Drought conditions and recovery in the Coorong wetland, south Australia in 1997–2013

Estuarine, Coastal and Shelf Science 163 (2015) 175e184

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Drought conditions and recovery in the Coorong wetland, south Australia in 1997e2013 Sophie C. Leterme a, *, Laetitia Allais a, Jan Jendyk a, Deevesh A. Hemraj a, Kelly Newton a, Jim Mitchell a, Margaret Shanafield b a b

School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide 5001, Australia School of the Environment, National Centre for Groundwater Research and Training (NCGRT), Flinders University, GPO Box 2100, Adelaide 5001, Australia

a r t i c l e i n f o

a b s t r a c t

Article history: Received 15 May 2014 Accepted 8 June 2015 Available online 17 June 2015

Between 2004 and 2009, South Australia suffered its longest period of below average annual rainfall. This impacted riverine ecosystems and particularly the Murray-Darling Basin (MDB), the largest river system in Australia. The MDB combines 30,000 wetlands of which the Coorong wetland is of significant importance for the reproduction of bird and fish species, and is listed under the Ramsar Convention. We sampled water in the Coorong wetland between 2011 and 2013 and compiled additional data from 1997 to 2013 to assess the impact of the drought and subsequent recovery of the environment. The salinity levels of the Coorong wetland increased dramatically during the drought because of the lack of freshwater inflow from the Murray River. The changes in water flow observed from 2002 to 2009 had an impact on the number of habitats present along the Coorong wetland. In addition, a shift in community composition was observed between the freshwater habitat (<5) dominated by chlorophytes to the hypersaline habitat (>85) dominated by diatoms. It is evident that during the drought, the Coorong wetland was dominated by diatoms and dinoflagellates. After the drought, the North Lagoon was dominated by chlorophytes up to a salinity level of 20. However, over 20 and in the South Lagoon, diatoms dominated the community. This study highlights how salinity levels drive the phytoplankton community. Based on the complementary data obtained for salinity between 1997 and 2010, there is a significant difference between the salinity levels observed during the drought and those observed before and after the drought. It appears that salinity levels are now recovered to what they were in the late 1990s. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Murray-Darling Basin habitat salinity rainfall river flow phytoplankton

1. Introduction The two primary drivers of water composition in coastal environments are evaporative loss and freshwater inflow, both of which can affect the salinity regimes of estuaries (Corlis et al., 2003; Price et al., 2012). Evaporative loss preferentially removes isotopically light molecules, leaving the remaining water with heavier molecules and therefore saltier (Horita and Wesolowski, 1994; Luz et al., 2009). Salinity gradients and fluctuations are integral to the structure and functioning of estuarine systems (McLusky and Elliott, 2004), and locally have been shown to influence the nature of the estuarine biota (Forbes and Cyrus, 1993). Rivers are often the main source of freshwater in estuarine systems and maintain both their water level and the salinity levels. However, constant

* Corresponding author. E-mail address: sophie.leterme@flinders.edu.au (S.C. Leterme). http://dx.doi.org/10.1016/j.ecss.2015.06.009 0272-7714/© 2015 Elsevier Ltd. All rights reserved.

pressure to divert and/or drain water for human use and associated changes in hydrological regimes threatens wetlands worldwide. The timing and volume of river flows have been altered to service those uses and under drought conditions, a further decrease in the flow of those rivers would occur and gradually intensify environmental parameters (Walther and Rowley, 2013). In shallow water systems, interactions between benthic and pelagic processes are more direct and susceptible to disturbances such as wind forcing, eutrophication (Scheffer, 1998) and evaporation (Vallet-Coulomb et al., 2001) than in deeper aquatic systems. In turbid shallow waters, benthic microalgae are also found suspended in the water column as a result of mixing and can contribute to net productivity in the pelagic habitat (de Jonge and van Beusekom, 1995; MacIntyre and Cullen, 1995; Loebl et al., 2007). The effect of droughts on phytoplankton communities in estuarine systems is likely to be indirect through changes in water quality drivers, such as salinity, temperature, turbidity (Attrill and

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Power, 2000), grazing (Alpine and Cloern, 1992), and nutrient inflows (Grange et al., 2000). An interesting deviation to this pattern of river flushing through coastal wetlands is the case of the “inverse estuary”, where the evaporation exceeds the freshwater input (Pritchard, 1952; Wolanski, 1986). One example of this type of coastal system is the Coorong wetland in South Australia. The Coorong wetland is a long, narrow coastal lagoon at the mouth of Australia's largest river system, the Murray-Darling Basin (MDB). This shallow water system is connected to the sea at the mouth of the River Murray (Murray Mouth, Fig. 1) which is subject to infilling and scouring on a seasonal basis. Unlike most estuaries, freshwater input from the MDB occurs close to the estuary mouth, and is primarily drawn along through the Coorong by salinity-driven gradients in response to evaporative water loss (Webster, 2010). In particular, the River Murray flows into Lake Alexandrina, which in turn is separated from the Coorong wetland by a series of barrages constructed in the late 1930s (Lintermans, 2007, Fig. 1). The flow from Lake Alexandrina to the Coorong wetland is controlled by opening the gates of the barrages. While seasonal and inter-annual fluctuations in salinity occur in the Coorong (Lester et al., 2011), the salinity levels of the Coorong wetland have increased dramatically because of the lack of freshwater inflow from the Murray River (Nayar and Loo, 2009), resulting from the drought (2004e2009; Zampatti et al., 2010). While salinity is a widely acknowledged factor causing variability in phytoplankton communities worldwide (e.g. Brogueira et al., 2007; Yunev et al., 2007), its links with other environmental changes have barely been investigated. Ford (2007) suggested that in the Coorong, salinity increased due to climate change, reduced frequency of riverine high-flow events, modification of water regime and increased evaporation. This increase in salinity exacerbated the already significant aridity of South Australia and required long-term management plans to ensure sustainability (Brookes et al., 2009). The Coorong wetland is known to be a habitat of significant importance for the reproduction of

Fig. 1. The location of the Coorong wetlands and the 20 sites sampled by Flinders University between Goolwa and Salt Creek over the period 2007e2013.

native, as well as migratory, bird and fish species (Nayar and Loo, 2009), and is ranked within the top six waterbird sites in Australia (Paton, 2010). Therefore, Australia designated the Coorong wetland, covering approximately 140,500 ha, as a wetland of international importance under the Ramsar Convention on wetlands in 1985 (Wentworth Group, 2008). It is also designated as an ‘icon site’ under the Murray-Darling Basin Authority program “The Living Murray” (Murray-Darling Basin Commission, 2006; Phillips and Muller, 2006). Due to its significance for local and migratory wildlife, as well as its position at the terminus of Australia's largest river system, the Coorong has received significant research attention. In particular, the hydrologic regime, including the connection between salinity levels in the Coorong and flow through the barrages that connect it to freshwater inflows from the MDB, has been well-studied. Recent studies show that since the 1960s, the Coorong wetland hydrology has experienced significant salinization, as freshwater from the MDB has been increasingly diverted for domestic and agricultural use, and the groundwater inputs have diminished due to extensive construction of drains throughout the region (Gell and Haynes, 2005). The salinity in the North Lagoon (and therefore also the South Lagoon, which draws on water from the North to replace evaporative losses) is negatively correlated with discharges from the barrages that separate it from MDB flows (Kingsford et al., 2011). However, at the same time, the higher flows result in increased channel scouring, causing the fresher waters to be removed from the Coorong more quickly. Higher flows also raise the level of the lagoons, promoting mixing between the North and South Lagoons (Webster, 2010). Sediment cores taken from the lagoons also show that this rise in salinity is responsible for a major, long-term shift in primary production and organic matter within the Coorong (Tulipani et al., 2014). Nutrient concentrations, especially in the South Lagoon, have also been affected by the changes in the hydrologic regime, with nitrogen and orthophosphate concentrations nearly doubling by 2006 as compared to background levels (Lester and Fairweather, 2009). Between 2004 and 2009, South Australia suffered its longest period of below-average annual rainfall since 1900. Riverine ecosystems were severely impacted by this “millennium drought”, particularly the Murray-Darling Basin (MDB). Reduced river flows throughout the MDB and the associated closure of the Murray Mouth during drought conditions threatened the ecological function of the Coorong wetland through the tendency for higher salinities in the system, modification of the water level regime and the obstruction of fish migration pathways (Brookes et al., 2009). While the long-term history of ecosystem change in the Coorong is now well-documented, and the relationship between barrage discharge and lagoon salinity is well established, the Coorong ecosystem's resilience to drought is still unclear. Although higher flows have been observed in the MDB since 2010, there has been little analysis to determine post-drought changes in the Coorong system to date. Because they form the base of the food chain, trends in primary production provide a good indicator of ecosystem resilience. Increases in salinity typically result in increased microbial abundance and decreased species diversity, and thus altered
s-Alio
et al., 2000; microbial processes in aquatic systems (Pedro Ayadi et al., 2004; Estrada et al., 2004). Fluctuations in salinity toward hypersalinity can result in alteration to species succession and salinity has been identified as a major selective pressure in primary producer communities (Estrada et al., 2004). This is particularly relevant to hypersaline systems such as the Coorong wetland that sustain the reproduction of native bird and fish species, as well as migratory bird species, because environmental/metabolic changes at the level of primary producers are known to propagate along the

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food chain to estuarine apex-predators such as fish and birds. Therefore, we hypothesise the lack of freshwater inflow from the Murray River during the drought impacted (1) the salinity levels, (2) the number of habitats and (3) the community composition of large (>5 mm) phytoplankton species in the Coorong wetland. To test this hypothesis, data from the period preceding, during and after the most recent drought period (i.e. 2004e2009) have been analysed. 2. Material and methods 2.1. Study area The Coorong wetland is a shallow coastal lagoon exceeding 140 km in length and is characterised by a strong salinity gradient ranging from ca. 0 (freshwater), in the north of the wetland to more than 190 near Salt Creek in the southernmost reaches (Fig. 1). The maximum depth of the Coorong is 1.7 m and water levels undergo a seasonal cycle of up to approximately 0.7 m in range with higher levels occurring in late winter to early spring and lower levels occurring in late summer to early autumn (Webster, 2005). This lagoon, parallel to the coast, is separated from the open ocean by a network of peninsular dunes (Webster et al., 2004) except at the Murray Mouth, where the Southern Ocean, River Murray and Coorong wetland meet. Depending on drought conditions, the mouth of the Murray can be seasonally opened or closed. Under normal circumstances, the mouth is closed approximately 1% of the time, while this increases to as much as 40% during years of drought (Brookes et al., 2009). The Coorong is divided into the Northern and Southern lagoons by a narrow constriction at Parnka Point (S15; Fig. 1). Infrequent freshwater releases through the barrages have led to decreased salinities in the Northwest part of the Coorong wetland, whereas excess evaporation over precipitation, coupled with minimal freshwater discharge from creeks in the South Lagoon increases salinity along its NortheSouth axis (Nayar and Loo, 2009). 2.2. Water sampling Samples were collected at 20 locations along the Coorong wetland, from the fresh to brackish waters near Goolwa (0e28) to the hypersaline waters near Salt Creek (~80e190, Fig. 1). Sampling was conducted between August 2011 and August 2013. At each sampling site, measurements and water sample collection was performed within the water column at a depth of 20e30 cm below the surface. The total water depth never exceeded 120 cm. Temperature (
C), salinity (Practical Salinity Scale), turbidity (NTU) and dissolved oxygen concentrations (DO, mg l1) were recorded using a TPS 90FL-T multi-parameter probe (TPS Pty Ltd, Brisbane, Australia). 2.3. Nutrients Dissolved inorganic nutrient concentrations (i.e., silica [Si], ammonia [NH3], orthophosphate [PO4] and nitrate/nitrite [NOx]) were determined using a Lachat Quickchem Flow Injection Analyser (FIA) following published methods (Hansen and Koroleff, 2007). For the analysis, 100 mL of water were filtered in triplicate through bonnet syringe Minisart filters (0.45 mm pore size, Sartorius Stedim, Dandenong, Australia) to remove large particles. Filtrates were then stored at 20
C until analysis. Prior to analysis, the samples were thawed and mixed before injecting approximately 10 mL of each sample into the FIA in duplicate for a total of 6 replicates per sample. The detection limits were 40 nM for dissolved Si species, 70 nM for NH3, 30 nM for PO4 and 70 nM

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for NOx. The method was calibrated using standard solutions prepared in 0.6 M sodium chloride, corresponding to typical seawater. 2.4. Phytoplankton Water samples (600 mL) for chlorophyll a (Chl a) extraction were filtered through 1.2 mm glass-fibre filters (Whatman GF/F) and immediately deep frozen in liquid nitrogen until analysis. Chlorophyllous pigments were then extracted in 5 mL of methanol in the dark at 4
C over 24 h, and concentrations of Chl a (mg L1) were determined following Strickland and Parson (1972) using a Turner 450 fluorometer. Chl a was used as a proxy for phytoplankton biomass. Plankton samples were obtained by collecting triplicates of water samples (500 mL) from each of the 20 sites sampled along the Coorong wetland (Fig. 1). The water samples were fixed with Lugol's iodine (5% final concentration) in order to preserve the structure of the organisms' chloroplast and subsequently identified and enumerated by Microalgal Services (Ormond, Victoria). Samples were filtered through 5 mm pore size Sterlitech mixed cellulose ester membranes (Sterlitech, Kent, USA). The cells on the filters were resuspended in a smaller volume of filtrate from the same sample. 1 mL of this suspension was then pipetted into a Sedgewick Rafter and counted using a Zeiss Axiolab upright microscope equipped with bright-field and phase contrast optics (Carl Zeiss Microscopy, Thornwood, USA). Cells were identified to the genus, or species, level based on their key taxonomic features (Tomas, 1997; Hallegraef et al., 2010). 2.5. Other datasets Data on river flow volume for the period from December 1994 to October 2013 are included in the study. River Murray flow reports, based on continuous depth measurements, for the South Australian portion of the Murray River were retrieved from WaterConnect (www.waterconnect.sa.gov.au). Barrage flow data were obtained from the Department of Environment, Water and Natural Resources (DEWNR). Complementary data for water quality, wind stress, chlorophyll a and phytoplankton species measured in the Coorong wetland between 1997 and 2013 were gathered from the literature (Geddes and Tanner, 2007; Bevan et al., 2009; Brookes et al., 2009; Schapira et al., 2009; Leterme et al., 2010; Webster, 2010; Dittmann et al., 2011; Jendyk et al., 2014). 2.6. Habitats and states of the ecosystem The available datasets were grouped into five different habitats based on salinity levels within the lagoons following Schapira et al. (2009) and Jendyk et al. (2014). Habitat 1 (H1) represents freshwater areas with salinities lower than 5. Habitat 2 (H2) is brackish with salinities ranging from 5 to 20. Habitat 3 (H3) is designated as high-brackish to marine with a salinity range of 21e40. Habitat 4 (H4) is characterised by salinities higher than ambient seawater with salinities ranging from 41 to 84. Habitat 5 (H5) is represented by hypersaline conditions equal to or greater than 85. Different states of the Coorong ecosystem have been described by Lester and Fairweather (2009). Habitats H1 and H2 were not described in their study as they were not observed in the Coorong wetlands during the timeframe of their study (i.e. 1999e2007). Habitat H3 corresponds to the ecosystem state ‘Estuarine/Marine’ with low salinity (<41.5 PSU), low total Kjeldahl nitrogen, low total orthophosphate and low turbidity. Habitat H4 regroups the three described states for the ‘Marine’

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category with salinity (41.5e85 PSU), very low total Kjeldahl nitrogen, very low total phosphate and low turbidity. Finally, H5 regroups the 4 states of the ‘Hypersaline’ category with salinity (85 to >151.4 PSU), high to very high total Kjeldahl nitrogen, moderate to very high total orthophosphate and moderate to very high turbidity.

2.7. Statistical analyses To assess species diversity, Margalef's community diversity index was computed following the formula for each habitat:

Da ¼ S  1=log N where S is the number of species present in a sample and N is the total number of individuals encountered (Margalef, 1968). In addition, a species accumulation curve was computed based on the data from each habitat, following Drozd and Novotny (2010):

Cðn; kÞ ¼

n k

¼

n! k!ðn  kÞ!

where k is the number of samples used within a data-subset and n is the total number of samples included in the dataset. Data collected were found not to be normally distributed after applying a KolmogoroveSmirnov test. To test for significant differences between means of parameters, nonparametric, two independent samples (Mann Whitney U) and Spearman rank correlation coefficients (r) were calculated (Zar, 1996). The analyses were performed using the SYSTAT 13 package (http://www.systat. com). A two-way crossed (factors: habitat and period) SIMPER (Similarity Percentages e species contributions) analysis was performed to reveal which genera are responsible for the multivariate community patterns within and between habitats and drought conditions (PRIMER-E Ltd., Plymouth, UK). Unconstrained multivariate analysis of the phytoplankton community was performed using principal coordinates analysis (PCO) to investigate differences in the community over the period 2004e2013. Phytoplankton group biomasses were log(xþ1) transformed before the calculation of the BrayeCurtis resemblance. The significance of the relation between single genera (plotted as supplementary variables) and the PCO axes was tested using Spearman rank correlations to identify which genera or group of genera was responsible for the differences observed. We adopted a probability threshold of p < 0.05 for all analyses, unless stated otherwise. In order to evaluate the importance of each environmental variable in the distribution of phytoplankton communities over the study period, distance-based redundancy analyses (dbRDA) were conducted. The analysis was performed on the period 2007e2013 only as not enough complementary environmental data were available for 2004 and 2005. The BEST procedure was used to identify the best match between multivariate among-sample patterns and environmental variables associated with these samples. The procedure BVSTEP within BEST searches for high rank correlations between a similarity matrix and matrices generated from different normalised variable subsets (Clarke and Gorley, 2006). The dbRDA is a routine for the ordination of principle coordinates based on multivariate regression. Vectors for environmental factors which best describe the variations observed in phytoplankton community composition (based on the BVSTEP procedure) are displayed on the dbRDA plot. For the ordination of data, PRIMER (v6) and PERMANOVA Aþ for PRIMER were used.

3. Results 3.1. Climatic conditions Changes in water temperature and salinity along the 20 sites of the Coorong wetland during the drought (February 2007 and May 2009) and after the drought (February and May 2012 and 2013) are shown in Fig. 2. Water temperatures appeared to be on average higher by ~3.25
C during the drought. In addition, salinity levels were significantly higher during the drought period (p ¼ 0.033; Fig. 2). Based on the complementary data obtained for salinity between 1997 and 2010 along the Coorong wetland (Geddes and Tanner, 2007; Brookes et al., 2009; Webster, 2010; Dittmann et al., 2011), there is a significant difference between the salinity levels observed during the drought (2002e2009) and the ones observed before (1997e2001) and after the drought (2010e2013; p ¼ 0.002; Fig. 3). It then seems that the salinity levels are now recovered and, especially in the north Lagoon, much lower than they were even before the drought period. Webster (2010) showed a strong connection between flow through the barrages and Coorong salinity for a period up to 2008. Flow through the barrages

Fig. 2. Fluctuations of temperature (A) and salinity (B) along the Coorong wetlands during the drought [i.e., February 2007 (open circles) and May 2009 (open diamonds)] and after the drought [i.e., February 2012 and 2013 (black circles) and in May 2012 and 2013 (black diamonds)].

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Fig. 3. Fluctuations of salinity along the Coorong wetlands before the drought [i.e., June 1997 to September 2003 (black triangles) from the literature], during the drought [i.e., December 2004 to February 2010 by the authors (open circles) and from the literature (open triangles)] and after the drought [i.e., February 2012 to August 2013 (black circles)]. Data not sampled by the authors were gathered from the literature (Geddes and Tanner, 2007; Brookes et al., 2009; Webster, 2010; Dittmann et al., 2011).

is often seasonal, with peak releases typically occurring in late winter and decreasing into the dry summer months. Three distinct patterns of releases can be observed in the recent data, with low releases before the drought, little to no water released during the drought, and typically higher releases post-drought (MDBA modelled flow releases). Averages over these periods were 180 GL before the drought (1997e2001), only 15 GL during the drought (2002e2009) with 0 GL released during 2002 and 2007e2009, and over 581 GL after the drought (2010e2013). The river flow also showed three distinct patterns (Fig. 4), with a high river flow (9.83 ± 7.79  103 ML day1) between December 1994 and August 1996, a low river flow (3.13 ± 1.86  103 ML day1) between January 2002 and December 2009 and a high river flow afterwards (13.66 ± 8.24  103 ML day1). Salinity was negatively correlated with the flow volume from the barrage in the North Lagoon (Spearman's correlation r ¼ 0.534, n ¼ 34, p < 0.001) and in the South Lagoon (Spearman's correlation r ¼ 0.543, n ¼ 34, p < 0.001).

Fig. 4. (A) Fluctuations of salinity in the North (black bars) and South (grey bars) lagoons of the Coorong wetlands and of the flow of the River Murray (dotted line) between December 1994 and August 2013. Data not sampled by the authors were gathered from the literature (Geddes and Tanner, 2007; Brookes et al., 2009; Webster, 2010; Dittmann et al., 2011). (B) Fluctuations of total flow through the barrages along the Coorong wetlands between December 1994 and August 2013. Data were provided by DEWNR.

3.2. Habitats and state of the ecosystem Changes in water flows observed from 2002 to 2009 (Fig. 4) would have had an impact on the habitats present along the Coorong wetland. When considering the distribution of habitats, i.e. from freshwater (H1) to hypersaline (H5), as a function of distance from the Murray Mouth (Fig. 5), a clear temporal pattern becomes apparent. The absence of the freshwater habitat (H1) in the data available between 1997 and 2010 was evident. The freshwater habitat only appeared in the Coorong wetland in the winter of 2011, when rainfall once more noticeably increased compared to years of drought (Fig. 4A), especially in the North Lagoon, and lowered average salinity significantly. However, the brackish habitat (H2) occurred largely in the northernmost 15 km of the Coorong wetland between June 1997 and September 2003. After this date, salinities in the North Lagoon rarely fell below 21 until August 2011. During the years preceding the drought, the high brackish habitat (H3) was mostly recorded between 20 and 40 km from the mouth, while the

Fig. 5. Percentage of observation of each saline habitats i.e. H1: freshwater (<5), H2: brackish (5e20), H3: high brackish to marine (21e40), H4: high salinity (41e84) and H5: hypersaline (>85) over the Coorong wetland [from the Murray Mouth (0 km) to Salt Creek (100 km)] for the period June 1997 to August 2013. Only sampled months are represented.

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drought-impacted years show a marked shift toward high brackish habitat areas throughout the first 20 km of the North Lagoon. In the years following the drought, the high brackish habitat only occurred in the southern reaches of the North Lagoon (e.g., 35e50 km from Murray Mouth). A comparable pattern is evident for the high salinity habitat (H4). A significant increase was observed along the Coorong wetland from the Murray Mouth to Salt Creek for turbidity (Spearman's correlation r ¼ 0.301, n ¼ 160, p < 0.05), NH3 (Spearman's correlation r ¼ 0.415, n ¼ 238, p < 0.05), NOx (Spearman's correlation r ¼ 0.155, n ¼ 232, p < 0.05) and Si (Spearman's correlation r ¼ 0.549, n ¼ 199, p < 0.05). However, PO4 did not show any significant changes along the Coorong wetland (Fig. 6). 3.3. Phytoplankton A significant increase in phytoplankton biomass (i.e. using Chl a as a proxy) was observed along the salinity gradient (Fig. 7) during the drought (Spearman's correlation r ¼ 0.580, n ¼ 52, p < 0.05)

and afterwards (2011e2013; Spearman's correlation r ¼ 0.644, n ¼ 193, p < 0.05). However, during drought conditions in the South Lagoon, at salinity levels >107, the Chl a values decreased after reaching a maximum value >9 mg L1. A dataset of 349 phytoplankton samples taken along the Coorong wetland, combining our data and data from the literature, was analysed for each type of saline habitat, from freshwater (<5, H1) to hypersaline (>85, H5). It is evident that with the decrease of salinity observed after the drought, a shift was observed in the composition of phytoplankton communities (Fig. 8). In particular, while diatoms and dinoflagellates dominated the Coorong wetland during the drought, the ecosystem was dominated by chlorophytes at salinities< 20 and by diatoms at salinities >20. The percentage of total variation inherent in the resemblance matrix is explained by the first two axes of the PCO plot and equals 48.3% (Fig. 9). The plot shows a clear separation of samples obtained ‘during the drought’ vs ‘after the drought’ period on the basis of the BrayeCurtis measure. The main species associated with those periods are indicated as vectors on the PCO plot. In particular,

Fig. 6. Fluctuations of nutrients (AeD) and turbidity (E) along the Coorong wetlands during the drought [i.e., February 2007 (open circles) and May 2009 (open diamonds)] and after the drought [i.e., AugusteDecember 2011 (grey triangles), 2012 (black diamonds) and FebruaryeAugust 2013 (black circles)].

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Fig. 7. Fluctuations of Chlorophyll a (Chla) along the Coorong wetlands during the drought [i.e., February 2007 (open circles) and May 2009 (open diamonds)] and after the drought [i.e., AugusteDecember 2011 (grey triangles), 2012 (black diamonds) and FebruaryeAugust 2013 (black circles)].

Fig. 9. Principal Coordinated Ordination (PCO) of the phytoplankton communities assessed between 2004 and 2013. The ordinations are based on the BrayeCurtis similarity index and the projected vectors denote the species with a correlation >0.4 with any of the two first ordination axes.

dinoflagellates such as Gymnodinium sp., Amphidinium sp., Gyrodinium sp. and Prorocentrum sp. have a strong negative relationship with PCO1 (indicative of ‘during the drought’) while Gymnodinoid sp. (dinoflagellate), Crucigenia sp. (Chlorophyte) and Cyclotella sp. (diatom) have a fairly strong positive relationship with PCO1 (indicative of ‘after the drought’). In addition, Tryblionella sp. (diatom) is correlated to PCO2 which separate the ‘during the drought’ years from each other. The SIMPER procedure (results not shown) also showed that the abundance variability of these species was most responsible for splitting the years into the three cluster groupings. The BVSTEP procedure identified the preferred minimum set of environmental predictors. The preferred set included the variables salinity, temperature, pH and wind stress, with a correlation of 0.279 (p < 0.01). All variables identified in the BEST procedure are displayed as vectors in a plot of the dbRDA analysis (Fig. 10). Salinity and temperature appear to be correlated with the first dbRDA axis. The variation in the second dbRDA axis seems to be related to the other variables; Chl a, PO4, NH3 and NOx. 4. Discussion 4.1. Climatic conditions

Fig. 8. Contribution of phytoplankton groups along the Coorong wetland during the drought (i.e., February 2007 and May 2009) and after the drought (i.e., August 2011e2013). Salinity is represented by the dotted line.

Here, we showed that temperature and salinity levels increased during the drought. Droughts are commonly associated with higher temperatures combined with dryness, which contributes to increased heat stress in ecosystems (McCabe et al., 2014). Heat stress mainly affects fish species. which become prone to heavy infestation from parasites (Lintermans, 2007) that can ultimately cause death. In the Coorong wetland, a reduction in fish diversity and abundance during the drought was reported by Zampatti et al. (2010). In addition, salinity concentrations in estuaries and coastal lakes are highly variable, both spatially and temporally, and reflect relative inputs from watersheds and tidal water intrusion,

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Fig. 10. Distance-based redundancy analysis (dbRDA) of the phytoplankton communities assessed between 2007 and 2013 and fitted environmental variables with their vector (strength and direction of effect of the variable on the ordination plot). Axis legends include % of total variation explained by the axis. Chl a: chlorophyll a, NH3: ammonia, PO4: orthophosphate and NOx: nitrate/nitrite.

circulation patterns and vertical, as well as horizontal mixing processes, precipitation and terrigenous run-off (Redden and Rukminasari, 2008). Typically, the Coorong wetland has a strong salinity gradient along its length from the Murray Mouth to Salt Creek (Fig. 1). When the barrages allow water flow from the River Murray and the Lakes, water can be near fresh at the Murray Mouth; however, when they are not flowing, salinity similar to that of seawater prevails in that area. As the Coorong stretches south-east towards the South Lagoon, salinity increases steadily due to evaporation, resulting in salinities considerably above that of seawater in the South Lagoon. During the drought, with no flow of freshwater across the barrages from the Murray River and between the Lower Lakes (Fig. 1), salinity rose to levels of 180e200 at Salt Creek during summer. In particular, the salinity levels in the South Lagoon (i.e. 56e100 km from the Murray Mouth) exceeded the maximum levels tolerated by the plants, fishes and birds that underpin the international status of these wetlands as stated in the Ramsar convention (Wentworth Group, 2008). This was exacerbated by the restricted water exchange between the South and North Lagoons at Parnka Point (S15, located at 56 km) and the mixing of water past that point (Lamontagne et al., 2004). The flow regimes observed here varied with the drought conditions and as the river flow decreased, the flow through the barrages decreased too. In particular, salinity decreased with the increase of flow through both the river and the barrages. Due to the low river flow and the location of those observations, salinity changes could have also been associated to water intrusion from the South Lagoon by lateral water exchange. Flow regime is often the major driver of river ecosystem structure and processes (Ward et al., 1999), and therefore its fluctuation alters the ecological character of the river. 4.2. Habitats and state of the ecosystem Species often rely on specific habitats, have specific diets and can be very vulnerable to the effects of water flows due to changes in water quality (e.g., salinity), connectivity and habitat (Lucas and Baras, 2001). Between 1997 and 2003, the Coorong wetland was characterised by high salinity habitats in the southern reaches of the North Lagoon, as well as the northern reaches of the South Lagoon. However, between 2003 and 2010, a marked northward

shift of high salinity habitats was observed, reaching as far north as the Murray Mouth (e.g., Fig. 5, February 2010). In addition, there was no flow through the barrages or from the river into the Coorong during that period. During the ‘post drought’ years (2011e2013), on the other hand, high salinity habitats were once again observed toward the southern end of the Coorong wetland, largely appearing at distances greater than 55 km from the Murray Mouth. Significantly, hypersaline habitats (H5) only appear in the years before the drought as well as during the drought. Before the drought, hypersaline habitats largely occurred 75 km south of the Murray Mouth, while hypersaline habitats were evident as far north as 40 km from the mouth during years of drought. Freshwater (H1, <5) as well as marine habitats (H3, 21e40) are known as relatively stable ecosystems (Remmert, 1969), allowing for long evolutionary histories of the organisms which fill the niches within these habitats (Telesh et al., 2013). However, a biodiversity gap would be expected in between the freshwater and marine ranges of the Coorong wetland i.e., in the brackish environment (H2, 5e20). This gap would be expected to be filled with the most highly adaptable organisms that have a broad range of salinity tolerance (Telesh et al., 2009; Mironova et al., 2012, 2013). In the high salinity (H4, 41e84) and hypersaline habitat (H5, >85) changes would be expected in the basic trophic relations as zooplankton would progressively disappear with increasing salinity (Hemraj, 2013). Fish would also disappear with increases in salinity (Kumar et al., 2009). When salinity reached more than 150 g/L in the South Lagoon, estuarine conditions disappeared completely (Kingsford et al., 2011). The South Lagoon then reached a degraded hypersaline state. This ‘Degraded Hypersaline’ state was described by Lester and Fairweather (2009) as occurring when there had been no freshwater flow from the River Murray to the Coorong for a period of 339 days. Such an event would have been likely less than 1% of the time in the absence of water-resources development in the Basin, and the documented hydrologic and ecological impacts of such dry conditions were severe (Bark et al., 2013).

4.3. Phytoplankton Phytoplankton biomass increased along the salinity gradient of the Coorong wetland. However, at salinity levels >107 the Chl a levels started to decrease. This suggests a salinity threshold above which the Chl a and abundance of phytoplankton cells decrease. Previous studies on seagrass Halodule uninervis (Forssk.) Aschers. have shown that photosynthetic pigments (i.e. Chl a, Chl b, total Chl and carotenoids) are significantly reduced when water salinity increases to a level >50 (Kalafallah et al., 2013). In particular, salinity fluctuations can alter important plant biochemical and physiological processes, which in turn can influence plant metabolism, growth, development, and reproduction (Vermaat et al., 2000; Torquemada et al., 2005). The same impact could also be observed in phytoplankton and might explain the decrease in Chl a values at salinity levels >107. Fluctuating salinity is one of the major natural stress factors for aquatic life in coastal waters of seas, estuaries, other brackish environments and hyperhaline water bodies (Telesh et al., 2013). It is evident here that the habitats described above dictate the presence of specific communities and dominant groups along the Coorong wetland. Here, we showed that chlorophytes dominated phytoplankton communities at H1 (i.e., <5), while diatoms were the prevalent group throughout the more saline habitats, H4 and H5 (i.e., >40). Between 5 and 40, no specific group dominated more that 50% of the community but two different communities were observed, characterising habitats H2 (5e20) and H3 (21e40).

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It may not be that those communities tolerate a wider range of salinity, but it shows the community variability in these habitats in contrast to the more group-dominated H1, H4 and H5. It is evident that during the drought, the Coorong wetland was dominated by two groups: diatoms and dinoflagellates as salinity levels ranged between 30 and 175. However, after the drought, the North Lagoon was dominated by chlorophytes at salinity levels up to 20 and by diatoms at salinities higher than 20 and in the South Lagoon. The increase in the abundance of diatoms towards the South Lagoon was also noted by Haynes et al. (2011) who described a marked northesouth diatom species gradient during their survey in 2007, with salinity explaining the greatest amount of variance observed in the diatom data. Changes in salinity, chemical and physical conditions, as well as nutrient input and grazing pressure strongly affect the diversity, community structure and temporal dynamics of phytoplankton (Winder and Sommer, 2012). Here we showed that phytoplankton species differed between ‘during the drought’ vs ‘after the drought’ periods. These differences were mainly driven by species of dinoflagellates. In addition, a set of environmental predictors explaining the differences observed was determined and showed that salinity and temperature were the main environmental factors impacting on the community composition. Leterme et al. (2010, 2013) showed that salinity fluctuations also impacted the morphology of diatom species by altering their nanostructure. Here, it is clear that the changes in salinity of the Coorong wetland affect the community composition of phytoplankton. Phytoplankton, which constitutes the base of aquatic food webs, as well as their consumers, are vulnerable to environmental alterations and climate change and changes in phytoplankton composition can cause serious repercussions for the entire ecosystem (Winder and Sommer, 2012). Changes in the dominant group of phytoplankton can indeed modify entirely the trophic system and such changes will propagate up the food chain, influencing higher levels such as zooplankton and fish (Leterme et al., 2013). For example, Wedderburn et al. (2012) showed that with the increase of salinity, diadromous and threatened fish species declined in the Coorong wetland. 5. Conclusions Wetlands worldwide are threatened by changes in hydrological regimes as the freshwaters that flush them are increasingly diverted for human uses. The Coorong wetland in South Australia is a good example of this environmental challenge. Several billion dollars have already been spent on mitigating the human and ecological effects of the degraded Coorong habitat; however, it remains unclear as to whether these efforts will be successful (Kingsford et al., 2011; Bark et al., 2013). The key to a healthy Coorong wetland ecosystem lies in its primary producers, which form the base of the food chain. Our paper highlights the changes in water quality that have been related to drought conditions in the MDB and shows that drought recovery of the primary producers is possible when salinity returns to environmental standards for the Coorong wetland. It is evident in this paper that since 2011, the salinity levels of the Coorong wetland have lowered and that this is linked to the increased flow from the River Murray. However, climate change predictions for Australia suggest that over the long-term, warmer and increasingly arid conditions can be expected (Mpelasoka et al., 2008). With approximately 70% of average natural discharge from the MDB being diverted for agricultural uses, impacts on wetland systems are unavoidable. For the MDB, van Dijk et al. (2013) estimated that regulation of the river almost doubled the reduction in flow during the 2004e2009 drought, compared to the reduction that would have occurred

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under natural conditions. However, the modelling scenarios of Lester et al. (2011) indicated that even moderate supplemental flows from the MDB to the Coorong will help to prevent further degradation of the Coorong system. While several studies debate the effectiveness of Australian management approaches to this economically and environmentally important river system (Bond et al., 2008; LeBlanc et al., 2010), for now the viability of the Coorong ecosystem will depend on the success of the 2012 MDB plan's ability to adequately protect its water dependent ecosystems despite these withdrawals, especially during future drought periods. Acknowledgements Funding was supported under Australian Research Council's Discovery Project funding scheme (DP0666420 and DP110101679). We would like to acknowledge the Department of Environment, Water and National Resources (DEWNR) for giving us access to the Coorong National Park. We also thank E. Bevan, M. Couraudon
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