The negative effects of short-term extreme thermal events on the seagrass Posidonia oceanica are exacerbated by ammonium additions

Abstract

Global warming is increasingly affecting our biosphere. However, in addition to global warming, a panoply of local stressors caused by human activities is having a profound impact on our environment. The risk that these local stressors could modify the response of organisms to global warming has attracted interest and fostered research on their combined effect, especially with a view to identifying potential synergies. In coastal areas, where human activities are heavily concentrated, this scenario is particularly worrying, especially for foundation species such as seagrasses. In this study we explore these potential interactions in the seagrass Posidonia oceanica. This species is endemic to the Mediterranean Sea. It is well known that the Mediterranean is already experiencing the effects of global warming, especially in the form of heat waves, whose frequency and intensity are expected to increase in the coming decades. Moreover, this species is especially sensitive to stress and plays a key role as a foundation species. The aim of this work is thus to evaluate plant responses (in terms of photosynthetic efficiency and growth) to the combined effects of short-term temperature increases and ammonium additions.To achieve this, we conducted a mesocosm experiment in which plants were exposed to three thermal treatments (20°C, 30°C and 35°C) and three ammonium concentrations (ambient, 30 μM and 120 μM) in a full factorial experiment. We assessed plant performance by measuring chlorophyll fluorescence variables (maximum quantum yield (Fv/Fm), effective quantum yield of photosystem II (ΔF/Fm’), maximum electron transport rate (ETRmax) and non-photochemical quenching (NPQ)), shoot growth rate and leaf necrosis incidence. At ambient ammonium concentrations, P. oceanica tolerates short-term temperature increases up to 30°C. However, at 35°C, the plant loses functionality as indicated by a decrease in photosynthetic performance, an inhibition of plant growth and an increase of the necrosis incidence in leaves. On the other hand, ammonium additions at control temperatures showed only a minor effect on seagrass performance. However, the combined effects of warming and ammonium were much worse than those of each stressor in isolation, given that photosynthetic parameters and, above all, leaf growth were affected. This serves as a warning that the impact of global warming could be even worse than expected (based on temperature-only approaches) in environments that are already subject to eutrophication, especially in persistent seagrass species living in oligotrophic environments.

Species-Specific Trait Responses of Three Tropical Seagrasses to Multiple Stressors: The Case of Increasing Temperature and Nutrient Enrichment

“…These results are in accordance with other studies with temperate species that showed no interactive effects on fluorescence parameters or growth (Bintz et al, 2003;Moreno-Marín et al, 2018;Ontoria et al, 2019b). However, in some studies significant interactions were found for yield, growth (Kaldy, 2014;Mvungi and Pillay, 2019;Ontoria et al, 2019a), or photosynthetic rate, as well as gross production rates (Egea et al, 2018;Moreno-Marín et al, 2018). Comparison among studies is difficult due to the variable traits measured; and care must be taken when comparing results that differ in exposure period, the intensity of the stressors (e.g., nutrient concentration used), or even the different geographical areas of the species, as all these factors, among others, might affects the plasticity of seagrass traits.…”

Does Warming Enhance the Effects of Eutrophication in the Seagrass Posidonia oceanica?

“…Optimum growth temperature for this temperate species range from 11.5 to 26 • C (Olsen et al, 2012). However, this optimal range probably depends on other co-occurring environmental factors, such as nutrient availability, leaf senescence and nutrient partitioning within plant tissues (Ontoria et al, 2019a). Indeed, photochemical efficiency and carbohydrate reserves of OL plants were not affected by warming in this study.…”

“…Few multi-factorial experiments have been performed on P. oceanica, including some assessing nutrient (ammonium) input and temperature (Gera et al, 2013;Ontoria et al, 2019a). In these studies, different levels of synergism have been found between stress factors, influencing negatively the survival, photosynthesis and plant growth.…”

“…However, the consequences of the combined effect of both stressors on the plant physiology are virtually unknown. A recent microcosm study on P. oceanica examined the interactions between ammonium addition and high temperature (Ontoria et al, 2019a). In this case, synergism between factors caused a decrease of about 70% in photosynthetic performance indicating the harming potential of eventual heat waves in areas exposed to high anthropic pressures.…”

Too hot to handle: Unprecedented seagrass death driven by marine heatwave in a World Heritage Area

“…When slow‐growing persistent seagrass species are disturbed, they can take decades to recover (O'Brien et al, 2018). Any recovery may also be inhibited by ongoing heating and recurrent MHWs (Marbà & Duarte, 2009) as well as synergistic pressures, such as heat stress and nutrients (Ontario, Cuesta‐Gracia, Ruiz, Romero, & Pérez, 2019). Following the 2011 WA MHW, Shark Bay was subjected to above average SST for several years (Gilmour et al, 2019), which may have impeded recovery rates of persistent seagrasses, prolonging the impacts associated with the initial loss.…”