Science of the Total Environment 624 (2018) 945–954
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Natural nutrient enrichment and algal responses in near pristine micro-estuaries and micro-outlets L.R.D. Human a,e,⁎, M.L. Magoro b,c, T. Dalu c,d, R. Perissinotto b, A.K. Whitfield c, J.B. Adams a, S.H.P. Deyzel e,f, G.M. Rishworth b a
Department of Botany, Institute for Coastal and Marine Research, Nelson Mandela University, Summerstrand South Campus, Port Elizabeth 6031, South Africa SARChI Chair: Shallow Water Ecosystems, Nelson Mandela University, Summerstrand South Campus, Port Elizabeth 6031, South Africa South African Institute for Aquatic Biodiversity, Grahamstown 6139, South Africa d Department of Ecology and Resource Management, University of Venda, Thohoyandou, Limpopo, South Africa e South African Environmental Observation Network, Elwandle Coastal Node, Ocean Science Campus, Nelson Mandela University, Port Elizabeth 6031, South Africa f Department of Zoology, Institute for Coastal and Marine Research, Nelson Mandela University, Summerstrand South Campus, Port Elizabeth 6031, South Africa b c
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• Naturally-occurring pristine estuarine ecosystems are rare worldwide. • Drivers and state shifts in algae were assessed in estuaries of varying quality. • Algal growth related to temperature, nutrient conditions and water residence time • Nutrient enrichment drove expected mesotrophic/eutrophic water body responses. • Only naturally-pristine systems revert to pre-enriched states after enrichment.
a r t i c l e
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Article history: Received 20 October 2017 Received in revised form 15 December 2017 Accepted 17 December 2017 Available online xxxx Editor: G. Ashantha Goonetilleke Keywords: Nutrient enrichment Phytoplankton Microphytobenthos Macroalgae Micro-estuary Micro-outlet
a b s t r a c t Naturally-occurring pristine estuarine ecosystems are rare in modern environments due to anthropogenic encroachment. There are more than 100 outlets around the South African coast arising from streams flowing from small catchments close to the sea. Eight near natural systems were sampled seasonally over the period of a year to acquire baseline information on water quality and chlorophyll a status across a variety of algal guilds (benthic microalgae, phytoplankton and macroalgal cover). Albeit on a much smaller-scale, these systems represent natural surrogates of larger temporarily open/closed estuaries (TOCEs). Inorganic nutrients (ammonium, total oxidized nitrogen and soluble reactive phosphate), phytoplankton and microphytobenthos chlorophyll a, as well as macroagal percentage cover, were measured using standard methods. Algae showed a seasonal trend, with blooms of both micro- and macro-algae occurring during summer, with a dieback recorded in autumn. During summer, only one system had a phytoplankton peak in chlorophyll a above 20 μg L−1, while the microphytobenthos concentrations in three of the systems were above 100 mg m−2. Summer blooms of green filamentous macroalgae occurred in all four micro-outlets and in one micro-estuary. Using a linear mixed-effects modelling approach, significant drivers for algal growth related to temperature, nutrient conditions, light availability and water residence time, all of which are known to stimulate primary production. The results show that enrichment from natural sources display similar responses from primary producers to mesotrophic and/or
⁎ Corresponding author at: South African Environmental Observation Network, Elwandle Coastal Node, Ocean Science Campus, Nelson Mandela University, Port Elizabeth 6031, South Africa. E-mail addresses:
[email protected],
[email protected] (L.R.D. Human).
https://doi.org/10.1016/j.scitotenv.2017.12.184 0048-9697/© 2017 Elsevier B.V. All rights reserved.
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L.R.D. Human et al. / Science of the Total Environment 624 (2018) 945–954
eutrophic water bodies, with the exception that they revert to a natural state rather than continue into a degraded state as is the case in artificially enriched systems. This importantly demonstrates how larger temporarily/ open closed estuaries, most of which are anthropogenically degraded, might have functioned under a former more balanced state. Some of these larger systems now respond to nutrient enrichment by exhibiting permanent cultural eutrophication. © 2017 Elsevier B.V. All rights reserved.
1. Introduction Nutrient enrichment on inland and coastal waters is highlighted as one of the major threats to modern ecosystem integrity (Paerl and Scott, 2010). Concomitant increases in the productivity of primary producers such as phytoplankton, microphytobenthos, seagrass and macroalgae results in competition between these groups under persistently enriched conditions, leading to one or more species dominating the system or displacing other taxa. This in turn has cascading effects through the food web, as one or more food sources may be eliminated whilst simultaneously limiting biodiversity. The transformed ecosystem is often characterized by an increased macro- and micro-algal biomass, shifts in community composition, harmful or toxic algal blooms, red tides, loss of submerged macrophytes and fish kills (Bricker et al., 2003; Devlin et al., 2011; Human et al., 2016a, 2016b). Following decomposition of primary producer biomass, a dramatic decrease in the dissolved oxygen concentration usually leads to hypoxic and/or anoxic conditions within the water body, with consequences for higher trophic levels. All the aforementioned effects have been well-demonstrated in a variety of coastal ecosystems (e.g. Nixon, 1995; Bricker et al., 2003; Anderson et al., 2008; Conley et al., 2009; Savage et al., 2010). Few studies, however, have been conducted on natural macronutrient enrichment, unaffected by anthropogenic influence, with a documentation of the resultant responses by primary producers. Observing the natural cycle between enrichment, primary productivity and botanical senescence in the current developed world is rare or non-existent (Halpern et al., 2008). Difficulties arise with the management of most estuaries where the current state cannot be compared to natural condition baselines. Developing countries boast some estuaries that are still in a near natural or pristine condition, with no development in the catchment and thus providing important systems for research (Lotze et al., 2006). From a water chemistry perspective, new insights on N and P cycling can lead to a better understanding of transformed systems. In South Africa, there are more than 100 micro-estuaries and micro-outlets that link small coastal rivers or streams to the sea. South Africa's National Biodiversity Assessment (Van Niekerk and Turpie, 2012) indicated that there is an urgent need to conduct research on these systems, as they are currently unprotected by legislation. Unfortunately, results obtained from a reconnaissance survey in KwaZulu-Natal indicated that 61% of the micro-estuary sites in this province were already in a poor condition, requiring intensive rehabilitation to restore them to a near natural state (Bate et al., 2017). This illustrates the urgency of obtaining formal protection for South African micro-estuaries, as the adverse conditions imposed on these small systems are most likely to accelerate as coastal development proceeds rapidly in the future. On a global basis, Bagella et al. (2016) noted that temporary aquatic environments are in great danger because they have been historically neglected and are being rapidly degraded such that they may even disappear altogether. Prior to the expansion of the anthropogenic footprint on most ecosystems, enrichment from natural processes would have had a favorable impact on living organisms within or in close proximity to such events, e.g. coastal upwelling and resuspension (Nixon, 1995; Su et al., 2015). These natural enrichment events have been linked to stimulation of phytoplankton blooms that ultimately become a food source for other marine organisms (Guinder et al., 2015; Wang et al., 2010). In the same way, it is proposed that estuaries would naturally have
experienced short-lived enrichment events that triggered high primary productivity. From the literature it can also be inferred (Winder and Cloern, 2010) that, after the primary producers respond to elevated nutrient inputs in the presence of sufficient light intensity, these plants then reach peak biomass, complete their life cycle and return to a ‘baseline state’ typical of the ecosystem. The purpose of this study was to obtain reference information on the water chemistry of selected near natural micro-estuaries and microoutlets in the Eastern Cape Province, South Africa, and to determine the effect this had on three major algal guilds, namely phytoplankton, microphytobenthos and macroalgae. We expected that natural enrichment would lead to high biomass or primary growth with no resultant adverse effects and no long-term disruption to ecosystem state. This study therefore links nutrient input to short-lived high productivity in eight small systems, all of which are in near pristine condition but may deteriorate in the future as coastal development proceeds. 2. Materials and methods 2.1. Study sites Seasonal sampling was conducted in eight systems along the warm temperate Eastern Cape coast of South Africa from July 2015 to June 2016 (Fig. 1). The rainfall along this section of coast is unpredictable, with small peaks usually occurring during the spring and autumn months. Four systems are representative of micro-estuaries (systems that have an open water surface area 0.5–3 ha, connect periodically to the sea and sometimes have a longitudinal salinity gradient), while the other four are micro-outlets (stream outlets that flow into the sea, are mostly perched systems with infrequent marine inflow, and have an open water surface area b 0.5 ha). It should be noted that, at this stage, no thorough attempt has been made to classify these systems as either micro-estuary or micro-outlet, and that the current groupings are merely chosen for ease of interpretation. The study systems all have relatively pristine catchments with the only development being relatively small cultivated areas, minor dirt roads and a few residential homes near some of the estuaries/outlets (Table 1). Some nutrient input from non-natural sources occurs in some of the catchments (e.g. Kwesani) from small-scale pastoral agriculture, but these inputs are minimal compared to largescale farming practices that impact most anthropogenically modified estuaries globally. All the systems had extensive intact riparian vegetation on the banks, which then graded into coastal dune thicket (Mucina and Rutherford, 2006). The extensive vegetation around these systems (Fig. 2) acts as a nutrient buffer further mitigating any possible nutrient loads from minor disturbances in the catchments. In a much more transformed catchment, Desbonnet et al. (1995) determined that approximately 70% of non-point source nitrogen inputs were removed by vegetated buffers of 25 m in width. Residence time was interpreted as the time it takes for any water parcel to leave a coastal water body through its outlet to the sea (Dronkers and Zimmerman, 1982). In the case of an estuary that closes to the sea for part of a year, the residence time would increase in relation to the length of the closed phase. Hence a water parcel during the closed mouth state would have a longer residence time when compared to an estuary that is permanently open to the sea. Although the residence time of water particles were not measured sensu stricto, mouth
