The Arctic is one of the regions that is changing most rapidly due to climate factors, feedback mechanisms and changes in energy transport towards the poles (Richter-Menge et al., 2017; Previdi et al., 2021). This results in 3.8 times faster warming in the Arctic than the global average (Rantanen et al., 2022), with the strongest temperature rise detected during the winter months (Wang et al., 2017; Maturilli et al., 2019). Generally, organisms populating the Arctic must have the ability to survive extreme abiotic conditions due to the strong seasonality (Zacher et al., 2009). For instance, Arctic kelps have to endure extreme photoperiodic conditions (Gattuso et al., 2020). In winter, they are exposed to very low temperatures and months-long complete darkness (Polar Night). Due to climate change, however, strong fluctuations in sea surface temperature (SST) have occurred in recent decades. For example, in Kongsfjorden, Svalbard, winter SST minima of −1.8°C were measured, while the maximum SST reached ~5°C (Huang et al., 2021; see Supplementary Material ; Diehl et al., 2024).

Kelp forests are among the largest biogenic structures of marine benthic habitats and are highly productive ecosystems with structural complexity and phyletic diversity (Steneck et al., 2002; Wernberg et al., 2019). By definition, they are formed by brown algae of the order Laminariales, which dominate shallow rocky shores of temperate and Arctic regions. As sedentary organisms, kelps are particularly affected by changes in their environment and rising temperatures result in shifts in distribution and abundance of many species (Smale et al., 2019). On the one hand, new suitable and ice-free habitats are expected to increasingly appear in the future (Krause-Jensen et al., 2020; Castro de la Guardia et al., 2023). Changes in kelp abundance have already been observed in High Arctic regions (Bartsch et al., 2016; Düsedau et al., 2024). On the other hand, elevated temperatures generally stimulate the metabolic activity of organisms (Pörtner et al., 2005), and may therefore have a negative impact on the dark survival of kelps (Gordillo et al., 2022). Yet, the mechanisms of winter survival are still poorly understood and only a few studies have investigated acclimation of kelps to the Polar Night (Scheschonk et al., 2019; Gordillo et al., 2022; Summers et al., 2023; Diehl et al., 2024).

Kelps have evolved various mechanisms to acclimatize to abiotic variations in the environment (Hurd et al., 2014). Due to the seasonal photoperiods in the Arctic, growth and reproduction of most kelps species is limited to a short time in spring and summer, while in winter they undergo a “starvation mode” due to the lack of light for photosynthesis (Wiencke et al., 2009; Gordillo et al., 2022).

The vitality of kelps can be determined via fluorescence-based measurements of the maximum quantum yield of photosystem II (F_v/F_m), a common parameter for assessing the health and stress level of photosynthetic organisms, including macroalgae (Dring et al., 1996; Dring, 2006). As they are part of the cellular machinery for photosynthesis, pigment contents in some seaweeds decrease during Polar Night, when the metabolism of the organisms slows down to survive this period of total darkness (Wiencke et al., 2009). Moreover, the de-epoxidation state of the xanthophyll cycle pigments (DPS), an intracellular stress response, is affected by light and low temperatures (Fernández-Marín et al., 2011; Li et al., 2020; Monteiro et al., 2021). The carbohydrates mannitol and laminarin play a crucial role in surviving the Polar Night. Mannitol is the primary photosynthesis product and an important short-term storage carbohydrate in brown algae (Yamaguchi et al., 1966). In summer, when photosynthesis rates are high, mannitol is converted into the polysaccharide laminarin, the long-term storage carbohydrate (Johnston et al., 1977). In periods of darkness, laminarin can be reconverted into mannitol to maintain important metabolic functions (Yamaguchi et al., 1966; Johnston et al., 1977; Küppers and Kremer, 1978). We hypothesize that winter warming could accelerate the use of carbon reserves and increase the decomposition of the biomass. Monitoring dry weight and the total carbon content alongside quantifying mannitol and laminarin provides information on the consumption of carbon-containing metabolites as well as the storage carbohydrates.

Laminaria digitata (Hudson) J.V. Lamouroux is a broadly distributed cold–temperate to Arctic North Atlantic kelp growing on hard substrates in the sublittoral zone. In the East Atlantic, it is present from Southern Brittany to Spitsbergen (Lüning, 1990), where it survives up to four months of Polar Night. The species is described to survive and grow at temperatures as low as 0°C, with a temperature optimum at 10°C (Bolton and Lüning, 1982; tom Dieck (Bartsch), 1992). Recent studies showed a distinct decrease in digitate kelps (including L. digitata) in Arctic fjords (Düsedau et al., 2024), potentially in response to changes in the underwater light climate as a consequence of increased meltwater run-off (Schlegel et al., 2024). Liesner et al. (2020) showed that lower temperatures (5 vs. 15°C) led to a higher phenotypic plasticity, as well as higher growth rates of juvenile sporophytes, highlighting the importance of cold seasons for the survival of L. digitata and potential threats of climate change. Exposing L. digitata gametophytes to low temperatures (5 vs. 15°C) also facilitated a positive growth response from subsequent juvenile sporophytes at sub-optimal low (0°C) and warm (20°C) conditions (Gauci et al., 2022).

The aim of this study was to determine the resistance of L. digitata sporophytes to simulated temperature increases during the Polar Night in the High Arctic. Therefore, we kept discs from L. digitata sporophytes at temperatures of 0°C and 5°C in total darkness for three months. Various physiological and biochemical variables were monitored during the experiment. We hypothesized that higher temperatures during Polar Night would lead to an increased metabolism and therefore a reduced survival capacity of L. digitata.

This study determined the impact of Arctic winter warming on Laminaria digitata sporophytes in a simulation of High Arctic Polar Nights. Over a period of three months in darkness, physiological variables and underlying biochemical metabolites were monitored in samples maintained at 0°C and 5°C. The two temperature treatments represented the mean and the maximum winter temperatures that have already been measured in the High Arctic, for example in Kongsfjorden, Svalbard (Huang et al., 2021; see Supplementary Material ; Diehl et al., 2024). From our results ( Figure 5 ), it can be deduced that L. digitata sporophytes from Arctic regions are well adapted to prolonged darkness regardless of temperature and do not reach the end of Polar Night with a considerable lack of storage reserves and pigments.

Relative changes in vitality indicated that L. digitata performed better at 0°C compared to 5°C. Yet, a certain chamber effect in combination with the temperature treatments cannot be ruled out as the samples were maintained in two different climate chambers. Relative F_v/F_m values increased for samples at 0°C and decreased for samples at 5°C from week 8 onwards. However, absolute F_v/F_m values were never below 0.6, so all samples could be considered vital for the duration of the experiment (Dring et al., 1996). Laminariales have been observed to maintain a good vitality after long periods of darkness before (Scheschonk et al., 2019; Gordillo et al., 2022; Summers et al., 2023; Diehl et al., 2024).

The degradation of metabolites during prolonged darkness was reflected in a continuous loss in DW over time, as has also been observed for other kelps (Gordillo et al., 2022). However, contrary to previous data on Saccharina latissima and Alaria esculenta, weight loss in L. digitata did not increase at enhanced temperatures (3°C vs. 8°C; Gordillo et al., 2022). By visually observing the discs and monitoring disc area every two weeks, we were able to exclude any impact of decomposition on the DW ( Supplementary Table S1 ; Supplementary Figure S2 ).

During polar winter kelps rely on accumulated energy stores, and must therefore be particularly energy efficient (Wiencke et al., 2009). In times of prolonged darkness, kelp derive mannitol from stocks of laminarin that they replenished during summer (Johnston et al., 1977; Küppers and Kremer, 1978). Accordingly, mannitol can be considered the main metabolite for respiration during the Polar Night. It must be taken into account that the storage carbohydrate content varies between the meristem and the distal part of the sporophyte (Scheschonk et al., 2019). By conducting the experiment with subsamples taken from the central part of the phylloid, we aimed to eliminate any impact of these variations. Mannitol content of L. digitata decreased by 37% (0°C) and 65% (5°C) over the three-month experiment, while laminarin decreased by 40% and 90% respectively. When comparing energy stocks in the cold–temperate kelp S. latissima from Kongsfjorden (Svalbard), Scheschonk et al. (2019) measured comparably high declines of mannitol and laminarin between October and February. They concluded that the strong reduction (>90%) of laminarin over the Polar Night maintains the metabolic functions of the kelp in that period. Additionally, lower laminarin concentrations were measured in L. digitata at higher temperatures during an experimental Polar Night treatment, as also observed in S. latissima (Scheschonk et al., 2019). The faster consumption of storage carbohydrates at higher temperatures suggests an increased energy requirement of L. digitata at 5°C. An even stronger rise in winter temperatures in the future could completely deplete L. digitata energy stocks before the end of the Polar Night and thus might lead to starvation or extensive stress. A faster consumption of storage carbohydrates with increasing temperatures during Polar Night was not observed for Laminaria hyperborea (Diehl et al., 2024). The different responses of Laminariales to winter warming will presumably have an impact on seaweed diversity and species abundance in the High Arctic in the future.

Nonetheless, despite the almost complete depletion of laminarin stocks at 5°C, L. digitata was not exposed to a “starvation stress” during three months of total darkness, as seen in stable total carbon content (Total C) over the three-month experiment. Although tendencies towards decreasing Total C content were observed in the samples, the degradation was less than 10% and independent from temperature. Consequently, L. digitata must have developed a strategy to preserve C during the Polar Night period. For S. latissima, also no changes in Total C were measured after four months of darkness (Gordillo et al., 2022). We assume that at complete darkness similar processes take place in L. digitata as have been described for the growth phase, when Laminariales remobilize and utilize their storage carbohydrates for energy generation (Gómez and Huovinen, 2012). Laminarin is first transformed into mannitol. Subsequently, mannitol is degraded stepwise to generate cellular energy, releasing CO₂ which can be directly recovered by the enzyme phosphoenolpyruvate carboxykinase (PEP-CK) (Gómez and Huovinen, 2012). Comparable to the mechanism of dark carbon fixation (Wiencke et al., 2009), this allows an efficient recycling of every available C molecule to the kelp. Since we worked with non-meristematic tissues of L. digitata and the total C content was unaffected throughout the experiment, we assume that L. digitata uses the same strategy employed to restore C in times when photosynthesis is not possible. Our samples were taken in July during Polar Day, hence with almost “full carbohydrate stores” (Singh et al., 2024). We conclude that the carbohydrate reserves accumulated over the summer are sufficient to maintain the physiological functions of L. digitata during Polar Nights in future warming scenarios, as reflected in high F_v/F_m values at enhanced temperatures.

This conclusion is further supported by an observed increase in total nitrogen content (Total N) during the experiment. High environmental N availability in winter, which exceeds the N demand for protein and amino acid synthesis, enables and regulates the remobilization of carbon stocks in Laminariales (Gómez and Huovinen, 2012). We kept our samples under realistic Arctic winter nutrient conditions (~14 µmol NO₃ ⁻ L⁻¹; Rokkan Iversen and Seuthe, 2011) and observed an increase in Total N over time, with significant increases at 5°C of about 40%. Potentially, a higher metabolic and enzymatic activity at 5°C enabled enhanced N uptake (Harrison and Hurd, 2001). The stable Total C and increased Total N contents led to C:N ratios below 20 towards the end of the experiment, showing that the samples were not N-limited at both temperatures (Atkinson and Smith, 1983).

The pigment content of seaweeds responds to metabolic processes and light availability (Blain and Shears, 2019), while metabolism and enzyme activity are in turn dependent on temperature (Daniel et al., 2008). Polar red algae are known to strongly adjust their pigments concentrations during the seasonal cycle, degrading pigments during long dark exposure (Wiencke et al., 2009). Pigment degradation during extended darkness is not yet confirmed for kelps, e.g., in Arctic S. latissima populations (Scheschonk et al., 2019; Gordillo et al., 2022). We observed that all pigments in L. digitata tend to deplete over three months in the dark, decreasing more at 5°C than at 0°C. Strongest reductions were measured in the xanthophyll cycle pool (VAZ). Chla remained almost stable and Acc only decreased significantly at 5°C. While Chla is the main photosynthetic pigment and Acc are important antenna pigments, VAZ are not directly involved in the process of photon harvesting, but act as photo-protective pigments (Falkowski and Raven, 2007). Though VAZ content was highly depleted during the experiment, the protective mechanism of the xanthophyll cycle (DPS) was still active and slightly increased over time. DPS increases during stress, such as dehydration or high and low temperatures, and is known to be active in the dark (Fernández-Marín et al., 2019; Li et al., 2020; Monteiro et al., 2021). We assume that the pigments in L. digitata were degraded to save energy or function as an additional energy source to outlast the long period of the Polar Night, while still keeping the photosynthetic machinery and photo-protective mechanisms intact, as was shown by Summers et al. (2023). Pigment reduction was enhanced at 5°C compared to 0°C, which aligns with higher physiological activity in L. digitata at 5°C.

In summary, our study has shown that the cold–temperate to Arctic kelp L. digitata is well adapted to Polar Night conditions in the Arctic. Although it has a lower performance and reveals higher biochemical activity levels at 5°C than at 0°C, our results indicate that Arctic winter warming alone will not result in a serious decline of Arctic L. digitata populations in the near future. Nevertheless, interactions between warming and changing light conditions, e.g. due to terrestrial or glacial run-off, have to be considered in studies on the prospective distribution of L. digitata in High Arctic regions (Niedzwiedz and Bischof, 2023; Düsedau et al., 2024).