis-dominated blooms5, 6. As a consequence, the major spring phytoplankton bloom tends to start earlier and last longer, impacting the food web structure in the area5. Phytoplankton blooms serve as a source of phytodetritus that develops in the photic zone, sinks throughout the water column, undergoes recycling along the way, and is eventually exported to the seafloor7, 8. The exported material is mainly composed of organic (decaying phytoplankton and other organic remains such as faecal pellets) and inorganic (terrigenous and cryogenic particles) components7, 8, 9. In the Arctic, the main ballasting particles that facilitate carbon export to depth are cryogenic gypsum crystals, which are formed in sea ice and preferentially released in the marginal ice zone9, 10. This carbon transfer from the surface ocean to the deep ocean, termed “the biological carbon pump”, is an important contributor to CO2 storage in the deep sea. However, the future of the Arctic biological carbon pump remains under debate. Recent studies suggest that its efficiency may decline and slow down11, 12, whilst other authors highlight considerable uncertainty9. Upon reaching the seafloor, phytodetritus takes on variable appearances, ranging from flocculent or phytodetritus aggregates to gelatinous or mucilaginous textures, and can appear green, brown, or grey8. The phytodetritus reaching the seafloor, provides food and habitat for benthic organisms8. Numerous studies showed that fauna can be rapid consumers of fresh phytodetritus, such as bacteria13, and benthic foraminifera14, 15, particularly in the northern latitudes, following the deposition of slightly altered phytoplankton remains11, 16. Transient phytodetrital aggregates can function as temporary microhabitats for foraminiferal communities17, primarily investigated in the North Atlantic18, and Weddell Sea19. However, similar observations remain missing in the Arctic Ocean, particularly in springtime, due to logistical challenges associated with accessing these remote environments. In the present study, we report the first investigations on living (Rose Bengal-stained) benthic foraminifera within phytodetritus deposits, including surface sediments collected during a late spring phytoplankton bloom event in the Arctic Ocean. This study aims to compare foraminiferal fauna in the accumulated phytodetrital layer, or phytodetritus, and underlying associated surface sediment from three sites: the Svalbard Shelf, Yermak Plateau, and Sophia Basin; to calculate the faunal density and relative abundances; and to identify potential microhabitat preferences of benthic foraminifera. This research will contribute to our understanding of the impact of labile organic matter fluxes on Arctic benthic communities and the broader implications for Arctic marine ecosystems.

Results

The foraminiferal density was variable across the accumulated phytodetrital layer and underlying associated surface sediment samples. The density in the phytodetrital layer was on average 18.5 times higher compared to sediment. It is worth mentioning that samples were collected in markedly different volumes. Faunal densities and relative abundances of dominant species in the phytodetrital layer and surface sediment samples are shown in Fig. 1. At the station PS92/32, Alabaminella weddellensis was the most abundant species in the phytodetritus (17.8%). It was accompanied by other prevalent species such as Adercotryma glomeratum (17.6%) and Cassidulina neoteretis (11%). In contrast, Melonis zaandami (22%) was found predominantly in the underlying sediment. At the site PS92/46, Cassidulina reniforme and C. neoteretis were significant in both phytodetritus (13.1% and 10.4%, respectively) and sediment (16.9% and 16.2%, in accordance). Lagenammina arenulata was another dominant taxon in the phytodetrital layer (10.4%). At the site PS92/47, the phytodetritus yielded the dominant species Epistominella arctica (30.8%) and Quinqueloculina akneriana (14.3%). On the contrary, the underlying substrate contained Ioanella tumidula (13.1%) and Hormosinelloides guttifer (29.2%). A summary of ecology of dominant foraminiferal species based on the references presented in Table 1. Raw and extrapolated counts, densities, and relative abundances of the foraminiferal species across stations and substrates are presented in Supplementary Tables S1–S5. Plates of foraminiferal species exhibiting well-developed greenish cytoplasm and living (Rose Bengal-stained) species that colonised the phytodetrital layer are shown in Supplementary Figs. S1 and S2, respectively. Non-metric multidimensional scaling (NMDS) based on the Morisita similarity index was used to visualise differences between foraminiferal communities in phytodetritus and those in sediment, in a two-dimensional ordination plot (Stress = 0.09) (Supplementary Fig. S3).

Fig. 1
Fig. 1
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Cumulative faunal density and relative abundances of dominant species (> 10%) in the accumulated phytodetrital layer and underlying associated surface sediment. Category “Others” includes species whose relative abundance is less than 10% at the corresponding station.

Table 1 Summary of the ecology of dominant foraminiferal species based on the references.
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Discussion

In spring, the Barents Sea slope, where the PS92/32 site is located, is influenced by the inflow of Atlantic Water and receives high fluxes of fresh organic matter to the seafloor20. The site was classified as a bloom site, with increased diatom-associated chlorophyll a, abundant under-ice fauna, and signs of active grazing by sea-ice and under-ice fauna6,21,22, suggesting recent phytodetritus deposition. Despite heavy ice cover reaching 94% during sampling (ice and snow thickness measured at 1.4 m), the conditions were productive, likely due to the presence of leads in the ice and proximity to open water, which triggered enhanced light penetration through the water column6,23. Under warm (2.1 °C) and saline (35 PSU) bottom water conditions, Alabaminella weddellensis, Adercotryma glomeratum, and Cassidulina neoteretis flourished in the densely populated and freshly deposited phytodetritus, whereas the surface sediment below was predominantly colonised by Melonis zaandami. Alabaminella weddellensis is a calcareous species known as one of the phytodetritus group members. The group is typically associated with seasonal primary production pulses24, extended sea ice retreats, and regions with no permanent sea ice25, 26, 27,28. Also, foraminifera associated with the phytodetritus (such as A. weddellensis) have a high dispersion potential29. Our findings are consistent with earlier evidence suggesting that A. weddellensis is an opportunistic phytodetritus-dwelling species, which is often found alongside another calcareous phytodetritus inhabitant Epistominella exigua18,24, 30, 33. Despite the specialist nature of E. exigua, it was found in low abundance across all samples (raw and extrapolated counts, densities, and relative abundances of E. exigua is presented in Supplementary Table S5). According to a previous study of Neogene samples34, A. weddellensis may be more prevalent than E. exigua in specific types of phytodetritus, such as dense diatom mats, implying the phytodetritus composition at the station may favour A. weddellensis. Therefore, the abundance of these opportunistic species may fluctuate depending on the phytodetritus type35. The agglutinated species A. glomeratum was present across both layers at all stations, showing its preferences to the high productive station. Adercotryma glomeratum is an opportunistic, detritivore infaunal species that exhibits epifaunal motile behaviour in response to episodic phytodetritus deposition36. Also, it was noted that the species tends to be associated with both phytodetritus and underlying sediment18 supporting our data. The calcareous Arctic and subarctic dwelling species C. neoteretis was one of the main contributors at the PS92/32 and PS92/46. However, it was absent at the deepest station, PS92/47, likely due to its preference for water depths between 200 and 1400 m26. The infaunal C. neoteretis is an opportunistic species previously reported as a phytodetritus indicator during an interglacial period in the fossil record37. It is well adapted to strong seasonal fluctuations in food supply28,32,38,39, and reproduction pulses are frequently associated with spikes in marine productivity40. The species benefits from the nutrient-rich conditions provided by phytoplankton blooms41,38,39, and is likely to feed on degraded organic matter and phytodetritus-associated bacteria28,32. Interestingly, it was stated that the species does not typically invade the phytodetritus32. However, our findings contradict this, as we observed the presence of C. neoteretis actively ingesting phytodetritus and inhabiting it (Supplementary Fig. S1). Therefore, our results may reflect its adaptive ecological flexibility that was not acknowledged in the past. Additionally, it was recognised as an indicator of modified Atlantic Water42. Nonetheless, some studies described that the exact nature of the relationship between C. neoteretis and Atlantic Water remains uncertain26. The sediment conditions appeared highly favourable for Arctic infaunal calcareous species M. zaandami. In accordance with the present results, earlier investigations demonstrated that the species tends to be associated with high fluxes of slightly altered organic matter and linked to increased phytodetritus accumulations26,27.

Station PS92/46, located on the eastern Yermak Plateau, was characterised as a pre-bloom station with dense sea-ice cover reaching 99% (ice and snow thickness measured at 1.2 m), and a low chlorophyll a standing stock6. Furthermore, low abundances of under-ice and sea-ice fauna, lack of grazing, and an estimated carbon demand nearly twice phytoplankton production indicated an insufficient carbon supply for local under-ice communities21,22. This evidence may support the hypothesis that the phytodetritus was likely either degraded and originated from earlier blooms rather than recent ones, or it represented the first material settling during the pre-bloom phase. This aligns with total organic carbon (TOC) results from the same cruise, showing lower TOC in Yermak Plateau sediments, likely due to prolonged sea ice cover and reduced fresh organic matter input compared to the Barents Sea slope20. Cassidulina reniforme and C. neoteretis occurred abundantly in both layers, although Lagenammina arenulata favoured the phytodetritus. These species thrived under cold (− 0.3 °C) and saline (34.9 PSU) bottom water conditions. The Arctic infaunal calcareous C. reniforme is typically associated with cool, saline waters43,44, which confirms our examinations. A positive correlation between living C. reniforme abundance and both organic carbon content and phytoplankton density was reported in the earlier study45. In contrast, its abundance demonstrated resilience to pre-bloom, food-limited condition in our samples. Another dominant taxon of the Cassidulina genus is C. neoteretis, an indicator of high productivity. Its microhabitat preferences are discussed above. Its presence at this site may indicate its environmental adaptability to varying food availability and temperature conditions. Another species that achieved maximum abundance in the phytodetrital layer was agglutinated L. arenulata. The ecology of this species is not well understood. In general, Lagenammina genus is an infaunal, detritivorous taxon that prefers cold-temperate environments46. It was highlighted as a dominant component of the benthic community at the Suiko Seamount, a subarctic site characterised by stable and higher fluxes of organic matter from July to December47. Moreover, L. arenulata was identified as one of the main components of the assemblages in Baffin Bay and Nares Strait, where it appeared at stations marked by cold temperatures and corrosive conditions48. Finally, it was noted that members of Lagenammina genus are not directly associated with phytodetritus17.

The station PS92/47 in the Sophia Basin was notable for its classification as a bloom station6. The station demonstrated heavy ice cover reaching 100% (ice and snow thickness measured at 1.4 m), moderate abundances of sea ice and under-ice fauna, and particularly high abundances of grazers21. During the PS92 cruise, the export of Phaeocystis to the seafloor was significantly enhanced through the ballasting of Phaeocystis aggregates with gypsum minerals released from melting sea ice at the site10,49. A video recording of the MUC deployment and aggregate accumulation on the seafloor indicated a rapid downward flux of gypsum-ballasted Phaeocystis during sampling10. However, some studies reported that Phaeocystis phytodetritus is found less frequently in the deep sea compared to diatoms, likely due to recycling and grazing in the water column7,8. Supporting this, cruise observations6 recorded that faecal pellets from krill and copepods contributed a substantial fraction to vertical carbon export in certain areas, especially where blooms of Phaeocystis dominated. Therefore, we can suggest that the phytodetritus was freshly delivered and partly originated from faecal pellets. Epistominella arctica and Quinqueloculina akneriana thrived in the phytodetritus, whilst Hormosinelloides guttifer and Ioanella tumidula extensively inhabited the sediment. These species flourished under the cold (− 0.8 °C), saline (34.9 PSU) conditions as well as at the previous station PS92/46. The Arctic-dwelling calcareous species E. arctica exhibits an opportunistic life strategy, reproducing during periods of high seasonal productivity in oligotrophic environments and becoming less abundant during extremely low food availability28. The accumulated phytodetritus yielded juveniles of E. arctica, indicating active reproduction and favourable conditions for its lifecycle. Our results are consistent with previous observations, which show that the distribution of E. arctica in the Arctic is linked to phytodetritus and, as a result, it tends to release large numbers of offspring in the Sophia Basin28. Our results also support findings from Weddell Sea samples, which showed that small phytodetritus balls were abundantly populated by E. arctica19. The site may be characterised by minimal to absent current activity, as indicated by the abundant occurrence of E. arctica. This species possesses minute lightweight tests that can be readily transported within the accumulated labile carbon on the seabed28. However, the study lacks the necessary data on bottom currents to quantitatively evaluate this parameter. An abyssal Arctic species38,50 that appeared in the phytodetritus was porcelaneous Q. akneriana. The ecology of this species remains insufficiently studied. The genus Quinqueloculina is generally classified as an epifaunal, herbivorous taxon46. Records from the abyssal stations of the Porcupine Abyssal Plain, NE Atlantic, showed that Q. sp. responded to flux events by migrating to the upper sediment layers and the sediment-water interface, where they grew and reproduced before returning to a dormant state in deeper layers as phytodetrital food becomes depleted51,52. Another genus representative, Q. seminula, was observed with its protoplasm filled with pennate diatoms and dinoflagellates following a sedimentation event under the East Greenland Current53,54. In the feeding experiments, Q. seminula and Q. sp. demonstrated similar behaviour by collecting detrital plugs around their apertures and ingesting food, with their youngest chambers containing coccoid algae, diatoms, and stercomata53,54. These findings highlight the adaptability of Quinqueloculina representatives, potentially including Q. akneriana, to fluctuating food availability. The agglutinated species H. guttifer is described as a surface sediment-dwelling taxon that responds to the input of labile organic matter55. It was reported as a characteristic species on the Yermak Plateau56. This species may be associated with higher Corg fluxes than A. glomeratum28. In our samples, H. guttifer was accompanied by the epifaunal calcareous deep-water species I. tumidula, whose distribution is primarily influenced by water depth, biological competition, and food availability38. Additionally, our examinations showed that living I. tumidula individuals tended to exhibit an epibenthic lifestyle, attaching to hard substrates and occasionally forming agglutinated cysts, which reflects its immobile behaviour and dependence on the substrate.

In conclusion, this study represents the first documented association of benthic foraminiferal species inhabiting the accumulated phytodetrital layers and underlying associated surface sediments within the marginal sea ice zone off northern Svalbard continental margin. This study highlights their ecological versatility during spring bloom. The origin of phytodetritus in the Arctic is shaped by various environmental processes in surface waters and the water column, including proximity to open waters, the activity of under-ice and sea-ice fauna, grazing pressure, ice cover intensity, and overall surface water conditions. These factors influence the composition of phytodetritus and, consequently, the faunal composition of benthic foraminifera, which is primarily driven by food availability, along with secondary factors such as water depth, salinity, and temperature in both the phytodetritus and surface sediment layers. Furthermore, some infaunal foraminiferal species, such as Adercotryma glomeratum, Cassidulina neoteretis, C. reniforme, potentially Lagenammina arenulata have been observed to inhabit phytodetritus deposits, highlighting their migratory abilities. This high-resolution study complements both seasonal/annual observations and time-averaged sedimentary archives, which document broader historical and contemporary ecological shifts.

Methods

Study area

From May 19 to June 28, 2015, the German icebreaker R/V Polarstern embarked on expedition PS92 (ARK-XXIX/1), known as “TRANSSIZ” (Transitions in the Arctic Seasonal Sea Ice Zone). This six-week mission aimed to investigate ecological and biogeochemical processes during early spring across the European Arctic margins and the Yermak Plateau. The study focused on three distinct sites in the Arctic Ocean: the Barents Sea slope, the Yermak Plateau, and the Sophia Basin (Fig. 2), all located north of Svalbard. Positioned above 81°N latitude, these regions were heavily covered by ice and snow during sampling, with sea ice coverage ranging from 94% to 100%6. Bottom water temperature and salinity varied from − 0.8 to 2.1 °C and from 34.9 to 35 PSU57. The ice and snow thickness varied from 1.2 to 1.4 m across the study area21. The potential environmental characteristics are listed in Table 2.

Fig. 2
Fig. 2
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Map of the study area in the north of Svalbard (a, b), sampled during the Polarstern expedition PS92. Vertical carbon export6, sea ice cover data6, and bottom water measurements57 were extracted from the cruise studies and datasets. The sea ice extent on 15.06.2015 (white line) was based on EUMETSAT’s Global Sea Ice Concentration Reprocessing dataset62. Red arrows indicate the branches of the Atlantic Water current (WSC: West Spitsbergen Current; Sb: Svalbard branch; Yb: Yermak branch; YPb: Yermak Pass branch; rb: recirculating branch), modified after the reference63.

Table 2 List of the potential environmental characteristics.
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Sample collection and processing

During the 2015 TRANSSIZ PS92 (ARK-XXIX/1) cruise aboard the R/V Polarstern, undisturbed seafloor sediments were retrieved from depths of 218.8 to 2174.7 m using a video-equipped multicorer (TV MUC) and a box corer (BC) (Table 3). The inner diameter of the MUC tubes was 10 cm. The MUC frame was equipped with a live broadcasting video system that transfers pictures to the ship via glass fibre cable. A Sanyo HD400P camera captured images of under-ice fauna, marine snow in the water column, and phytodetritus patches on the seafloor (Fig. 3). The BC was deployed to acquire sediment samples from a large area, typically 50 × 50 cm. On the surface of MUC tubes and BC, marine snow could be observed either as recently deposited ball-like green aggregates ballasted by cryogenic gypsum at the site PS92/4710 or as more featureless “green soup” at the site PS92/32. Immediately after retrieval, three specific-volume samples of phytodetritus were extracted from the sediment surfaces of both the MUC and BC using a one-way pipette. Sediments were sampled from 0 to 15 cm in 1 cm steps, but only surface sediments (0–1 cm) are considered in the current study. Following retrieval of sediment cores from three MUC tubes, samples corresponding to the same depth interval from each tube were combined into a single Kautex bottle and homogenised. The phytodetritus and underlying associated surface sediment samples were preserved in Rose Bengal-ethanol mixture (2 g L⁻¹), washed through a 63 μm mesh, and dried. Each fraction was then split into subsamples using a microsplitter.

Table 3 Sampling stations for the accumulated phytodetrital layer and the underlying surface sediments.
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Fig. 3
Fig. 3
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Organic material export to the seafloor. Large aggregates or accumulations of aggregates are indicated by dotted green circles (image was taken and provided by Jutta Erika Wollenburg).

Taxonomical identification

Benthic foraminifera from fraction > 63 μm were isolated from both matrixes and were identified based on external morphological features. We aimed to collect a minimum of 300 Rose Bengal-stained individuals from whole sample splits of each sample, whenever possible. Picked individuals were mounted on micropalaeontology slides. Identification was performed using a Nikon SMZ-18 stereo microscope and using available literature. Nomenclature followed the World Register of Marine Species58, with taxon names validated by protist taxonomy experts within the team.

Statistical analysis and data visualisation

The foraminiferal counts from the split samples were calculated by multiplying the picked total number of individuals of each taxon by the splitting factor. Subsequently, foraminiferal counts from the phytodetritus and underlying associated surface sediment samples were standardised to individuals per cm3 (ind./cm3) to compare the foraminiferal absolute abundances between samples. Dominant species were defined as those comprising more than 10% of the assemblage. Those species, occurring at proportions below 10%, were included in quantitative analyses but are not discussed in the present study. The figures were plotted in RStudio version 2024.12.1 + 563. The RStudio package ggplot2 3.5.159 was used. The maps were produced in Ocean Data View software version 5.7.160. The photo and illustration were prepared with Inkscape 1.2.2. Non-metric multidimensional scaling (NMDS) based on the Morisita similarity index was performed and plotted using PAST software61.