Intertidal estuarine habitats are inundated by seawater and uncovered with every tidal cycle, with potential exposure to both marine and atmospheric heatwaves. Little is known about the role of intertidal soft sediment ecosystems in the carbon cycle and how increasing extreme temperature events may affect carbon flux dynamics. Here we conducted a multi-day experiment simulating a low tide atmospheric heatwave at two estuary intertidal flats (sandy/muddy) to test the responses of macrobenthic biodiversity and fluxes of methane (CH4) and carbon dioxide (CO2). Results show heatwave simulation increases CO2 uptake at the sandy site and causes a switch from efflux (source) to influx (sink) of CO2 at the muddy site. Raw CH4 fluxes are unchanged by the temperature treatment but effect sizes relative to controls are greatest in muddy sediments. We provide evidence for cumulative effects of heatwave duration on macrobenthic biodiversity and greenhouse gas fluxes and show that increasing muddiness (often associated with degradation) and increasing duration of heatwave events may change the carbon source/sink status of estuaries.
Increasing anthropogenic greenhouse gas (GHG) emissions are changing our planet's climate and causing losses of biodiversity, ecosystem function, and ecosystem services worldwide. Climate change is altering temperature regimes, and increasing the frequency, intensity and duration of atmospheric and marine heatwaves. Intertidal habitats in estuaries and along the coast are particularly vulnerable because they submerge and emerge (being alternately exposed to seawater and air) during every tidal cycle. Situated at the land-sea margin, they will also bear the impacts of increased storm events that deliver increased sediments, nutrients and pollution from land and larger waves and tidal forces from the sea.
Temperature modulates all physiological processes and thus governs the functioning and biogeochemistry of ecosystems, including the carbon cycle. In general, metabolic rates of organisms increase with temperature, but this is constrained by thermodynamics and the thermal sensitivities of particular species. Climate change is increasing mean temperatures, but extreme events and increased temperature variation are likely to drive ecosystem change as organisms reach their thermal tolerance limits. Short-term extreme events such as heatwaves are strong drivers of ecosystem dynamics and resilience and are known to have long-term irreversible consequences for coastal populations, communities and their ecosystem functions [e.g. refs. ]. Cumulative effects of prolonged heat exposures are expected to differ from effects of single short-term heat exposures. Consequently, there have been many calls for studies that provide a deeper understanding of these impacts [e.g. ref. ]. Intertidal organisms may be particularly vulnerable to extreme temperature events because they are already living close to their thermal maxima.
Most research on GHG fluxes in intertidal coastal ecosystems has focussed on vegetated habitats (i.e., mangrove, saltmarsh, and seagrass for their 'blue carbon' potential). In contrast, relatively little is known about the role of 'unvegetated' (microphytobenthos dominated) intertidal flats in the carbon cycle, and how they will be influenced by higher frequency and intensity of extreme temperature events. Interest in the effects of changes in GHG emissions in intertidal habitats with broad areal coverage is driven by the potential for reinforcing feedbacks. If GHG effluxes (CO, CH) increase with increasing temperatures, this could create a feedback that contributes to accelerated climate warming.
Intertidal flats may be a significant reservoir for carbon, but their GHG emissions may offset their rates of carbon uptake. The contributions of estuaries in global GHG flux calculations are often limited to water-air fluxes, i.e., excluding sediment-air fluxes in the intertidal zone. For many estuaries, the contributions of intertidal sediments as carbon sinks remain uncertain, hampering efforts to constrain carbon budgets in estuaries with large proportions of intertidal area. A further complication is that intertidal environments can vary greatly in sediment and habitat types present, tidal ranges, exposure times, and freshwater inputs that are likely to influence GHG fluxes.
Photosynthesis by microphythobenthos is a carbon sink (i.e., CO fixation). However, it also generates oxygen as a byproduct, which increases rates of organic matter remineralisation and CO release relative to other oxidants. Organic matter remineralisation continues until available oxidants are consumed or all oxidisable organic carbon is utilised. Methane is primarily produced (methanogenesis) in anoxic sediments and is the final step in organic matter degradation producing CH and CO. Elevated temperature can be detrimental to microphytobenthic biomass and productivity, and can cause changes in community composition. Photosynthetic capacity of microphytobenthos can increase with temperature but may be inhibited at temperatures greater than 25 °C or 35 °C. Temperature influences CH production through direct effects on methanogens, and via indirect effects on carbon mineralisation and substrate availability (because mineralisation increases with temperature, which results in more carbon substrate available and therefore faster depletion of other electron acceptors).
There is a lack of data and understanding of the drivers of CH and CO fluxes in estuarine systems, especially spatial and temporal variability and dynamics. GHG fluxes on intertidal flats are known to have diurnal patterns, and fluctuations in water level have a significant effect on CO and CH fluxes. Fluxes of GHGs are influenced by temperature, generally because warming increases microbial activity, therefore heatwave simulation is expected to alter CO and CH fluxes through direct and indirect effects on the microbial community, including the microphytobenthos. The influence of temperature on microbial communities is likely to have a large influence on the biogeochemical response to heating because thermal tolerance and adaptation will vary among species, which will differentially impact different biogeochemical pathways. For example, net CH flux is the balance of activity of CH-producing methanogens and CH-consuming methanotrophs, but temperature may affect these processes differently. Temperature increases have been shown to accelerate organic matter breakdown and increase GHG production.
Changing sedimentary environments in estuaries, especially increasing bed sediment muddiness (silt + clay content), is the product of intensified anthropogenic land use, which can lead to changes in habitats and species composition, reduced ecosystem functioning, and loss of ecosystem services. Consequently, sediment mud content is used as a proxy for estuary degradation. Increasing sediment mud content can also reduce ecosystem interaction network complexity, which is an important indicator of ecosystem resilience. Sediment characteristics, especially mud content, are known to be a key regulator of carbon fluxes in tidal flats. Estuaries, at the interface of freshwater and marine ecosystems and subject to increasing sediment and organic inputs resulting from human activities, may be at risk of rapidly changing GHG emission status (switching from sinks to sources of CO). Methane emissions increase as aquatic ecosystems become more impacted by humans (especially through increases in organic inputs), and they are generally higher in freshwater ecosystems than marine ecosystems. In this study, we aim to evaluate the influence of low tide temperature extremes and subsequent impacts on GHG fluxes in unvegetated estuary intertidal flats with different sedimentary environments.
To investigate the influence of a low-tide atmospheric heatwave event on sediment-air fluxes of CO and CH we conducted a week-long field experiment using Open Top Chambers (OTCs) to increase low-tide sediment temperatures of two contrasting intertidal flats, one sandy and one muddy. We hypothesised that heatwave simulation would 1) increase the uptake of CO by stimulating photosynthetic activity of microphytobenthos (we expect surfaces to be warmed, and photosynthesis therefore enhanced, to a greater extent than within-sediment microbial respiration), and 2) increase the emission of CH by stimulating methanogenesis. We also hypothesised that 3) longer exposure to low tide heatwave simulation (i.e. cumulative days) would result in a greater effect on fluxes (i.e. effect size; the difference between control and treatment plot values). We chose heatwave treatment durations based on the definitions of atmospheric and marine heatwaves; events with at least three and five days, respectively. The 5-day treatment duration was used to satisfy the temporal conditions of heatwave definitions, and the longer duration treatment (seven days) provided an extension of this, allowing us to begin to test for cumulative effects of slightly longer heatwave duration. We expected that 4) heatwave simulation would negatively affect the benthic macrofaunal communities through loss of sensitive species. Finally, we postulated that 5) treatment effects (and hypotheses 1-4) would be site-dependent where the muddy site would show less resilience to heatwave simulation than the sandy site.