Spatial and temporal variability of carbon budgets of shallow South African subtropical estuaries
Graphical abstract
Introduction
Estuarine areas are recognized as important carbon reservoirs able to sustain high burial rates and act as net carbon storages (Kuwae et al., 2016). However, this is only one aspect of the estuarine carbon budget since the intense mineralisation and respiration activities, promoted by terrestrial inputs, generally lead to a net heterotrophic state (Chen and Borges, 2009; Herrmann et al., 2015). Carbon budgets in estuarine systems are therefore a delicate balance between carbon burial and CO2 emissions strongly dependent on the environmental conditions and on anthropic pressure (Kuwae et al., 2016).
Several anthropogenic activities such as nutrient inputs, water abstraction and wetland degradation, together with climate change pressures have been known to affect estuarine carbon fluxes and enhance CO2 degassing (Bauer et al., 2013; Dai et al., 2006). Estuaries constitute a crucial link between terrestrial and oceanic ecosystems propagating human impacts through the global carbon cycle (Bauer et al., 2013). Therefore, the study and monitoring of these areas is fundamental for the understanding of both land-ocean and ocean-atmosphere CO2 fluxes.
The Intergovernmental Panel on Climate Change (IPCC) recognized that estuaries could constitute a significant component of coastal CO2 emissions, but there is still great uncertainty due to the high heterogeneity of these areas (IPCC, 2013). While in the last few decades several studies focused on coastal carbon budgets and dynamics, still little information is available on subtropical estuarine systems (Chen and Borges, 2009; Eyre et al., 2011; Maher and Eyre, 2012). Furthermore, the majority of studies on estuarine carbon budgets have been performed on macro-tidal estuaries and very little information is available on other types of estuarine ecosystems (Borges et al. 2005).
Although South Africa has nearly 300 estuaries, very little is known about their contribution to carbon emissions or sequestration (Anandraj et al., 2007; Froneman, 2002). South African estuaries are highly heterogeneous in term of biotic, hydrodynamic and physico-chemical characteristics and numerous systems are subjected to strong anthropic pressures (Van Niekerk et al., 2013; Whitfield, 1992). In the subtropical area, primary production and biomasses have been shown to vary significantly between estuaries but also within the same system depending on the hydrodynamic conditions (Anandraj et al., 2007; Anandraj et al., 2008; Ortega-Cisneros et al., 2014).
Since carbon cycling in estuaries can vary tremendously both spatially and temporally, within and between estuaries, there is a strong need for systematic flux estimations on small and local spatial scales (Bauer et al., 2013; Eyre et al., 2011). Oxygen and nutrient community fluxes are good indicators of critical ecological processes such as photosynthesis and remineralisation of organic matter (Pratt et al., 2015). Moreover, incubation-based estimations can provide direct and detailed information on the contribution of the various communities to the global processes (Hopkinson and Smith, 2005; Maher and Eyre, 2012).
For these reasons, this study aimed to provide an estimation of carbon fluxes of two South African subtropical estuaries through a direct quantification of nutrient, respiration and primary production fluxes. In situ fluxes were measured simultaneously in the benthic and pelagic communities on a seasonal basis together with the main biotic and abiotic parameters in order to explore the drivers affecting the metabolic fluxes.
We hypothesize that, due to high organic matter and nutrient fluxes, the communities will be net heterotrophic predominantly during the rainy season (Ortega-Cisneros et al., 2016). We also expect that areas submitted to stronger anthropogenic pressure will exhibit higher carbon emissions (CO2) than the other sites and that spatial and temporal change in the environmental conditions will lead to changes in the balance between benthic and pelagic productivity.
Section snippets
Experimental sites and set up
This study focused on two subtropical estuarine areas with opposite characteristics, both located to the north of Durban on the KwaZulu-Natal coast, South Africa. The Mdloti Estuary is a temporarily open/closed system generally shallow with a low salinity (Deale et al., 2013). The estuary has been classified as largely modified with fair health (Van Niekerk et al., 2013). The Mlalazi estuary is a permanently open system that may only close during major droughts. The estuary is located within
Water and sediment proprieties
The benthic chambers were installed at depths ranging from 0.4 and 1.6 m depending on the site and on the tide. During the experiments, daily mean water temperature ranged between 16.1 and 28.8 °C in Mdloti and between 18.9 and 25.8 °C in Mlalazi estuaries (Table 1). Salinity in Mdloti was always lower than 2.7 with a minimum of 0.4 in winter. Conversely, the salinity in Mlalazi was relatively high and ranged between 25.7 in summer to 36.1 in autumn (Table 1).
Throughout the year, TSS content
Discussion
This study represents the first direct quantification of both benthic and pelagic primary production and respiration of estuaries in South Africa. Previous authors rather focused on microalgae production exclusively or on sediment-water interface solely (Anandraj et al., 2007, Anandraj et al., 2008; Fielding et al., 1988; Froneman, 2002; Human et al., 2015). Their results showed that primary production and biomass are strongly influenced by the estuarine mouth status and by the seasonal
Conclusions
Our study focused specifically on two contrasting estuarine environments in the South African subtropical region. The results confirm our hypothesis on spatial and temporal heterogeneity of the carbon fluxes between and within systems. The remarkable differences in functioning and carbon budgets between estuaries, together with the lack of models estimating carbon dynamics and exports can lead to important errors in the quantification of carbon budgets in estuarine communities. Our results
Authors' contributions
M. Tagliarolo conceived the experiments, developed the methodology, collected the data, analysed the data and wrote the manuscript. U. M. Scharler funded the project, analysed the data and wrote the manuscript.
Acknowledgements
We would like to thank Ezemvelo KZN Wildlife for their support during fieldwork and Fiona Mackay (Oceanographic Research Institute, Durban) for the help with macrozoobenthos identification. Many thanks also to Kajal Lechman, Dane Garvie, Thembeka Radebe, Kendyl Le Roux and Gavin Tweddle for assistance in the field.
We would like to thank Dr. Francesca Porri (SAIAB, Rhodes University) for providing the Fibox oxygen meter.
Data accessibility
All data are accessible in the paper.
References (54)
- et al.
A comparative study of microalgal production in a marine versus a river-dominated temporarily open/closed estuary, South Africa
Estuar. Coast. Shelf Sci.
(2007) - et al.
The recovery of microalgal production and biomass in a South African temporarily open/closed estuary, following mouth breaching
Estuar. Coast. Shelf Sci.
(2008) - et al.
Reconciling opposing views on carbon cycling in the coastal ocean: continental shelves as sinks and near-shore ecosystems as sources of atmospheric CO2
Deep-Sea Res. II Top. Stud. Oceanogr.
(2009) - et al.
Oxygen depletion in the upper reach of the Pearl River estuary during a winter drought
Mar. Chem.
(2006) - et al.
Organism responses to habitat fragmentation and diversity: habitat colonization by estuarine macrofauna
J. Exp. Mar. Biol. Ecol.
(1999) - et al.
Benthic diatom biomass, production and sediment chlorophyll in Langebaan lagoon, South Africa
Estuar. Coast. Shelf Sci.
(1988) Response of the plankton to three different hydrological phases of the temporarily open/closed Kasouga estuary, South Africa
Estuar. Coast. Shelf Sci.
(2002)- et al.
Effect of production and biomass of intertidal microphytobenthos on meiofaunal grazing rates
J. Exp. Mar. Biol. Ecol.
(1995) - et al.
Resilience of estuarine phytoplankton and their temporal variability along salinity gradients during drought and hypersalinity
Estuar. Coast. Shelf Sci.
(2015) - et al.
Inlet mouth phase influences density, variability and standing stocks of plankton assemblages in temporarily open/closed estuaries
Estuar. Coast. Shelf Sci.
(2014)
Comparative study of methodologies to measure in situ the intertidal benthic community metabolism during immersion
Estuar. Coast. Shelf Sci.
Phytoplankton biomass and size structure in two South African eutrophic, temporarily open/closed estuaries
Estuar. Coast. Shelf Sci.
Country-wide assessment of estuary health: an approach for integrating pressures and ecosystem response in a data limited environment
Estuar. Coast. Shelf Sci.
Biogeochemical generation of dissolved inorganic carbon and nitrogen in the North Branch of inner Changjiang estuary in a dry season
Estuar. Coast. Shelf Sci.
Qualitative and quantitative interactions between microphytobenthos and herbivorous meiofauna on a brackish intertidal mudflat
Internationale Revue Der Gesamten Hydrobiologie Und Hydrographie
The changing carbon cycle of the coastal ocean
Nature
Environmental drivers of benthic flux variation and ecosystem functioning in Salish Sea and Northeast Pacific sediments
PLoS One
Budgeting sinks and sources of CO2 in the coastal ocean: Diversity of ecosystems counts
Geophys. Res. Lett.
Factors controlling net ecosystem metabolism in U.S. estuaries
Estuaries
The utilization of inorganic and organic phosphorous compounds as nutrients by eukaryotic microalgae: a multidisciplinary perspective: part 2
CRC Crit. Rev. Microbiol.
Phytoplankton primary production in the world's estuarine-coastal ecosystems
Biogeosciences
Recovery dynamics of zooplankton following mouth-breaching in the temporarily open/closed Mdloti Estuary, South Africa
Afr. J. Aquat. Sci.
Respiration in Aquatic Ecosystems
Resource Directed Measures: reserve determination study of selected surface water and groundwater resources in the Usutu/Mhlathuze Water Management Area
Metabolism of different benthic habitats and their contribution to the carbon budget of a shallow oligotrophic sub-tropical coastal system (southern Moreton Bay, Australia)
Biogeochemistry
Grazing on intertidal microphytobenthos by macrofauna: is pheophorbide a a useful marker?
Mar. Ecol. Prog. Ser.
Impact of dissolved organic phosphorus on the competition for phosphorus between algae and bacteria in Lake Constance
Arch. Hydrobiol. Beih. Ergebn. Limnol
Cited by (12)
How drought affects range and variability of environmental conditions in two subtropical South African estuaries
2023, Estuarine, Coastal and Shelf ScienceHealthy aquatic ecosystem, towards sustainable food supply
2023, Innovation of Food Products in Halal Supply Chain WorldwideSpatial distribution and influencing mechanism of CO<inf>2</inf>, N<inf>2</inf>O and CH<inf>4</inf> in the Pearl River Estuary in summer
2022, Science of the Total EnvironmentCitation Excerpt :In addition, the ecological services of estuarine waters are valued in terms of the provision of abundant material products and the storage of sedimentary organic carbon (Canuel et al., 2012). Increasing anthropogenic disturbances such as fertilizer use, soil erosion, and sewage discharge (Yevenes et al., 2016) increase C and N inputs to estuaries, leading to dramatic changes in the nutritional status of coastal aquatic ecosystems (Murray et al., 2015; Tagliarolo and Scharler, 2018), which in turn affect GHGs production and emissions (Harley et al., 2015; Rosentreter et al., 2021). Estuarine ecosystem C cycles are an important part of the global C budget.
Comparing production and life-history traits of a key amphipod species within and between estuaries under different levels of anthropogenic pressure: amphipod dynamics under varying anthropogenic pressure
2022, Marine Environmental ResearchCitation Excerpt :The within sites variability observed in E. marinus production and life-history traits of the three studied populations suggests that the sampled sites at Mondego estuary present a lower variability related to the factors that control and favour the production and fitness of the gammarid, compared to Ave and Minho. Spatial heterogeneity is a common feature of estuaries and other coastal areas linked to environmental gradients determined by the upstream freshwater input and the downstream saltwater entrance, originating salinity and organic matter gradients, variability on nutrient budgets and different types of sediments (Lillebø et al., 2004; Tagliarolo and Scharler, 2018; Chu et al., 2020). In turn, these variations create distinct microhabitat structures, such as substratum patches, different patch shapes and sizes, epiphytic microstructures, distinct depth and wave exposure, and settlement of different algal types (Bologna and Heck, 2002; Korpinen and Westerbom, 2010; García-Roger et al., 2013), which play an important role on the fitness and spatial distribution of aquatic macroinvertebrates, namely, gammarids (Korpinen and Westerbom, 2010).
Analysing 70 years of research output on South African estuaries using bibliometric indicators
2021, Estuarine, Coastal and Shelf ScienceCitation Excerpt :Research conducted on South African estuaries has covered a wide range of topics. These include isotopic ecological niche partitioning and isotopic tracing of salt loads (Muller and Strydom, 2017; Sigidi et al., 2017), salt marsh response to climate change (Tabot and Adams, 2019; Raw et al., 2020), geographic distribution of mangroves (Adams and Rajkaran, 2020; Taylor, 2020), microalgae as indicators (Lemley et al., 2016), mangrove carbon storage (Tagliarolo and Scharler, 2018; Johnson et al., 2020), macrophyte relationships with fishes (Whitfield, 2017; Wasserman et al., 2020), nutrient cycling (Adams et al., 2020b; Human et al., 2020), and pollution (Adeniji et al., 2019; Olisah et al., 2020). To protect biodiversity, various studies have produced guidelines to manage human use in different estuary types (van Niekerk et al., 2020; Wooldridge and Adams, 2020).
Dynamics of organic carbon under bioturbation by mud crabs (Macrophthalmus japonicus) and clamworms (Perinereis aibuhitensis) in an estuary ecosystem
2021, Journal of Experimental Marine Biology and EcologyCitation Excerpt :The estuary often has “filtering” or “buffering” effects on chemical substances from terrestrial ecosystem, presenting a non-conservative behavior of surplus or loss (Ford et al., 2005; Tang et al., 2010). The organic carbon flux at the sediment-water interface in estuarine area not only plays an important role in maintaining the food chain and biodiversity of coastal ecosystem, but also affects the one-way transfer of carbon from global terrestrial carbon pool to marine carbon pool (Tagliarolo and Scharler, 2018). Bioturbation, defined as the biological activity such as feeding, excretion, bulldozing, burrowing, and construction of tubes, mounds, and pits by macrobenthos in estuarine sediments, profoundly affects nutrients exchange of sediment-water interface (Thayer, 1979; Sun and Torgersen, 2001; Zhang et al., 2019).