Microscopic life stages of North Atlantic Laminaria digitata (Phaeophyceae) exhibit trait-depedent thermal adaptation along latitudes

Kelp forests in the North Atlantic are at risk of decline at their warm temperature distribution margins due to anthropogenic temperature rise and more frequent marine heat waves. To investigate the thermal adaptation of the cold-temperate kelp Laminaria digitata, we sampled six populations, from the Arctic to Brittany (Spitsbergen, Tromsø, Bodø [all Norway], Helgoland [Germany], Roscoff and Quiberon [both France]), across the species’ entire distribution range, spanning 31.5° latitude and 12-13°C difference in mean summer sea surface temperature. We used pooled vegetative gametophytes derived from several sporophytes to approximate the genetic diversity of each location. Gametophytes were exposed to (sub-) lethal high (20-25°C) and (sub-) optimal low (0-15°C) temperature gradients in two full-factorial, common-garden experiments, subjecting subsets of populations from different origins to the same conditions. We assessed survival of gametophytes, their ability to develop microscopic sporophytes, and subsequent growth. We hypothesized that the thermal performance of gametophytes and microscopic sporophytes corresponds to their local long-term thermal history. Integrated gametophyte survival revealed a uniform upper survival temperature (UST) of 24°C among five tested populations (Tromsø to Quiberon). In contrast, following two weeks of thermal priming of gametophytes at 20-22°C, sporophyte formation at 15°C was significantly higher in southern populations (Quiberon and Roscoff) compared to the high-latitude population of Tromsø. Between 0-15°C, survival of the Arctic population (Spitsbergen) was negatively correlated with increasing temperatures, while the southernmost population (Quiberon) showed the opposite. Thus, responses of survival at low, and sporophyte formation at high temperatures, support the concept of local adaption. On the other hand, sporophyte formation between 0-15°C peaked at 6-9°C in the Quiberon and at 9-12°C in the Spitsbergen population. Sporophyte growth rates (GR) both in length and width were similar for Spitsbergen, Tromsø and Quiberon; all had maximum GRs at 12-15°C and low GRs at 0-6°C. Therefore, responses of sporophyte formation and growth at low temperatures do not reflect ecotypic adaptation. We conclude that L. digitata populations display trait-dependent adaptation, partly corresponding to their local temperature histories and partly manifesting uniform or unpredictable responses. This suggests differential selection pressures on the ontogenetic development of kelps such as L. digitata

Performance of different life cycle stages of the Arctic kelps Laminaria digitata and Saccharina nigripes along temperature gradients

Understanding the physiological responses of macroalgae to changing temperatures is crucial to predict future scenarios ecosystems will face due to climate change. The two phenotypically similar kelp species, Laminaria digitata and Saccharina nigripes, inhabit overlapping ecological niches in the Arctic but their southern distribution boundary is dissimilar. This suggests a different adaptation towards temperature as their life cycle stages have to withstand a broad temperature range from Arctic to Sub-Arctic or temperate waters. The present study, comparatively investigated the respective two life cycle stages (sporophytes and gametophytes) of both kelp species, starting from unialgal clonal cultures. Gametophytes and sporophytes were subjected to temperature gradients in the laboratory in a full-factorial approach. Gametogenesis, sporophyte recruitment and gametophyte survival was followed in gametophytes. Growth rate, photosynthetic quantum yield and chlorophyll fluorescence vs. irradiance curves (PI-curves) in sporophytes all over two weeks. L. digitata gametophytes and sporophytes survived 24 and 22 °C and thereby 4 and 5 °C higher temperatures than S. nigripes gametophytes and sporophytes, respectively. Although both species recruited between 0-10 °C and L. digitata also at 15 °C. S. nigripes sporophytes showed a much better performances at 0 and 5 °C than L. digitata in growth, but not in photosynthetic parameters. The overall temperature performance of S. nigripes that was investigated here for the first time shows a true Arctic affinity, while L. digitata behaves similarly than populations from temperate populations. Future increase in Arctic seawater temperatures, especially over winter, most probably will reduce presence of S. nigripes. Whether both species take the same or different functional roles in Arctic kelp forest communities is however still non-resolved

Looks can be deceiving: contrasting temperature characteristics of two morphologically similar kelp species co-occurring in the Arctic

Two morphologically similar digitate kelp species, Laminaria digitata and Hedophyllum nigripes, co-occur along a shallow sublittoral depth gradient in the Arctic but, in contrast to L. digitata, very few ecophysiological data exist for H. nigripes. We investigated growth, survival, photosynthetic characteristics and carbon:nitrogen ratios of juvenile sporophytes, and recruitment and survival of gametophytes in genetically verified Arctic isolates of both species along temperature gradients (0–25 °C) over 14 days. Laminaria digitata gametophytes survived 23–24 °C, while sporophytes survived 21–22 °C. Hedophyllum nigripes had lower temperature affinities. Gametophytes survived 19–21 °C, while sporophytes survived 18 °C. Male gametophytes were more heat-tolerant than female gametophytes in both species. The pronounced cold adaption of H. nigripes compared to L. digitata also became apparent in different sporophyte growth optima (L. digitata: 15 °C; H. nigripes: 10 °C) and gametogenesis optima (L. digitata: 5–15 °C; H. nigripes: 0–10 °C).Higher carbon:nitrogen ratios in H. nigripes suggest an adaptation to nutrient poor Arctic conditions. The overall temperature performance of H. nigripes possibly restricts the species to Arctic–Sub-Arctic regions, while Arctic L. digitatabehaved similarly to cold-temperate populations. Our data suggest that a future increase in seawater temperatures may hamper the success of H. nigripes and favour L. digitata in Arctic environments

Contrasting temperature chracteristics of Laminaria digitata and Hedophyllum nigripes - C:N-ratio, growth rate, PAM fluorometry, gametogenesis

We investigated effects of temperature on gametophytes and sporophytes of the two morphologically similar kelp species Laminaria digitata and Hedophyllum nigripes co-occurring in the Arctic. We quantified gametogenesis, sporophyte recruitment and growth, optimal quantum yield and carbon and nitrogen content of sporophytes, as well as survival of both life cycle stages along temperature gradients (0-25°C), using several unialgal strains isolated from the European Arctic in Kongsfjorden, western Spitsbergen

Information on Laminaria hyperborea samples off the island of Helgoland in summer 2014

Laminaria hyperborea off the island of Helgoland (North Sea, Germany) was sampled along a depth gradient (0.5, 2, 4, 6 m) throughout summer 2014. Stipe length of the sporophyte was measured. In blade discs from three different blade regions (5, 25 and 50 cm above the stipe-blade transition zone) dry mass, fresh mass and dry mass:area ratio were measured

Dataset for estimating the photosynthetic oxygen production of Laminaria hyperborea off the island of Helgoland in summer 2014

The impact of variable underwater photosynthetically active radiation (PAR) and photosynthetic parameters on photosynthetic oxygen production of Laminaria hyperborea off the island of Helgoland (North Sea, Germany) was investigated throughout summer 2014. L. hyperborea was sampled along a depth gradient (0.5, 2, 4, 6 m) and discs from three different blade regions (5, 25 and 50 cm above the stipe-blade transition zone) were set into photosynthesis versus irradiance (PI) curves. After cutting and before the oxygen incubation, maximum quantum yield (Fv/Fm) were measured as a health indicator. PI-curve parameters were normalized to either fresh mass or disc area. Additionally, chlorophyll a content was measured in each disc and normalized to the same two parameters as PI parameters. In situ PAR was measured in different depths (1.2, 2.9, 4.4, 6.6 m) to gain daily diffuse vertical attenuation coefficient (Kd). PAR along the vertical depth profile was calculated and together with PI-curve parameters oxygen production was calculated along the vertical depth profile. Leaf area index (Pehlke and Bartsch, 2008) was used to extrapolate oxygen production rates to seafloor and a photosynthetic quotient (PQ) of 1.18 (Miller III et al., 2009) to convert rates into carbon fixation rates. This net primary production (NPP) was given along the vertical depth profile based on different Kd values (daily Kd, mean Kd, minimum Kd, maximum Kd)

Photosynthetically active radiation measured in different water depths near the island of Helgoland in summer 2014

In-situ photosynetically active radiation (PAR) was measured in different depths (1.2, 2.9, 4.4, 6.6 m) every 10-15 min during summer 2014. Odyssey PAR loggers were calibrated against a cosine-corrected planar PAR sensor (LI-190SA quantum sensor, LI-COR Inc., USA) over a 24 h period at 4 m depth in the Helgolandic South harbor. During the Laminaria hyperborea sampling period (seven weeks), incoming PAR was recorded continuously every 15 min at 1.2 and 2.9 m, and every 30 min at 4.4 and 6.6 m near the sampling area of sporophytes. To avoid biofouling of the sensor heads, PAR loggers were cleaned every week (1.2 m) or every second week (all other depths) by SCUBA divers

Maximum quantum yield measured in Laminaria hyperborea off the island of Helgoland in summer 2014

Laminaria hyperborea off the island of Helgoland (North Sea, Germany) was sampled along a depth gradient (0.5, 2, 4, 6 m) throughout summer 2014. Discs were cut from three different blade regions (5, 25 and 50 cm above the stipe-blade transition zone). The maximum quantum yield of photosystem II was measured after cutting and after one night of wound healing before oxygen measurements were conducted using pulse-amplitude-modulated fluorometry (PAM 2100, WALZ, Germany)

Chlorophyll a content of Laminaria hyperborea off the island of Helgoland in summer 2014

Laminaria hyperborea off the island of Helgoland (North Sea, Germany) was sampled along a depth gradient (0.5, 2, 4, 6 m) throughout summer 2014. Chlorophyll a content was measured. Discs were cut from three different blade regions (5, 25 and 50 cm above the stipe-blade transition zone) and normalized to either dry mass, fresh mass or disc area. The samples were freeze-dried for approximately 36 h (Beta 1–8 LDplus, Christ, Osterode am Harz, Germany), finely ground for several minutes using steel grinding balls (3 mm diameter) in a Mikro-Dismembrator U (Braun Biontech International, Melsungen, Germany), cooled centrifuged (Centrifuge 3K10, Sigma, Osterode, Germany), and measured in the spectrophotometer (U-3310, Hitachi High-Tech, Japan) at two wavelengths (347 and 664.5 nm)