Intra‐Annual Variability in Responses of a Canopy Forming Kelp to Cumulative Low Tide Heat Stress: Implications for Populations at the Trailing Range Edge

Abstract

Anthropogenic climate change is driving the redistribution of species at a global scale. For marine species, populations at trailing edges often live very close to their upper thermal limits and, as such, poleward range contractions are one of the most pervasive effects of ongoing and predicted warming. However, the mechanics of processes driving such contractions are poorly understood. Here, we examined the response of the habitat forming kelp, Laminaria digitata, to realistic terrestrial heatwave simulations akin to those experienced by intertidal populations persisting at the trailing range edge in the northeast Atlantic (SW England). We conducted experiments in both spring and autumn to determine temporal variability in the effects of heatwaves. In spring, heatwave scenarios caused minimal stress to L. digitata but in autumn all scenarios tested resulted in tissue being nonviable by the end of each assay. The effects of heatwave scenarios were only apparent after consecutive exposures, indicating erosion of resilience over time. Monthly field surveys corroborated experimental evidence as the prevalence of bleaching (an indication of physiological stress and tissue damage) in natural populations was greatest in autumn and early winter. Overall, our data showed that L. digitata populations in SW England persist close to their upper physiological limits for emersion stress in autumn. As the intensity of extreme warming events is likely to increase with anthropogenic climate change, thermal conditions experienced during periods of emersion will soon exceed physiological thresholds and will likely induce widespread mortality and consequent changes at the population level.

Heatwaves during low tide are critical for the physiological performance of intertidal macroalgae under global warming scenarios

“…Increased air temperature caused important negative short-and intermediate-term effects on the physiological performance of the macroalgae in the field and the laboratory experiment, effects that were cumulative after exposure to two consecutive emersion cycles in the laboratory experiment. This pattern is consistent with the findings of other studies in which air temperature was found to be a relevant factor modulating physiological stress in intertidal macroalgae 6,15,20,26,37 and of others that related contractions in the distribution of intertidal macroalgae to large increases in air temperature 37,52,53 . The seawater temperatures applied in the laboratory experiment (which reflected realistic present and future climatic scenarios according to historic databases, scientific literature and IPCC predictions) were below the physiological threshold of 23 °C for B. bifurcata 54 .…”

“…If such conditions persist during few consecutive days, physiological performance of macroalgae may be negatively affected as the conditions will lead to harsh thermal and desiccation stresses 15,20 . Thus, for example, the kelp Laminaria digitata (Hudson) J. V. Lamouroux showed reduced resilience after repeated exposure to atmospheric heatwaves on emersion 25,26 . These two types of warming are, therefore, important drivers in the global distribution of intertidal canopy-forming macroalgae, leading to species decline and range shifts [27][28][29][30] with further consequences on the structure and functioning of communities and entire ecosystems 16,[31][32][33] .…”

“…In the fucoid F. serratus, air and seawater temperatures act additively 20 , which suggests that these stressors may exert some general effects on macroalgae. Consecutive periods of exposure at low tide within a single spring tidal cycle can also affect the physiological response of some species 21,25,26 . The effect of different temperatures during consecutive emersion cycles is yet unknown and it should therefore be taken into account by replicating low tide exposure experienced in the field 25 .…”

Priming of Marine Macrophytes for Enhanced Restoration Success and Food Security in Future Oceans

“…Modeling studies, based on projected carbon emission scenarios, predict that poleward range shifts will intensify (Jueterbock et al, 2013;Valle et al, 2014;Assis et al, 2016Assis et al, , 2017Chefaoui et al, 2018;Wilson and Lotze, 2019). Even if rising sea temperatures remain below lethal limits, they reduce macroalgal growth and performance (Nepper-Davidsen et al, 2019;Hereward et al, 2020;Smale et al, 2020), increase disease outbreaks and biofouling (Harley et al, 2012;Nepper-Davidsen et al, 2019;Qiu et al, 2019;Smale et al, 2020), and radically alter ecological interactions that determine persistence (Provost et al, 2017;Vergés et al, 2019)-thus compromising future sustainability of natural habitats, and production security of associated industries.…”

Ecological performance differs between range centre and trailing edge populations of a cold-water kelp: implications for estimating net primary productivity

“…Laboratory experiments have shown L. digitata can grow over a broad range of temperatures with optimum growth occurring between 10 and 15 °C (Bolton and Lüning 1982;tom Dieck 1992). Temperatures experienced in both regions during the springtime period of peakgrowth fall within this optimal temperature range, whereas during the summertime period of reduced-growth both water and air temperatures experienced at trailing edge sites can induce considerable stress (Hargrave et al 2017;Hereward et al 2020). The trailing edge region also receives more sunshine hours than the range centre, and as such, likely receives higher amounts of harmful UV radiation, causing additional stress (Bischof et al 2006).…”