Altered nutrient cycling functionality in seagrass meadows under a simulated future marine heatwave event

Abstract

Seagrasses are important contributors to environmental nutrient cycling in marine ecosystems and can improve water quality by absorbing excess nitrogen (N). However, these ecosystems are vulnerable to human-mediated pressures, including marine heatwaves (MHWs), particularly those of longer duration. We performed an experiment simulating a 30-d, +5°C intensity MHW to examine the effects on maximum potential N cycling and transformation rates in different system compartments associated with the tropical seagrass Halophila ovalis. Under the MHW, the seagrass exhibited higher ammonium assimilation rates in the leaves, increased respiration rates, and highly variable survival and growth than those at ambient temperature. Contrary to expectations, sediment denitrification rates were lowered under the MHW, reflecting the loss of microbial functions and therefore signifying reduced N removal benefits. Moreover, the lowered seawater total alkalinity under the MHW suggests that the habitat would provide less ocean acidification buffer under future climate change. However, cycling rates in vegetated and unvegetated sediments were not significantly different, showing that the seagrass does not strongly influence the sediment N cycling capacities at this time scale. Our study demonstrates that future MHWs may alter nutrient cycling rates across ecosystem compartments in seagrass meadows, potentially leading to reductions in ecosystem function and services.

Keywords: Halophila ovalis; biogeochemistry; climate change; ecosystem services; isotopes; nitrogen.

Fig. 1

Overview of the N cycle relating to the different system compartments of seagrass meadows (Inspired by Camillini, ; Herbert, 1999). It includes N uptake processes into the seagrass through assimilation of free amino acids (FAAs), urea, ammonium, and nitrate from the overlying water, along with sediment processes, anammox, nitrification, DNRA, and nitrification in oxic and anoxic depths of the sediment.

Fig. 2

Overlying water analysis from experimental tanks, including (a) total alkalinity and (b) nitrate concentration under different temperature treatments and vegetation presence and absence. Boxplots represent median, upper, and lower quartiles, with the diamonds showing the mean values and individual points showing each measurement. Different letters indicate statistical differences from ANOVA main effects tests (‘Treatment’ and ‘Vegetation’). MHW, marine heatwave.

Fig. 3

Halophila ovalis seagrass growth and metabolism measurements at the end of the experiment, including (a) seagrass ramet mortality percentage per tank, (b) change in leaf density per tank, (c) respiration rate, and (d) net primary productivity rate, calculated from changes in dissolved oxygen concentrations. Boxplots represent median, upper, and lower quartiles, with the diamonds showing the mean values and individual points showing each measurement. Different letters indicate statistical differences from ANOVA main effects tests (‘Treatment’). Graphs without letters revealed no statistical differences between any treatments. MHW, marine heatwave.

Fig. 4

Halophila ovalis seagrass nitrogen uptake rates of (a) NH₄ ⁺ through assimilation and (b) N₂ through fixation, along with the naturally occurring abundance of (c) δ¹³C, (d) N%, and (e) C% in the above (leaves) and belowground (roots and rhizome) compartments. Boxplots represent median, upper, and lower quartiles, with the diamonds showing the mean values and individual points showing all measurements. Different letters indicate statistical differences from ANOVA main effects tests (‘Treatment’ and ‘Compartment’, but a post hoc Tukey test for (a) since there was a ‘Treatment’ × ‘Compartment’ interaction). Graphs without letters revealed no statistical differences between any treatments. MHW, marine heatwave.

Fig. 5

Sediment maximum potential N utilization rates in (a) DNRA, (b) denitrification, (c) anammox, as well as rates of (d) nitrification. Boxplots represent median, upper, and lower quartiles, with the diamonds showing the mean values and individual points showing all measurements. Different letters indicate statistical differences from ANOVA main effects tests (‘Treatment’ and ‘Vegetation’). Graphs without letters revealed no statistical differences between any treatments. MHW, marine heatwave.

Fig. 6

Gene copies in the sediment encoding enzymes involved in denitrification, specifically (a) nirS in nitrite reduction and (b) nosZ in nitrous oxide reduction. Boxplots represent median, upper, and lower quartiles, with the diamonds showing the mean values and individual points showing all measurements. Different letters indicate statistical differences from ANOVA main effects tests (‘Treatment’ and ‘Vegetation’). MHW, marine heatwave.

Fig. 7

Summary of the average flux of maximum potential rates of seagrass leaf N uptake (ammonium assimilation and N₂ fixation), sediment N loss (denitrification and anammox), and N retention (DNRA and nitrification) in the experimental tanks. Arrows show the direction of the N movement in the different seagrass meadow system compartments, with the size of the arrows indicating the magnitude of the flux. Rates are in μmol N h⁻¹, standardized by the approximate wet weight of the sediment and seagrass in each tank (1.15 kg of sediment and 0.112 g seagrass, from unpublished data). Error values indicate the standard deviation between treatment replicates. MHW, marine heatwave.