Research papers

Environmental variability and phytoplankton dynamicsin a South Australian inverse estuary

Jan Jendyk a,n, Deevesh A. Hemraj a, Melissa H. Brown a, Amanda V. Ellis b, SophieC. Leterme a,nn

a School of Biological Sciences, Faculty of Science and Engineering, Flinders University, GPO Box 2100, Adelaide 5001, Australiab Flinders Centre for Nanoscale Science and Technology, School of Chemical and Physical Sciences, Faculty of Science and Engineering, Flinders University,GPO Box 2100, Adelaide 5001, Australia

a r t i c l e i n f o

Article history:Received 6 February 2014Received in revised form15 May 2014Accepted 29 August 2014Available online 16 September 2014

Keywords:CoorongSalinityDiatomsChlorophytesCryptophytesDinoflagellates

a b s t r a c t

Estuaries are widely viewed as hotspots of primary productivity. The Coorong in South Australia is aninverse estuary divided into two lagoons, extremely important to the associated riverine, lacustrine andmarine environments and characterized by a steep, lateral salinity gradient. Here, we analyzed theabundance and distribution of primary producers over two years (August 2011–2013) and investigatedthe biogeochemical factors driving observed changes. The phytoplankton community was numericallydominated by chlorophytes in the North Lagoon with Chlorohormidium sp. and Oocystis sp. being themost abundant species. In the South Lagoon, diatoms dominated the community, with Cylindrothecaclosterium, Cyclotella sp. and Cocconeis sp. being the most prevalent species. Finally, cryptophytes anddinoflagellates were found to be present throughout both lagoons but in comparatively much lowerabundances. Salinity was the most important driver of phytoplankton communities and ranged from0.15 to 72.13 PSU between August 2011 and August 2013. Chlorophytes were found to be most prolific infreshwater areas and abundances rapidly declined laterally along the Coorong. Beyond a salinitythreshold of 28 PSU, extremely limited numbers of Crucigenia sp. and Oocystis sp. were observed, butabundance were seven to ten-fold lower than in less saline waters. The salinity of the North Lagoon wasfound to be directly controlled by the flow volume of the River Murray, however, no effect of river flowon the South Lagoon was evident. Our findings suggest that management plans for the Coorong need tobe put into place which can regulate salinity regimes via river flow, even during periods of drought. Thisis highly important in order to maintain low enough salinities throughout the North Lagoon, ensuring acontinued healthy ecosystem state.

& 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Estuaries are defined as bodies of water marking the interfacebetween one or more rivers and the open ocean. They aregenerally influenced by tidal forcing and, in the case of inverseestuaries, often exhibit pronounced spatial salinity gradients(Corlis et al., 2003; Cyrus and Blaber, 1992). In addition to beingof significant economic value, estuaries are highly productiveecosystems, acting as breeding grounds for birds or nurseries formarine, brackish and riverine/lacustrine fish species (Lamontage etal., 2004). Fueled by the influx of nutrients from the sea, rivers and

terrigenous compounds, they also often constitute biological hot-spots of primary productivity (Cloern, 1987; Millie et al., 2004).

In Australia, the Murray-Darling Basin (MDB) represents thelargest river system and is shared by five states/territories. Rankedfifteenth in the world in terms of length (3780 km) and twentiethfor area (covering 1,056,000 km2), it drains an estimated 14% ofthe Australian landmass (Lintermans, 2007) and supplies approxi-mately 2 million people with freshwater. Nearly 30,000 wetlandshave been described in the MDB, most of these wetlands beingrecognized as important for feeding and breeding of waterbirdsand native fish. In particular, the Coorong (South Australia) isrecognized as a habitat of significant importance to endemicwildlife, including birds and fish (Fig. 1; Leterme et al., 2010;Nayar and Loo, 2009). It is characterized by strong salinityfluctuations which become extremely pronounced during recur-ring periods of drought (e.g., between 2004 and 2010) (Leterme etal., 2012; Zampatti et al., 2010). Persistent spatial salinity

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Continental Shelf Research

http://dx.doi.org/10.1016/j.csr.2014.08.0090278-4343/& 2014 Elsevier Ltd. All rights reserved.

n Corresponding author. Tel.: þ61 8201 2215.nn Corresponding author. Tel.: þ61 8201 3774.E-mail addresses: Jan.jendyk@flinders.edu.au (J. Jendyk),

Sophie.leterme@flinders.edu.au (S.C. Leterme).

Continental Shelf Research 91 (2014) 134–144

gradients, ranging from riverine conditions to hyper-saline condi-tions well in excess of 150 Practical Salinity Units (PSU) at thefurthest point from the ocean during drought periods havepreviously been recorded (Leterme et al., 2010).

The Coorong is connected to the sea at the mouth of the RiverMurray which flows into Lake Alexandrina, which in turn isseparated from the Coorong wetland by a series of barragesconstructed in the late 1930s (Lintermans, 2007; Fig. 1). Recurringdrought conditions throughout South Australia had prompted theconstruction of the barrages to retain water levels and to protectthe Lower Lakes (Lake Alexandria and Lake Albert; Fig. 1) fromseawater intrusion (Nayar and Loo, 2009). These barrages, how-ever, also limit the influx of fresh water into the Coorong, furthercontributing to increasing salinity levels, especially during sum-mer or drought periods. Therefore, the Coorong, like manytemporarily open/closed estuaries, is largely unaffected by littoraltidal regimes during dry periods. Instead, the mixing of the watercolumn and exchanges between deeper and shallow sections ofthe estuary are exclusively driven by wind stress and riverine/lacustrine influx (Thomas et al., 2005; Webster, 2007). In yearsduring which drought conditions are not met, water is irregularlyflushed through the barrages into the Coorong, further adding tothe variability of salinity and other environmental parameters(Nayar and Loo, 2009).

In inverse estuaries, where annual evaporation exceeds freshwater input, strong spatial salinity gradients can be observed(Corlis et al., 2003). These gradients result in the formation of arange of micro-habitats, exhibiting distinct environmental

conditions and unique biota composition (Turner et al., 1979).Due to their fundamental importance as the base of aquatictrophic webs and typical rapid response to environmental change,phytoplanktonic organisms are widely used as indicators ofecosystem health (Smol and Stoermer, 2010). Driven by seasonallychanging environmental conditions, recurring multi-specificblooms of brackish dinoflagellates and centric diatoms havepreviously been characterized and studied extensively in estuaries(Orive et al., 1998; Smayda, 2008). Environmental changes cangenerate alterations in morphology, as well as shifts in abundance,distribution and biodiversity (Flöder et al., 2010; Leterme et al.,2010; Piehler et al., 2002). However, information is still lacking onthe impact of salinity gradients on the dynamics of primaryproducer communities in inverse estuaries.

Monthly samples were collected over a two year samplingperiod (between August 2011 and August 2013) to investigate (i)temporal and spatial changes in the biochemical properties of theestuary and (ii) the effect fluctuations in these properties have onthe abundance, diversity and distribution of the phytoplanktoncommunity along the Coorong wetland. This study was performedto establish the background knowledge on primary producers inthe Coorong and how changes in environmental conditions affectthem to provide a tool for future management of the estuary.

2. Materials and methods

2.1. The Coorong wetlands

The Coorong is an inverse estuary located 70 km south ofAdelaide, South Australia (Fig. 1) and is recognized as a habitatof significant importance to native and migratory fish and birdspecies (Nayar and Loo, 2009). It stretches approximately 170 kmin length along the coast between Goolwa and Salt Creek, butremains protected from the Southern Ocean by a barrier ofestablished foredunes. Its only connection to the ocean is locatedwhere the Coorong, the River Murray and Encounter Bay/theSouthern Ocean meet at the Murray Mouth and it is divided intotwo lagoons (North and South) at Parnka Point (Fig. 1).

2.2. Sampling design

Monthly samples were taken along the Coorong at five sites(Sites 1 to 5, Fig. 1) between August 2011 and August 2013. Threesites were located in the North Lagoon and two sites in the SouthLagoon. In order to assess environmental variability and its effectson phytoplankton communities, a range of parameters weremeasured in the sub-surface waters at each site, in 70–100 cmof water.

2.2.1. Hydrological and physical parametersSalinity (PSU), pH, and water temperature (1C) were measured

using an AquaRead multi-parameter probe. The monthly river flowdata (volume) of the Murray River were retrieved from Water-Connect (WaterConnect, 2014). The half-hourly wind speed data(m s�1) were obtained from the Bureau of Meteorology weatherstation at Meningie (Fig. 1) to approximate wind stress followingthe formula for estimating boundary layer turbulence proposed byMacKenzie and Leggett (1991):

εw ¼ 5:82:10�9w3=z

where w is the wind speed and z is the water depth.

2.2.2. NutrientsDissolved inorganic nutrient concentrations (i.e., silica [Si],

ammonium [NH3], orthophosphate [PO4] and nitrate/nitrite

Fig. 1. Schematic map of the sampling sites (1–5) located along the Coorong, SouthAustralia, between Goolwa and Salt Creek. The weather station recording therainfall data is located at Meningie, approximately at the middle of the Coorong.

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[NOx]) were determined using a Lachat Quickchem Flow InjectionAnalyzer (FIA) following published methods (Hansen and Koroleff,2007). For the analysis, 100 mL of water were filtered in triplicatethrough bonnet syringe Minisart filters (0.45 mm pore size, Sartor-ius Stedim, Dandenong, Australia) to remove large particles.Filtrates were then stored at �20 1C until analysis. Prior toanalysis, the samples were thawed and mixed before injectingapproximately 10 mL of each sample into the FIA in duplicate for atotal of 6 replicates per sample. The detection limits were 40 nMfor dissolved Si species, 70 nM for NH3, 30 nM for PO4 and 70 nMfor NOx. The method was calibrated using standard solutionsprepared in 0.6 M sodium chloride, corresponding to typical sea-water salinity values of 35 PSU.

2.2.3. PhytoplanktonChlorophyll a (chl a) concentrations were used as a proxy for

phytoplankton biomass and were determined by filtering 300 mLof water sample through 47 mm glass microfiber filters (1 mmpore size, Filtech, Fairy Meadow, Australia) using a vacuumpump and a filtration ramp and frozen at �20 1C until analysis.Pigments were extracted in 5 mL of methanol at 4 1C in the darkfor 24 h, before chl a measurements (μg L�1) were made on aTurner 450 fluorometer (Holm-Hansen and Riemann, 1978;Verity et al., 1999).

For the identification and enumeration of phytoplanktonicorganisms larger than 5 mm, 1 L of water was collected in poly-ethylene terephthalate bottles and preserved in 0.5% Lugol's iodine(0.6 M potassium iodide, 0.4 M iodine and 1.5 M acetic acid) andsubsequently identified and enumerated by Microalgal Services(Ormond, Victoria). Samples were filtered through 5 mm pore sizeSterlitech mixed cellulose ester membranes (Sterlitech, Kent, USA).The cells on the filters were resuspended in a smaller volume offiltrate from the same sample. This suspension (1 mL) was thenpipetted into a Sedgewick Rafter and counted using a Zeiss Axiolabupright microscope equipped with bright-field and phase contrastoptics (Carl Zeiss Microscopy, Thornwood, USA). Cells were identi-fied to the genus, or species, level based on their key taxonomicfeatures (Hallegraef et al., 2010; Tomas 1997).

For analytical purposes, the phytoplankton species were groupedinto four taxonomic brackets: diatoms, dinoflagellates, chlorophytesand cryptophytes. To assess species diversity, Margalef's communitydiversity index was computed following the formula:

Dα¼ S�1= log N

where S is the number of species present in a sample and N is the totalnumber of individuals encountered (Margalef, 1968). In addition, aspecies accumulation curve was forecast based on data from the Northand South Lagoons following Drozd and Novotny (2010) using theformula:

Cðn;kÞ ¼nk

� �¼ n!k!ðn�kÞ!

where k is the number of samples used within a data-subset and n isthe total number of samples included in the dataset.

2.2.4. Statistical analysesData collected were found not to be normally distributed after

applying a Kolmogorov–Smirnov test. Therefore, non-parametricSpearman's rank correlations were calculated to estimate thetrends in environmental and biological parameters throughoutthe five sampling sites. To test for significant differences betweenmeans of parameters, nonparametric, two independent sample(Mann Whitney U) tests were applied. Four habitats were selectedaccording to the salinity range of sites, loosely based on the VeniceSystem for the Classification of Marine Waters According toSalinity (Venice System 1959). These were designated H1 to H4

distinguished by the following salinity regimes; H1o5 PSU (freshto low brackish), H2¼5–20 PSU (brackish water), H3 ¼21–40 PSU(high brackish to marine) and H4441 PSU (high marine to hyper-saline).

In order to evaluate the importance of each environmentalvariable in the distribution of phytoplankton communities overthe study period, distance-based redundancy analyses (dbRDA)were conducted. The dbRDA is a routine for the ordination ofprinciple coordinates based on multivariate regression. This ana-lysis was performed to detect linear combinations of environ-mental factors which best describe variations in phytoplanktoncommunity composition. For the ordination of data, PRIMER (v6)and PERMANOVA Aþ for PRIMER were used.

3. Results

3.1. Salinity, river flow and wind stress

In general, the Coorong exhibited clear temporal cycles insalinity and temperature throughout both lagoons. Maxima wererecorded during the austral summer and minima during theaustral winter for both parameters (Fig. 2). The salinity at Site1 during August 2011 was the lowest recorded at 0.15 PSU, whilethe highest salinity was measured at Site 5 during February 2012at 72.13 PSU. Site 1 was found to be the only site at which salinityand wind stress were positively correlated (ρ¼0.443, po0.05). Itbecame apparent that North-Easterly winds generally resulted innoticeable increases in salinity at Site 1. Additionally, salinity wasfound to be negatively correlated with the flow volume of RiverMurray (ρ¼�0.571, po0.01) throughout the North Lagoon(Fig. 6), while no correlation was observed between river flowvolume and salinity in the South Lagoon.

3.2. Nutrient concentrations

Nutrient concentrations were found to be highly variablethroughout the Coorong (Fig. 4). The Murray mouth (Site 1) wasthe most variable site in terms of environmental conditions, asriverine output volume severely affects flow direction/speedand source, and therefore suspended sediment, salinity and

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Fig. 2. Averaged salinity (PSU) of the North Lagoon (black) and South Lagoon (gray)measured over the 24 month sampling period (7SD). The error bars represent thestandard deviation to the mean. The water temperature at the time of sampling inthe North Lagoon (dashed line) and the South Lagoon (solid line) is plotted on thesecondary vertical axis (1C).

J. Jendyk et al. / Continental Shelf Research 91 (2014) 134–144136

anthropogenic/terrigenous pollutant load (Fig. 3). Silicate concen-trations remained relatively constant in the North Lagoon, rangingfrom 25 to 200 mMol L�1. Concentrations in the South Lagoonwere found to be more variable, ranging from 10 to 450 mMol L�1

(Fig. 4A). NH3 concentrations were highly variable during thesurvey, with no clear trends or patterns, although, NH3 concentra-tions in the South Lagoon were markedly higher than in the NorthLagoon (Fig. 4B) (pr0.01). PO4 concentrations were also very

variable but a temporal trend was observed at the Murray mouth(Site 1), with an increase between August 2011 and August 2013(ρ¼0.711, po0.01). With the exception of Site 1, PO4 maxima wererecorded throughout February to April 2012 and throughoutJanuary to April 2013 with concentrations up to 30 mMol L�1.During the other sampled months, PO4 concentrations in theNorth Lagoon (Sites 2 and 3) were lower. NOx concentrations weremarkedly higher in August to November 2011 than throughout the

Fig. 3. Relative abundance of phytoplankton at Site 1 (A), Site 2 (B), Site 3 (C), Site 4 (D) and Site 5 (E). Groups of phytoplankton displayed are: diatoms (light gray),dinoflagellates (black), chlorophytes (white and gray striped) and cryptophytes (dark gray). The total abundance of phytoplankton (number of cells�106 per litre) is plottedalong the secondary vertical axis.

J. Jendyk et al. / Continental Shelf Research 91 (2014) 134–144 137

rest of the study, with concentrations reaching up to 180 mMol L�1

in the South Lagoon. From January 2012 to April 2013, NOx

concentrations in the North Lagoon never exceeded 40 mMol L�1

and concentrations in the South Lagoon ranged from 20 to50 mMol L�1 (Fig. 4D).

3.3. Phytoplankton community

The abundance and distribution of phytoplankton were found tobe highly variable between sites and, especially, between lagoons(Fig. 5). Over the 24 months study period, a total of 52 species of

Fig. 4. Averaged nutrient concentrations of silicate (A), ammonia (B), phosphate (C) and nitrate/nitrite (D) in the North Lagoon (black) and South Lagoon (gray) betweenAugust 2011 and August 2013 (7SD). The error bars represent the standard deviation to the mean. Values for November 2012 are solely based on nutrient concentrationfrom Site 5.

J. Jendyk et al. / Continental Shelf Research 91 (2014) 134–144138

diatoms, 27 species of dinoflagellates, 35 species of chlorophytes and11 species of cryptophytes were identified (Table 2). In general, apositive correlation between phytoplankton abundance and salinitywas observed in the Coorong (ρ¼0.660; po0.05). Chlorophytes,numerically dominated by Chlorohormidium sp. and Oocystis sp.,were found to be the most abundant group in the North Lagoon,particularly at Site 1, where they represented 65% of the overallphytoplankton abundance throughout most of the study. In parti-cular, chlorophytes exhibited a strongly negative correlation tosalinity (ρ¼�0.556; po0.01) and it seemed that 28 PSU representsa threshold value for many of the chlorophytes species, beyondwhich abundance and diversity (Dα) rapidly declined. Some species(e.g. Crucigenia sp. and Oocystis sp.), presumably more tolerant tohigher salinity levels were present in samples from other sites,sometimes exceeding 35 PSU (Fig. 5; Table 1). Diatoms were foundto be the most abundant taxonomic group in the South Lagoon,especially from late Spring until early Autumn. Of the diatoms,Cylindrotheca closterium, Cyclotella sp. and Cocconeis sp. were foundto be the most frequently occurring species. On average, theyaccounted for 19.9%, 12.3% and 12.5% of diatoms recorded eachmonth, respectively. Extensive blooms of C. closteriumwere recordedduring February and April 2012 (Fig. 3), during which C. closteriumconstituted 99.3% and 98.5% of the overall abundance of phyto-plankton, respectively. In addition to being the only species involvedin highly expressed bloom events, C. closterium was found to be themost widely occurring diatoms species, present at every site andduring every month of the two year study period. It becameapparent that increases in the relative diatom abundance oftencoincided with increases in salinity in a given month, particularly inthe South Lagoon (Figs. 2 and 3) and strong positive correlationsbetween diatom abundance and salinity were evident (ρ¼748;po0.01). Similarly, phytoplankton diversity was highly variableboth temporally and spatially. While diatoms were found to be the

most diverse group across both lagoons, the dinoflagellate commu-nity was more diverse in the South Lagoon than in the North Lagoon.The two most abundant dinoflagellate species observed throughoutthe study were Gymnodinioid sp. and Heterocapsa rotundata. Likedinoflagellates, cryptophytes were found to be markedly morediverse in the South Lagoon than in the North Lagoon. However,no significant correlation was observed between cryptophytesabundance/diversity and salinity (p40.05). Hemiselmis sp. andPlagioselmis prolonga were found to be the most abundant crypto-phytes throughout both lagoons.

The distance-based redundancy analyses conducted revealedthat salinity and Si were the two most important environmentalfactors for the distribution of diatoms, explaining approximately13% of the overall geographical community variation. For chloro-phytes, salinity and NOx were found to explain a combined 25% ofthe observed community distribution. For dinoflagellates and cryp-tophytes, salinity and PO4 explained approximately 15% and 16% ofthe total variation in species distribution, respectively. In combina-tion, salinity, Si and PO4 explained approximately 19% of the totaldistribution of all phytoplankton species included (Fig. 7; Table 1).

Based on the entire data set collected, a species accumulationcurve was calculated (Fig. 5), forecasting the expected number ofspecies encountered in a given number of samples. It was foundthat the species encounter rate was considerably higher in theNorth Lagoon than in the South Lagoon which was likely due tothe generally higher variability of environmental parameters inthe South Lagoon.

4. Discussion

4.1. Environmental variability and formation of ecotones

Inverse estuaries are traditionally viewed as ecotonal ecosys-tems because a wide range of comparatively pronounced environ-mental changes often occur over a confined spatial expanse (Attrilland Rundle, 2002). In the Coorong, however, we define thetransition in environmental parameters between different sites,particularly salinity, as ecoclinal as the observed salinity gradientincreases progressively along the estuary. On the other hand, theoverall consistent differences observed between both lagoons(driven by their topo-geographical separation) are viewed asecotonal (Van der Maarel, 1990). This implies the existence oftwo distinct over-arching environments within the Coorong,created by minimal water exchange between the lagoons andthe overall difference in water residence times, fresh water andmarine water input quantities. A third, transient habitat exists invicinity to the mouth which changes, often quite drastically,depending on prevailing weather conditions and whether or notthe mouth is open or closed.

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Fig. 5. Species accumulation curves for the North Lagoon (gray diamonds) andSouth Lagoon (black circles), forecasting the number of species encountered at agiven number of collected samples.

Table 1Margalef's diversity index for the North (N) and South (S) Lagoons by groupa

Wi_11 Sp_11 Su_12 Au_12 Wi_12 Sp_12 Su_13 Au_13 Wi_13

Diatoms N 0.82 0.71 0.61 0.57 0.48 0.43 0.48 0.50 0.59Diatoms S 0.58 0.73 0.45 0.35 0.35 0.43 0.49 0.52 0.42Dinoflagellates N 0.36 0.40 0.19 0.10 0.09 0.10 0.15 0.17 0.20Dinoflagellates S 0.71 0.38 0.17 0.28 0.33 0.19 0.20 0.19 0.15Chlorophytes N 0.34 0.19 0.29 0.49 0.39 0.22 0.12 0.17 0.31Chlorophytes S 0.00 0.02 0.00 0.00 0.05 0.00 0.00 0.03 0.00Cryptophytes N 0.19 0.23 0.20 0.17 0.16 0.13 0.20 0.16 0.18Cryptophytes S 0.24 0.19 0.21 0.09 0.07 0.07 0.03 0.08 0.24All N 1.67 1.39 1.33 1.41 1.22 0.98 1.05 1.09 1.26All S 1.56 1.38 0.88 0.81 0.94 0.80 0.83 0.95 0.77

Shown are the index values for the Austral Winter (Wi), Spring (Sp), Summer (Su) and Autumn (Au) between August 2011 and August 2013.a Highest diversity denoted in bold font.

J. Jendyk et al. / Continental Shelf Research 91 (2014) 134–144 139

The differences observed between both lagoons show someseasonal dependency. Water levels and salinity have previously beenfound to be the main causal factors in ecological response modeling inthe Coorong (Lester and Fairweather, 2009). In particular, mostecologically significant variables (e.g., salinity and nutrient regimes)are affected by fresh water influx and can be expected to varysignificantly between periods of increased river flow and ‘dry’ periods.

The large difference in salinity between lagoons can beexplained by the exacerbation of water-flow limitations duringperiods of decreased precipitation, constricting Parnka Pointfurther and impeding the water exchange between lagoons

Table 2List of phytoplankton identified in the Coorong, South Australia. Chlorophytes (CHLOR; 35 spp.), cryptophytes (CRYPT; 11 spp.), diatoms (DIAT; 52 spp.) and dinoflagellates(DINO; 28 spp.).

Achnanthes sp. DIAT Eucampia zodiacus DIAT Nitzschia spp. DIATAchnanthidium sp. DIAT Fallacia sp. DIAT O1yrrhis marina DINOActinastrum sp. CHLOR Fragilaria sp. DIAT Oocystis sp. CHLORAmphidinium sp. DINO Fragilariopsis sp. DIAT Paralia sulcata DIATAmphora sp. DIAT Fusola sp. CHLOR Pediastrum sp. CHLORAnaulus australis DIAT Gomphonema sp. DIAT Peridinium sp. DINOAnkistrodesmus sp. CHLOR Gonyaulax spp. DINO Plagioselmis prolonga CRYPTAnkyra sp. CHLOR Grammotophora sp. DIAT Plagiotropis sp. DIATAsterionella formosa DIAT Guinardia Striata DIAT Pleurosigma sp. DIATAsterionellopsis glacialis DIAT Gymnodinioid o20 um sp. DINO Polykrykos schwartzii DINOAsteromphalus sarcophagus DIAT Gymnodinioid 420 um sp. DINO Preperidinium meunieri DINOAulacoseira granulata DIAT Gymnodinium cf. aureolum DINO Prorocentrum cordatum DINOBacillaria paxillifera DIAT Gyrodinium spp. DINO Prorocentrum micans DINOCeratium furca DINO Gyrosigma spp. DIAT Prorocentrum sp. DINOcf. Fragilaria sp. DIAT Hantzschia sp. DIAT Protoperidinium spp. DINOChaetoceros spp. DIAT Hemiselmis sp. CRYPT Pseudo-nitzschia delicatissima DIATChlamydomonas sp. CHLOR Heterocapsa rotundata DINO Pseudo-nitzschia australis DIATChlorella sp. CHLOR Heterocapsa triquetra DINO Rhisozolenia sp. DIATChlorohormidium sp. CHLOR Hyaloraphidium sp. CHLOR Rhodomonas lacustris CRYPTChodatella sp. CHLOR Karenia mikimotoi DINO Rhodomonas salina CRYPTChroomonas spp. CRYPT Karenia spp. DINO Rhodomonas sp. CRYPTClosteriopsis sp. CHLOR Katodinium glaucum DINO Rhopalodia sp. DIATClosterium sp. CHLOR Katodinium sp. DINO Scenedesmus quadricaudus CHLORCocconeis spp. DIAT Kirchneriella sp. CHLOR Scenedesmus sp. CHLORCochlodinium spp. DINO Komma sp. CRYPT Schroderia sp. CHLORCoelastrum sp. CHLOR Kryptoperidinium sp. DINO Scrippsiella spp. DINOCoenocystis sp. CHLOR Kryptoperidinium sp. DINO Skeletonema costatum DIATCoscinodiscus spp. DIAT Leucocryptos marina CRYPT Sphaerocystis sp. CHLORCosmarium sp. CHLOR Leucocryptos sp. CRYPT Staurastrum sp. CHLORCrucigenia sp. CHLOR Licmophora sp. DIAT Stauroneis sp. DIATCryptomonas sp. CRYPT Mastogloia sp. DIAT Surirella sp. DIATCyclotella sp. DIAT Melosira sp. DIAT Tabellaria sp. DIATCylindrotheca closterium DIAT Meunieria membranacea DIAT Takayama sp. DINODictyosphaerium sp. CHLOR Micractinium sp. CHLOR Teleaulax acuta CRYPTDimorphococcus sp. CHLOR Micrasterias sp. CHLOR Tetraedron sp. CHLORDiploneis sp. DIAT Minidiscus trioculatus DIAT Tetrastrum sp. CHLORDiplopsalis sp. DINO Minutocellus sp. DIAT Thalassionema sp. DIATDunaliella sp. CHLOR Monoraphidium sp. CHLOR Thalassiosira cf. mala DIATElakatothrix sp. CHLOR Mougeotia sp. CHLOR Thalassiosira sp. DIATEncyonema sp. DIAT Naviculoid spp. DIAT Torodinium sp. DINOEntomoneis sp. DIAT Nephrocytium sp. CHLOR Treubaria sp. CHLOREpithemia sp. DIAT Nitzschia sigmoidea DIAT Trybionella sp. DIAT

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Fig. 6. Monthly flow volume of the River Murray over the 24 months samplingperiod. Averaged salinities of the North Lagoon (solid line) and the South Lagoon(dotted line) are plotted on the secondary vertical axis.

Fig. 7. Distance-based redundancy analysis of all phytoplankton identified andenumerated over the study period. Habitats were used as factors in the ordinationand data points are displayed as H1 (black triangle), H2 (gray circle), H3 (dark graydiamonds) and H4 (asterisks).

J. Jendyk et al. / Continental Shelf Research 91 (2014) 134–144140

(Figs. 1 and 8). In addition, evaporation will be higher during thosedry periods, particularly throughout the southern reaches of theCoorong (Grigg et al., 2009; Lamontage et al., 2004). While adecrease in the amount of riverine and lacustrine inflow can causean increase in the intrusion of seawater into the Coorong,recurring drought conditions also intensify the expression of theecotonal boundary between lagoons.

In terms of ecological disparity between sites, ‘wet’ years wouldimply the formation of one clear ecotonal boundary marked by theseparation of both lagoons. Another, less pronounced, ecotonalboundary between Site 1 and the rest of the North Lagoon can beobserved, based on the prevalence of wind and tides. During ‘dry’periods, on the other hand, the ecotonal boundary between bothlagoons would intensify drastically. Furthermore, the ecotonalboundary between the Murray Mouth and the rest of the NorthLagoon could theoretically fade as the mouth loses connectionwith the open ocean (or the width of the mouth decreases) andtides no longer penetrate the estuarine main.

This model reflects the extent to which the river plume, as wellas seawater, penetrate into the lagoons. Webster (2001) foundshort-term wind stress to affect water levels in both lagoonsindividually, while long-term and unidirectional wind stress facil-itates exchange of water between the lagoons through Parnka Point,leading to an overall ‘tilt’ in the water-level equilibrium. Dependingon the direction of this tilt (manifesting as an unusual difference intotal volume of one lagoon) and the overall volume of water in theCoorong, a drop in latitudinal wind stress would therefore triggerequilibrating between lagoons and facilitate further exchange.Currently, we regard the Coorong as healthy, as it has recoveredfrom the last drought event. It maintains connection to the oceanand also receives continuous, albeit varying, freshwater input overthe barrages. However, this can be regarded as a transitory state, asall water bodies related to the Coorong (Figs. 1 and 8) are directlydependent on continuous connectivity in order to maintain currentconditions. A cessation of rainfall along the Murray-Darling basincan be expected to trigger a chain reaction, causing not only thewater flow across the barrages to decrease (or stop) but alsoexchange between the lagoons as well as between the North Lagoonand the Southern Ocean.

4.2. Phytoplankton communities

Throughout this study, it became apparent that the structure ofthe phytoplankton community was highly variable along the

length of the Coorong, as both temporal and spatial differ-ences in abundance and diversity were evident. Spatially, thedisparity in the structure of phytoplankton communities wasparticularly noticeable between both lagoons. In general, themain environmental variable driving differences was found tobe salinity.

Previous studies have established that the anthropogenicregulation of water flows into an estuary can negatively impactupon its productivity (Burford et al., 2011). Here, the River Murrayand the amount of water it carries towards the Coorong, stronglyimpacts upon the abundance and diversity of the phytoplanktoncommunities throughout the North Lagoon. This is corroboratedby the findings of Lester and Fairweather (2009), who determinedthat the River Murray plays a key role in the distribution ofphytoplankton in the North Lagoon. Previous studies on theabundance of phytoplankton in estuaries generally agree thatsharp distinctions between marine and freshwater species exist,giving rise to two distinct populations as well as a third, estuarinecommunity (Muylaert et al., 2009). The salinity regimes of theCoorong allowed for the distinction of 4 habitats (i.e. H1 to H4).Waters in the H1 category (o5 PSU) were dominated by chlor-ophytes, although diatoms and cryptophytes sporadicallyaccounted for between 10 and 50% of the overall phytoplanktonabundance at Site 1 and Site 2. The H2 category (5–20 PSU) was co-dominated by chlorophytes, diatoms and cryptophytes with nosignificant temporal differences in the relative overall abundanceevident. Waters in the H3 category (21–40 PSU) saw drasticdecreases in the prevalence of chlorophytes compared to lowersalinity habitats and marked increases in the abundance ofdinoflagellates, particularly toward the higher end of the salinityspectrum. The H4 category (441 PSU) was mainly dominated bydiatoms, although the abundance of dinoflagellates was some-times higher than that of diatoms.

The inter-annual variations in fresh water input therefore seemto carry significant implications for the phytoplankton commu-nities of the Coorong. While chlorophytes dominated the commu-nity at lower salinities (i.e., H1 and H2), diatoms were the prevalentgroup observed throughout the more saline sites (i.e., H3 and H4).On average, diatoms were between two and three times moreabundant in H3 and H4 areas than in less saline regions. On theother hand, dinoflagellates were up to five times more abundant inH3 and H4 areas than in H1 and H2 waters. Furthermore, thecomparatively low dinoflagellate abundances throughout thenorthern reaches of the Coorong may partly be owing to barrageand estuarine interface-driven water column perturbation andwarrant further investigation.

The subdivision of biomes into habitats along salinity gradientsfurther supports the notion of distinct phytoplankton populations,based on their origin (Muylaert et al., 2009). It should be notedthat the de facto absence of chlorophytes throughout the H3 and H4

reaches of the estuary is the main causal factor behind thegenerally lower phytoplankton diversity in the South Lagoon,when compared to the North Lagoon (Figs. 3 and 5; Table 1).

Of the 35 species of chlorophytes encountered throughout thisstudy, only 4 appeared in samples from the South Lagoon for morethan one month (Chlamydomonas sp., Chlorohormidium sp., Dunaliellasp. and Oocystis sp.). Previous studies have elucidated that certainspecies of chlorophytes, e.g., Oocystis sp., are directly affected bychanges in salinity and nutrient regimes and that salinities exceedinga certain threshold may prevent proliferation (Huang et al., 2012;Talbot et al., 2008). Here, we therefore suggest that chlorophytes havea maximum salinity threshold of 28 PSU. In terms of overall abun-dance, there existed a seven-fold difference between the abundance ofchlorophytes in H1 to H2 areas and their abundance in H3 to H4 areas.This is further supported by the ordination of data as shown in Fig. 7.Using the habitats as factors, a clear pattern along salinity emerges.

Fig. 8. Conceptual model of water exchange between both lagoons of the Coorong,separated at Parnka Point (PP), and connected water bodies. Dark arrows betweentwo water bodies indicate a potential for increasing salinity via water exchange,light arrows indicate decreases in salinity.

J. Jendyk et al. / Continental Shelf Research 91 (2014) 134–144 141

This reinforces the fact that salinity is an important variable for each ofthe phytoplankton groups surveyed.

It has been shown that increases in the water exchange ratesand/or increases in turbidity negatively affect dinoflagellate growth,while stimulating both diatoms and chlorophytes (Smayda, 1998).Conversely, in the South Lagoon, elevated nutrient concentrationsmay further support the overall higher success of diatoms, due totheir greater nutrient uptake affinity, allowing diatoms to out-compete groups with lower uptake affinities (Margalef, 1968). Thismay also be corroborated by highly fluctuating nutrient concentra-tions over the study period. Similar patterns (spontaneous, atypicallyhigh ammonia concentrations) were reported by Haese et al. (2009)and may be symptomatic of the Coorong during periods of eitherincreased terrigenous run-off or re-suspension of sediments bywind-forcing in the South Lagoon.

The predominance of diatoms in the South Lagoon suggeststhat they are more adaptable to hyper-saline conditions. Whilecertain species/genera (e.g., Cocconeis sp.) are ubiquitously dis-tributed over the entire length of the Coorong, other species (e.g.,C. closterium) can be found at each site throughout the year but aremuch more successful at H3 to H4 sites, where saline conditionsmay be too high for other species to proliferate. Leterme et al.(2010) demonstrated that the endemic diatom Cocconeis placen-tula modifies its nano-morphology in order to adapt to varyingenvironmental conditions, particularly salinity. They hypothesizedthat this mechanism allows the diatoms to absorb nutrients fromits environment, regardless of saline regimes and thereforeincreases its competitiveness under environmental stress.

The period of drought observed from 2004 to 2010 caused asevere recession of water levels, particularly in the South Lagoon(Leterme et al., 2012; Zampatti et al., 2010). This could suggest thatsome of the species observed in the South Lagoon throughout thisstudy are newly established. Because salinity appears to be themain factor driving the composition of the phytoplankton com-munity, the onset of a new drought would imply an overall shifttoward diatom dominance in the Coorong.

A change of dominance patterns within the phytoplanktoncommunity could have significant consequences for the trophicweb. For example, previous studies have investigated the potentialof certain diatom species to reduce or inhibit reproductive successin copepods (Ban et al., 1997; Irigoien et al., 2002). In an estuarine,and therefore geographically constricted, environment this meansthat harmful primary producer blooms could potentially seriouslyimpact upon the recruitment success of zooplankton and trigger acascading effect, altering entire ecosystems. This could impact onthe higher levels of the food chain such as fish and migratory birdsand need to be monitored.

4.3. Maintaining environmental health in the Coorong

While the Coorong shares features with many other interna-tionally researched inverse estuaries and coastal lagoons, its statusas terminus of Australia's most important waterway (the Murray-Darling Basin; Leterme et al., submitted for publication) and itsabsolute dependency on continuing freshwater flow make itcomparatively highly susceptible to climatic change. Salinitiesare known to more than double (in some areas even triple) duringperiods of drought, which drastically changes the suitability of theCoorong as habitat not only for primary producers, but for alltrophic levels encountered within the estuarine main. It stands toreason that the impact of salinity as ecological driver of thephytoplankton community becomes even more pronouncedduring times of increased environmental variability (Fig. 7). Evenduring drought recovery and ‘wet’ periods, falling water levelswithin the River Murray and the Lower Lakes have a direct

and significant impact on the Coorong, resulting in salinityincreases, as well as significant increases in water residence times.This is largely due to circulation patterns becoming limited towind-driven exchange between the lagoons and progressivelydecreasing channel width at the division, Parnka Point (Fig. 8).This eventually leads to a cessation of exchange between thelagoons and further increasing salinity disparity between them.While increases in water residence times have previously beenreported to directly affect biota composition in estuaries, they arerarely accompanied by salinity spikes as pronounced as in theCoorong. Everett et al. (2007) describe the closure of Smiths Lake,New South Wales, from the open ocean as trigger for an expansionof seagrass meadows, likely caused by a drastic change to nutrientregimes and exchange rates, while the reopening of the estuaryand its flushing with nutrient-poorer water results in a decline inbiomass expansion. While we did not encounter periods ofnutrient limitation in the Coorong, we observed a similar patternof community re-structuring in that chlorophytes were graduallyreplaced by diatoms during periods of salinity increase or locationswith inherent salinity variability (e.g., Site 3; Fig. 1).

Coutinho et al. (2012), on the other hand, found that areas of anestuary (i.e., Óbidos) with particularly low circulation patterns buthigh nutrient loads were dominated by green macroalgae. While itis hypothesized that these green algae outcompete other phyto-plankton groups for nutrients, it appears feasible to assume thatshading may well play an important role as well. While sewagecontamination is a major factor in their study, Coutinho et al.(2012) further stipulated that, during times of estuarine separationfrom the sea, the calm conditions and augmented nutrient con-centrations benefit the phytoplankton community. While ourstudy does not encompass data from dry periods, during whichthe Coorong is disconnected from the Southern Ocean, it stands toreason that, while the resulting increase in water residence timescould benefit local phytoplankton communities, the (sometimes)exponential increase in salinity has the potential of drasticallyskewing the North Lagoon community composition in favor ofdiatoms and other, more salinity tolerant groups.

Maintaining environmental health is a topic of high importancefor the Coorong. Because recurring drought conditions and theimplied rise in industrial/agricultural water abstraction from theRiver Murray lead to inevitable increases in salinity, particularly inthe South Lagoon, management plans need to be designed in orderto minimize damage to the ecosystem. Especially for the NorthLagoon, our findings suggest a possible shift from chlorophyte todiatom dominance during times of decreased river flow andeventual Murray mouth closure. Historical data (Leterme et al.,submitted for publication) suggests that, during years of drought(e.g., 2004), even the northernmost reaches of the estuary exceedthe 28 PSU threshold for chlorophytes and therefore becomeuninhabitable for most species encountered throughout our study.For obvious reasons the removal of chlorophytes, as integral partof estuarine trophic webs (Parab et al., 2013), from the NorthLagoon may carry significant ramifications for the ecosystem andits suitability for various endemic, as well as migratory speciesfound in vicinity of the Coorong during wet years. One measure,frequently employed in the Murray mouth region, is dredging tomaintain shipping channel depths. While this aides in diffusinglong water residence times in the North Lagoon, it does in no wayimply a decrease in salinity as marine water enters the estuarywithout subsequent mixing with freshwater through the barrages.Even at ambient seawater salinity, the dominant chlorophytesspecies, Chlorohormidium sp., has been found not to flourish.

Ultimately, this means that in order to maintain the Coorong ina healthy condition, steps must be taken to ensure sufficientfreshwater enters the system, particularly during exceptionallyarid years and summers. While this may imply significant losses in

J. Jendyk et al. / Continental Shelf Research 91 (2014) 134–144142

terms of agricultural yield along the Murray Darling Basin, it maybe the only option to prevent long-term damage, lasting changesto trophic orders and the disappearance of endemic species fromthis iconic ecosystem.

5. Conclusion

The Coorong, South Australia, has been established as a habitatin a constant state of change. While a wide range of phytoplanktonspecies has been encountered throughout this study, their originand/or preferred habitat within the estuary are highly group-dependent. Two distinct ecoclinal groupings were evident, mark-ing the lateral increase in salinity along the North Lagoon betweenSites 1 to 3, an ecotonal ‘cut-off’ at Parnka Point, followed by thefar less variable ecocline (but more extreme, in terms of salinityand nutrient concentrations) of the South Lagoon. Parnka Point isespecially interesting in that the amount of water exchangebetween both lagoons, afforded by its narrow channel, is clearlyinsufficient to allow for any measurable impact of the flow volumeof the River Murray on the southern reaches of the Coorong. Basedon this, we can identify three distinct populations of phytoplank-ton as a function of salinity:

� Based largely on the evidence provided by the absence ofchlorophytes in the higher salinity ranges, they would consti-tute the first population that is adapted to fresh water and lowbrackish conditions.

� The second population consists mainly of diatoms and dino-flagellates which are much more successful in the highersalinity areas of the Coorong in comparison to chlorophytesand cryptophytes.

� An additional population is identified as transitory or euryha-line. This population consists mainly of species encountered atmost (if not every) site throughout much of the year andremains largely unaffected by inter-seasonal changes insalinity.

These findings are essential to the future management of theCoorong wetlands in order to preserve its environmental healthand, by extension, its fisheries and touristic significance. Inaddition to presenting a useful tool for assaying the local phyto-plankton communities, our findings can help predict the impacton other members of the food chain, particularly commerciallyimportant species. Considering the fundamental role phytoplank-ton plays in determining the quality of estuarine habitats and theirbottom-up control on trophic webs in general, they representexcellent bio-indicators for the Coorong. In order to preventextensive damage to the current trophic interactions in theCoorong, recurring drought conditions should be mitigated byadjusting freshwater flow over the barrages accordingly. Given weregard the estuary as healthy at the moment, future managementplans should aim to maintain salinities as close to what they arenow as possible. At the very least, drastic increases, especially past28 PSU throughout the northernmost parts of the estuary shouldbe avoided where possible to ensure the currently evident speciesbalance.

Acknowledgments

Funding was supported under Australian Research Council'sDiscovery Project funding scheme (DP110101679). J.J. was sup-ported by a Flinders University Research Scholarship as well as aNational Center for Excellence in Desalination supplementaryscholarship. The authors kindly thank Dr. Daniel Jardine and

Mr. Jason Young of Flinders Analytical, Dr. Steve Brett of MicroalgalServices, and Ms. Elsa Abs of the Paris Institute for Life, Food andEnvironmental Sciences for their help in the acquisition andanalysis of samples and data. We would like to acknowledge theDepartment of Environment, Water and National Resources(DEWNR) for giving us access to the Coorong National Park andSA water for access across the barrages.

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