Effects of temperature and nutrients on microscopic stages of the bull kelp (Nereocystis luetkeana, Phaeophyceae)

Abstract

Warming ocean temperatures have been linked to kelp forest declines worldwide, and elevated temperatures can act synergistically with other local stressors to exacerbate kelp loss. The bull kelp Nereocystis luetkeana is the primary canopy‐forming kelp species in the Salish Sea, where it is declining in areas with elevated summer water temperatures and low nutrient concentrations. To determine the interactive effects of these two stressors on microscopic stages of N. luetkeana, we cultured gametophytes and microscopic sporophytes from seven different Salish Sea populations across seven different temperatures (10–22°C) and two nitrogen concentrations. The thermal tolerance of microscopic gametophytes and sporophytes was similar across populations, and high temperatures were more stressful than low nitrogen levels. Additional nitrogen did not improve gametophyte or sporophyte survival at high temperatures. Gametophyte densities were highest between 10 and 16°C and declined sharply at 18°C, and temperatures of 20 and 22°C were lethal. The window for successful sporophyte production was narrower, peaking at 10–14°C. Across all populations, the warmest temperature at which sporophytes were produced was 16 or 18°C, but sporophyte densities were 78% lower at 16°C and 95% lower at 18°C compared to cooler temperatures. In the field, bottom temperatures revealed that the thermal limits of gametophyte growth (18°C) and sporophyte production (16–18°C) were reached during the summer at multiple sites. Prolonged exposure of bull kelp gametophytes to temperatures of 16°C and above could limit reproduction, and therefore recruitment, of adult kelp sporophytes.

Thermal performance curves identify seasonal and site‐specific variation in the development of Ecklonia radiata (Phaeophyceae) gametophytes and sporophytes

“…Sporophyte densities 42 days after zoospore release, conversely, were highest at 15–18°C, which is below the thermal optimum for gametophyte growth (~20°C) and closer to the estimated optima for gametophyte survival. Higher rates of transition from gametophyte to sporophytes at temperatures below maximal gametophyte growth have also been observed in other laminarian species (Lüning & Neushul, 1978; Martins et al., 2017; Park et al., 2017; Weigel et al., 2023) and may be due to the mutual exclusivity of gametophyte growth and gametogenesis (Hurd et al., 2014). We did not quantify sporophyte density when we measured gametophyte surface area 28 days after spore release: It is possible that gametophytes below T opt estimated for gametophyte size stopped growing and became reproductive, which would explain the higher sporophyte densities at these temperatures (15–18°C).…”

“…The thermal optima for gametophyte survival was ~3°C lower than that for growth, indicating that lower densities resulting from reduced survival might favor growth as shown in previous work (Schwoerbel et al., 2022). A thermal optimum for survival of E. radiata gametophytes below the optimum for growth has also been found for E. radiata in Western Australia in a 6‐day experiment (Mohring et al., 2013) and for Nereocystis luetkeana from the Salish Sea during a 6‐week experiment (Weigel et al., 2023). In our study, gametophyte densities at T opt were often higher than the initially estimated densities, but it is unclear if this was due to fragmentation, missed zoospores during the initial count and small germinating gametophytes during the initial measurement, or the use of lower magnification when we quantified density after 28 days.…”

“…However, the upper thermal range limit for L. digitata was consistent between both populations, and there were no differences in survival (Martins et al., 2020), whereas survival of the related L. ochroleuca was severely impacted by heatwaves at the cooler range edge over an 11‐day period (Strasser et al., 2022). Like in L. digitata , the upper temperature thresholds for gametophytes of Nereocystis luetkeana did not differ between populations in the Salish Sea after 6 weeks of cultivation (Weigel et al., 2023). Whether differences in thermal performance are due to genetic adaptation and/or thermal plasticity may depend on the species and, likely, a variety of other factors (Alsuwaiyan et al., 2021; Becheler et al., 2022; Liesner et al., 2020; Strasser et al., 2022).…”

Interactive effects of temperature and nitrogen on the physiology of kelps (Nereocystis luetkeana and Saccharina latissima)

“…Franco et al (2018) found that nitrogen had no effect on the survival of Laminaria ochroleuca at elevated temperatures, but additional nitrogen increased growth under optimal temperatures. Studies on the interactive effects of temperature and nitrogen on early life history stages of kelp (zoospores, gametophytes, and microscopic sporophytes) found that elevated temperatures were much more limiting than low nitrogen concentrations (Mabin et al, 2013;Martins et al, 2017;Muth et al, 2019;Weigel et al, 2023). These studies highlight the complexity of kelp responses to interactive stressors, including the potential for nitrogen availability to reduce negative impacts of high temperatures, and the importance of assessing nitrogen and temperature interactions across multiple species and populations.…”

“…"), and 2) sporophyte blades of N. luetkeana and Saccharina latissima collected from the same location ("species exp."). For the population exp., we collected non-reproductive blades of N. luetkeana on July 06, 2022 from two different spatially separated populations: 1) Cherry Point, Strait of Georgia, USA (48.855194, -122.730944), a warm and nutrient poor site, and 2) Turn Rock, San Juan Islands, USA (48.535333,), a cool and nutrient rich site (Weigel et al, 2023). We collected blades of N. luetkeana (n = 48 per population from distinct individuals) from the surface by carefully detaching the blade from the pneumatocyst at the narrowest point.…”