Estuarine, Coastal and Shelf Science 79 (2008) 599–606

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Estuarine, Coastal and Shelf Science

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The recovery of microalgal production and biomass in a South African

temporarily open/closed estuary, following mouth breaching
Akash Anandraj a, b, *, Renzo Perissinotto b, Christian Nozais b, c, Derek Stretch d
a
Department of Nature Conservation, Mangosuthu University of Technology, PO Box 12363, Jacobs 4026, Durban, South Africa
b
School of Biological and Conservation Sciences, University of KwaZulu-Natal, Westville Campus, Private Bag X54001, Durban 4000, South Africa
c
Département de biologie et centre d’études nordiques, Université du Québec à Rimouski, 300 Allée des Ursulines, Rimouski (Québec), Canada G5L 3A1
d
School of Civil Engineering, Surveying and Construction, University of KwaZulu-Natal, Howard College Campus, Durban 4041, South Africa

a r t i c l e i n f o a b s t r a c t

Article history: Mouth breaching is a recurrent event in temporarily open/closed estuaries (TOCEs). Such disturbances
Received 14 February 2008 result in flushing and sediment scouring, reducing the microalgal biomass stock. The depletion of these
Accepted 30 May 2008 microalgae may have negative repercussions in the form of depleted stocks of commercial fish, game fish,
Available online 7 June 2008
crustaceans and mollusks. The aim of this investigation was therefore: (1) to monitor the recovery of
microalgal biomass and production following a breaching event; and (2) to determine the key envi-
Keywords: ronmental parameters influencing primary production during the open and recovery phases. Phyto-
primary production
plankton and benthic microalgal production was measured (14C-uptake method) successively during the
phytoplankton
benthic microalgae
closed, open and recovery phases of the Mdloti TOCE (South Africa). Upon breaching, 94–99% of
temporarily open/closed estuaries microalgal biomass was washed out to sea through flushing and sediment scouring. A temporary
South Africa recovery of phytoplankton and benthic microalgal biomass was observed during the open phase, but this
was not sustained because of continual flushing and scouring of the sediment. During the re-closure
(recovery phase), microalgal biomass immediately increased, reaching pre-breaching levels 35–40 days
following the breaching event. In contrast to biomass, autochthonous pelagic primary production
reached a maximum level (341 mg C m2 h1) during the open phase. Pelagic primary production nor-
malized to biomass (PB) significantly increased during the open phase. This is attributed to a favorable
combination of optimum light conditions, high influx of macronutrients and high water temperatures
(33  C). Similarly, benthic primary production normalized to biomass (PB) peaked during the open phase
(35 mg C mg chl-a1 h1). Multivariate analysis showed that major variations in primary production were
mainly controlled by temperature, dissolved inorganic nitrogen (DIN) to phosphorus (DIP) molar ratios
(water-column and pore-water) and light extinction (Kd), all of which were regulated by the state of the
mouth.
Ó 2008 Elsevier Ltd. All rights reserved.

1. Introduction microalgae also stabilize the sediment by the extrusion of extra-

cellular polymeric substances (Holland et al., 1974; Paterson and
During the last decade, major interest has arisen on the role of Black, 1999). Phytoplankton are equally important as they play
benthic microalgae as a primary carbon source for estuarine food a significant role in the nutrient cycling, water quality and as a food
webs and as an important component in the cycling of nutrients in source for pelagic heterotrophs (Dame and Dankers, 1988; Cloern,
tidal estuaries (Heip et al., 1995; MacIntyre et al., 1996; Guarini 1996; Lucas et al., 1999). Although the importance and dynamics of
et al., 1997, 2006). Benthic microalgae are an essential carbon microalgae in temperate tidal estuaries are reasonably well
source for both benthic and pelagic estuarine heterotrophs (Her- established (Underwood and Kromkamp, 1999), there is little in-
man et al., 1999; Kibirige and Perissinotto, 2003; Nozais et al., formation in this regard for tropical and subtropical temporarily
2005), and can influence the exchange of oxygen and nutrients open/closed estuaries (TOCEs). In TOCEs, microalgal biomass has
across the sediment–water interface (Sundbäck and Granéli, 1988; shown clear temporal and spatial patterns during the heteroge-
Sundbäck et al., 1991, 2004; Cabrita and Brotas, 2000). These neous conditions of the open and closed phases (Adams et al., 1999;
Froneman, 2002; Perissinotto et al., 2002; Skinner et al., 2006;
* Corresponding author. Department of Nature Conservation, Mangosuthu Uni-
Anandraj et al., 2007). However, the causal agents of the variability
versity of Technology, PO Box 12363, Jacobs 4026, Durban, South Africa. in microalgal production in these dynamic systems are poorly
E-mail address: [email protected] (A. Anandraj). understood, with the knowledge limited to what has so far been

0272-7714/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2008.05.015
600 A. Anandraj et al. / Estuarine, Coastal and Shelf Science 79 (2008) 599–606

gathered through a few studies conducted in Australia (Eyre, 2000;

Roy et al., 2001) and South Africa (Froneman, 2002; Perissinotto
et al., 2003; Skinner et al., 2006). Information on the recovery of
microalgal production and biomass, especially after breaching
events, is a critical requirement for the effective management of
South
conditions such as artificial breaching, regulation of nutrient influx Mdloti Estuary
Africa
from sewage treatment plants and the monitoring of microalgal Durban 29o38‘S; 31o08‘E
growth and eutrophication.
The South African coast has 71% of its estuaries classified as
TOCEs (Whitfield, 1992). In KwaZulu-Natal, rainfall is strongly
seasonal with more than 80% of annual rain falling between
October and March (de Villiers, 2005). During winter and under low Mdloti Estuary
river flow conditions, TOCEs mouths remain closed by a sandbar.
Scale
Subsequent to periods of high rainfall and freshwater runoff, the
water level inside these estuaries may rise until it equals or exceeds 0 300 m
the height of the sandbar at the mouth (Whitfield, 1992). Breaching
of the sandbar at the mouth is driven directly by high water levels, N
which cause overtopping and/or seepage-driven-erosion of the
sandbar. TOCEs close when the sandbar at the mouth is regen-
erated, usually within weeks, by long-shore and cross-shore sand S
movements in the surf-zone. This period of re-closure initiates
a new phase of relatively stable physical conditions and an asso-
ciated biological recovery of the estuary.
U
Recovery of an aquatic ecosystem generally implies return to
a pre-disturbance state, termed the nominal state or equilibrium Old North Coast Road
state (O’Niell, 1999). Physico-chemical and/or biological indicators M
are generally used to assess the extent of recovery. According to De
Pledge (1999), detailed knowledge of community and population
processes will not guarantee a proper assessment of recovery if L
physiological indicators fail to show recovery at the individual level.
Determining that the extent of biological recovery is complex, Indian Ocean
a consequence of organisms compensating for the disturbance by
exhibiting adjusted physiological or behavioral mechanisms for Fig. 1. Map of the Mdloti Estuary with sampling stations lower (L), middle (M) and
survival (Power, 1999). upper (U) reaches.
In this study, the recovery phase is defined as the period
coinciding with re-closure of the mouth and during which micro-
algal biomass increases to reach pre-breaching levels. This study, (ca. 20 cm above the sediment). Pore-water samples for the mea-
therefore, aims to: (1) monitor the recovery of microalgal biomass surement of dissolved inorganic nitrogen, DIN (NO  þ
2 , NO3 and NH4 )
and primary production following a breaching event; and (2) and dissolved inorganic phosphorus, DIP (ortho-phosphorous)
determine the key environmental parameters influencing primary were collected using a hand-operated vacuum pump extractor
production during the open and recovery phases. connected to an enclosed stainless steel rod inserted into the sed-
iment (5–10 cm below the sediment–water interface). At the lower
2. Materials and methods tip of the pipe, tiny holes were drilled, in order to ensure the inward
flow of pore-water while minimizing the passage of fine sand and
2.1. Physico-chemical environment silt particles. Pore-water samples were then placed in 500 ml acid
pre-washed polyethylene bottles and stored at w4  C for 24 h.
The study took place at the Mdloti, a perched temporarily open/ Triplicate sub samples (100 ml) were used to determine inorganic
closed estuary (TOCE) located on the north coast of KwaZulu-Natal nutrient concentrations, using a Technicon Autoanalyzer II system,
(Fig. 1). Investigations commenced during the closed phase (12, 19, following the methods of Mostert (1983).
26 September; 10 October and 14 November 2003), and continued
during the open (13, 17, 20, 24, 27 February and 5 March 2004) and
recovery phases (23, 29 March; and 2, 6, 8, 12, 15 April 2004). 2.2. Microalgal biomass and production
Environmental parameters were measured at three stations: the
lower (L), middle (M) and upper reaches (U) (Fig. 1). Vertical pro- Samples for phytoplankton biomass analysis were collected at
files of salinity and temperature were recorded at 10 cm intervals the sub-surface and in near-bottom water using a 500 ml poly-
during each sampling period, using a YSI 6920 multi-probe data ethylene bottle and a 1000 ml weighted pop-bottle, respectively.
logger. Irradiance levels (PAR, 400–700 nm) were measured at Water-column samples (200 ml) were sequentially size-fraction-
50 cm depth intervals with a LI-COR light meter provided with a ated into microphytoplankton (>20 mm), nanophytoplankton
LI-193SA spherical quantum sensor. PAR diffuse attenuation (2–20 mm) and picophytoplankton (<2 mm), using a 20-mm Nitex
coefficient, Kd, was then determined from these data according to filter, a 2-mm Millipore filter and a GF/F Advantec filter, respectively.
Kirk (1994). The theoretical depth of the euphotic zone was esti- Size-fractionated phytoplankton biomass was determined during
mated using the formula: 4.6/Kd (Falkowski and Raven, 1997). the open and recovery phases only. For the determination of benthic
Water samples for the determination of dissolved inorganic nitro- microalgal biomass, triplicate samples of the upper 3 and 10 mm of
gen (DIN; nitrate þ ammonia) and dissolved inorganic phosphate sediments were collected using a perspex twin-corer (20 mm i.d.)
(DIP; ortho-phosphate) concentrations were collected at the sub- (Nozais et al., 2001). Phytoplankton and benthic microalgal pig-
surface (ca. 5 cm below surface) and in the near-bottom layers ments were all extracted in 90% acetone over 24–48 h, at 4  C in the
 A. Anandraj et al. / Estuarine, Coastal and Shelf Science 79 (2008) 599–606 601

dark. Chl-a and phaeopigment concentrations of phytoplankton 800

lower middle upper
and benthic microalgae were estimated using a 10-AU Turner
Designs fluorometer, fitted with the narrow band, non-acidification 700
system (Welschmeyer, 1994; Nozais et al., 2001). Vertically in-

Bottom irradiance (µmol m-2s-1)

tegrated water-column chl-a concentrations were calculated for 600
each station by averaging the surface and bottom chl-a values and
multiplying the average by total water depth. Pelagic and benthic
500
microalgal production was estimated using the 14C-uptake method
according to the protocol described in Anandraj et al. (2007). Carbon
400
fixation by phytoplankton and benthic microalgae was computed
according to Parsons et al. (1984) and Roux et al. (2002),
300
respectively. For each station, phytoplankton production was in-
tegrated over the water-column by averaging the surface and bot-
tom primary production values and multiplying the average by the 200
total water depth. Surface and bottom production values were
normalized to chl-a. The benthic microalgal production normalized 100
to chl-a was determined using chl-a concentrations obtained from
the 3 mm cores. 0

12 Sept. 03

02 Oct. 03

22 Oct. 03

11 Nov. 03

01 Dec. 03

21 Dec. 03

10 Jan. 04

30 Jan. 04

19 Feb. 04

10 Mar. 04

30 Mar. 04

19 Apr. 04
2.3. Statistical analyses

The analysis of primary production data was undertaken using

pooled and individual stations (lower, middle and upper reaches). Months
Prior to the analysis, all variables were log10-transformed to comply
Fig. 2. Bottom irradiance of the lower, middle and upper reaches during the closed
with the requirement of normality in the data distribution. Pelagic
(solid line, 12 Sept.–14 Nov. 2003), open (dotted line, 13–27 Feb. 2004) and recovery
and benthic environmental parameters were each subjected to phases (solid line, 23 Mar.–12 Apr. 2004).
a Principal Component Analysis (PCA) to identify those variables
accounting for most of the spatial and temporal variability in
phytoplankton and benthic microalgal production. The ordination
was performed with the SPSS (Version 11.5) on the correlation
matrix. Differences in integrated pelagic and benthic primary
production between stations (lower, middle and upper reaches)
250
and between the open, closed and recovery phases were examined
using a two-way ANOVA. Differences in pelagic and benthic
DIN:DIP molar ratios between the closed (n ¼ 15), open (n ¼ 18) and lower middle upper
recovery (n ¼ 21) phases were determined using a two-way ANOVA
on pooled data. Correlation analysis (Pearson r) of pelagic and
200
benthic primary production and biomass with environmental var-
iables as well as with pelagic and benthic Principal Component
scores was computed. For partial correlation analysis, the con-
trolled factors used in the computation were temperature, salinity,
Pelagic chl-a (mg m-2)

DIN, DIP, Kd, PAR, depth and mouth state.

150

3. Results

3.1. Physico-chemical environment (Table 1)

100
The survey period (Sept. 2003–Apr. 2004) coincided with the
high rainfall, spring–summer, season with a maximum of 115 mm
of rain recorded in February 2004. Consequently, the Mdloti

50
Table 1
Physico-chemical parameters (min–max) measured for the closed, open and
recovery phases. The data are pooled for the lower, middle and upper reaches of the
Mdloti Estuary

Closed phase Open phase Recovery phase

(n ¼ 15) (n ¼ 18) (n ¼ 21) 0
Water depth (m) 1–3.4 0.08–1 0.8–2
12 Sept. 03

26 Sept. 03

14 Nov. 03

17 Feb. 04

24 Feb. 04

05 Mar. 04

29 Mar. 04

06 Apr. 04

12 Apr. 04

Euphotic depth (m) 1–14 0.2–92 1–4

Kd (m1) 0.3–3 0.05–21 1–4
Bottom PAR (mmol m2 s1) 7–50 7–697 2–90
Salinity 0.3–0.7 1–31 0.9–2.5
Pelagic DIN (mmol) 1–24 0.1–70 0.07–26 Months
Pelagic DIP (mmol) 0.7–338 0.1–3 0.06–4
Fig. 3. Temporal variations in pelagic chlorophyll-a (average  SD) at the lower, middle
Pore-water DIN (mmol) 3–30 3–229 5–239
and upper reaches, for the closed (solid line, 12 Sept.–14 Nov. 2003), open (dotted line,
Pore-water DIP (mmol) 1.5–11.5 0.06–2 0.06–69
13–27 Feb. 2004) and recovery phases (solid line, 23 Mar.–15 Apr. 2004).
602 A. Anandraj et al. / Estuarine, Coastal and Shelf Science 79 (2008) 599–606

sandbar breached twice during this period; a complete breaching ANOVA, p < 0.001) and recovery phases (0.03–21) (Tukey’s HSD,
took place on 11 February and reduced the average water depth p < 0.05). Similarly, pore-water molar ratios of DIN:DIP were sig-
inside the estuary to 0.5 m, while a partial breaching (constricted nificantly higher during the open (3–2364) phase compared to the
mouth) occurred on 17 February 2004. Prior to breaching, the es- closed (0.5–9) (two-way ANOVA, Tukey’s HSD, p < 0.0001) and
tuary remained closed for most of the year, with an average rainfall recovery phases (0.3–1406) (two-way ANOVA, Tukey’s HSD,
of 89 mm recorded during the months of September–November p < 0.05).
2003. During the closed phase, the maximum water depth was
3.4 m. The average monthly rainfall during the recovery phase was 3.2. Microalgal biomass and production
39 mm and at the end of this period, 56 days after the breaching
event, the average water depth was 2 m (lower reaches). During the closed phase (12 Sept.–14 Nov. 2003), phytoplankton
The theoretical euphotic depth was often deeper than the total biomass ranged from 3 (upper reaches) to 96 mg chl-a m2 (lower
water depth during the study period. It ranged from 1 to 14 m, from reaches) (Fig. 3). Two weeks prior to breaching, phytoplankton
0.2 to 92 m and from 1 to 4 m during the closed, open and recovery biomass averaged 49, 76 and 48 mg chl-a m2, and benthic micro-
phases, respectively. The light extinction coefficient, Kd, ranged algal concentrations averaged 57, 195 and 109 mg chl-a m2 in the
from 0.05 to 21 m1 during the open periods, in conjunction with lower, middle and upper reaches, respectively (Fig. 4). The benthic
an increase in silt loading, with the bottom PAR ranging from 7 to (10 mm cores) microalgal biomass was significantly higher than
697 mmol m2 s1 (Fig. 2). Kd decreased during the closed phase, that of the pelagic compartment (one-way ANOVA, p < 0.05).
varying between 0.3 and 3 m1 in response to the settling of the Pelagic primary production ranged from 21 (upper reaches) to 96
sediment. At this stage, bottom PAR ranged from 7 to (middle reaches) mg C m2 h1. When normalized to chl-a (pelagic
50 mmol m2 s1. During the recovery phase, Kd varied between 1 PB), these values ranged from 0.8 (lower reaches) to 4 mg C mg chl-
and 4 m1, while bottom PAR ranged from 2 to 90 mmol m2 s1. a1 h1 (middle and upper reaches) (Fig. 5). Benthic primary pro-
Salinity was highest during the open phase, ranging from 1 duction ranged from 0.06 (lower reaches) to 7 mg C m2 h1 (upper
(upper reaches) to 31 (lower reaches). The closed phase was reaches) and from 0 to 0.34 mg C mg chl-a1 h1 (upper reaches)
marked by low salinity at all three reaches (<1). During the when normalized to chl-a (Fig. 6).
recovery period, salinity ranged from 0.9 (upper) to 2.5 (middle). Regarding the open phase (13 Feb.–5 Mar. 2004), 2 days after
Water temperatures during the closed phase ranged from 20 to breaching, the sub-surface phytoplankton biomass averaged 3, 4
24  C, increasing to a maximum of 33 and 26  C during the open and 5 mg chl-a m2 for the lower, middle and upper reaches,
and recovery phases, respectively. respectively, experiencing a 94% loss in total biomass. A rapid
Molar ratios of pelagic DIN:DIP were significantly higher during
the open phase (1–283) than during the closed (0.01–15) (two-way
70
lower middle upper
600

60
lower middle upper

500
50
Pelagic PB (mg C chl-a-1 h-1)

400
Benthic chl-a (mg m-2)

40

300
30

200 20

100 10

0
0
12 Sept. 03
19 Sept. 03
26 Sept. 03
10 Oct. 03
14 Nov. 03
13 Feb. 04
17 Feb. 04
20 Feb. 04
24 Feb. 04
27 Feb. 04
05 Mar. 04
23 Mar. 04
29 Mar. 04
02 Apr. 04
06 Apr. 04
08 Apr. 04
12 Apr. 04
15 Apr. 04
12 Sept. 03
19 Sept. 03
26 Sept. 03
10 Oct. 03
14 Nov. 03
13 Feb. 04
17 Feb. 04

05 Mar. 04
23 Mar. 04
29 Mar. 04
02 Apr. 04
06 Apr. 04
08 Apr. 04
12 Apr. 04
15 Apr. 04
20 Feb. 04
24 Feb. 04
27 Feb. 04

Months
Months
Fig. 5. Temporal variations in pelagic primary production normalized by chlorophyll-
Fig. 4. Temporal variations in benthic chlorophyll-a (average  SD) at the lower, a (average  SD) at the lower (black bars), middle (white bars) and upper (grey bars)
middle and upper reaches for the closed (solid line, 12 Sept–14 Nov 2003), open reaches. Closed phase (solid line, 12 Sept.–14 Nov. 2003), open phase (dotted line, 13–
(dotted line, 13–27 Feb. 2004) and recovery phases (solid line, 23 Mar.–15 Apr. 2004). 27 Feb. 2004) and recovery phases (solid line, 23 Mar.–15 Apr. 2004).
 A. Anandraj et al. / Estuarine, Coastal and Shelf Science 79 (2008) 599–606 603

1.4 40
lower middle upper

35
1.2

30
Benthic PB (mg C mg chl-a -1 h-1)

Benthic PB (mg C mg chl-a -1 h-1)

1

25

0.8

20

0.6

15

0.4
10

0.2
5

0 0
12 Sept. 03

19 Sept. 03

26 Sept. 03

10 Oct. 03

14 Nov. 03

13 Feb. 04

17 Feb. 04

20 Feb. 04

24 Feb. 04

27 Feb. 04

05 Mar. 04

23 Mar. 04

29 Mar. 04

02 Apr. 04

06 Apr. 04

08 Apr. 04

12 Apr. 04

15 Apr. 04
Months
Fig. 6. Temporal variations in benthic primary production normalized by chlorophyll-a (average  SD) at the lower (black bars), middle (white bars) and upper (grey bars) reaches.
Closed phase (solid line, 12 Sept–14 Nov 2003), open phase (dotted line, 13–27 Feb. 2004) and recovery phases (solid line, 23 Mar.–15 Apr. 2004). Data for the lower and middle
reaches are shown on the primary Y-axis and on the secondary Y-axis for the upper reaches.

temporary build-up of the phytoplankton stock was evident 6 days phase (Tukey’s HSD, p < 0.001). Benthic microalgal biomass levels
after breaching (17 Feb.), ranging from 31 (upper reaches) to ranged from 15 (upper reaches) to 355 (middle reaches) mg m2.
73 mg chl-a m2 (middle reaches) (Fig. 3). For the entire duration of Tukey’s HSD post hoc test showed a significantly higher benthic
the open phase, water-column integrated microalgal biomass microalgal biomass during the closed and recovery phases
ranged from 1 (upper reaches) to 88 mg m2 (lower reaches) (p < 0.001) compared to the open phase. Similarly, Tukey’s HSD
(Fig. 3). The nanophytoplankton fraction dominated the pelagic post hoc test showed a significant decrease in benthic microalgal
biomass (85%) during this period. Tukey’s HSD post hoc analysis biomass from the closed to the open phase (p < 0.05) with a sig-
showed that benthic microalgal biomass had decreased drastically nificant increase from the open to the recovery phase (p < 0.001).
when the estuary breached (p < 0.05) with levels dropping to During the recovery period, pelagic primary production varied
1 mg chl-a m2 2 days after the initial breaching, i.e. a 99% loss of between 5 (upper reaches) and 115 (middle reaches) mg C m2 h1
biomass. A build-up of the benthic microalgal stock was evident 7 and pelagic PB from 0.2 (upper reaches) to 1.5 (middle reach-
days after the second breaching event when benthic biomass es) mg C mg chl-a1 h1. Both maximum and minimum rates of
attained levels of 58 (upper reaches)–136 mg chl-a m2 (middle benthic primary production were recorded in the middle reaches
reaches). For the duration of the open phase (21 days), benthic (0.06–3 mg C m2 h1). Benthic PB ranged from 0 (upper reaches) to
microalgal biomass ranged from 0.8 (lower reaches) to 316 (upper 0.1 mg C mg chl-a1 h1 (upper reaches). Pelagic primary pro-
reaches) mg m2. duction showed no significant differences between stations
Pelagic primary production ranged from 0.8 (upper reaches) to (p > 0.05) but was significantly higher during the closed than the
341 (middle reaches) mg C m2 h1 and pelagic PB from 0.4 (lower open phase (Tukey’s HSD, p < 0.05) only. However, pelagic PB was
reaches) to 59 (upper reaches) mg C mg chl-a1 h1. The maximum significantly higher during both closed and open phases compared
rate of benthic primary production was recorded in the upper to the recovery phase (Tukey’s HSD, p < 0.001). Benthic PB was
reaches (16 mg C m2 h1) and the minimum in the lower reaches significantly higher during the breaching period than in the closed
(0.05 mg C m2 h1). Benthic primary production normalized to (p < 0.05) and recovery phases (Tukey’s HSD, p < 0.001).
chl-a (benthic PB) ranged from 0 (lower and middle reaches) to
35 mg C mg chl-a1 h1 (upper reaches) (Fig. 6). 3.3. Relationships between biomass, primary production
During the recovery phase (23 Mar.–15 Apr. 2004), phyto- and environmental parameters
plankton biomass ranged from 16 (lower reaches) to 112 (lower
reaches) mg chl-a m2 and once again was dominated by nano- From the Principal Component Analysis (PCA), applied to the
phytoplankton (62%). Phytoplankton biomass was significantly benthic and pelagic parameters, factors one (F1) and two (F2)
higher during the recovery and closed phases compared to the open explained approximately 64 and 66% of the total variance,
604 A. Anandraj et al. / Estuarine, Coastal and Shelf Science 79 (2008) 599–606

respectively. In the pelagic region, temperature, salinity and water 4. Discussion

depth were the parameters contributing the highest component
scores of the F1 variance (Fig. 7A), while DIN, DIP and PAR con- The disturbance of the breaching event drastically altered the
tributed the highest component scores of the F2 variance. For the dynamics of both benthic and pelagic microalgae. Following the
benthic region, salinity and temperature contributed the highest breaching of the Mdloti mouth, the open phase stimulated both
component scores of the F1 variance, while pore-water DIP and PAR benthic and pelagic PB but washed out to sea almost the entire
contributed the highest component scores of the F2 variance stock (94–99%) of estuarine microalgal biomass. Benthic PB signif-
(Fig. 7B). icantly increased by almost an order of magnitude during this
During the closed phase, no significant correlations were period compared to the closed phase. Similarly, pelagic primary
observed between primary production and biomass either in the production increased by 108% and pelagic PB by 94%. These high
benthic or the pelagic compartments. During the open phase, rates of autochthonous pelagic primary production were probably
however, pelagic primary production was significantly correlated a consequence of optimal environmental conditions that prevailed
with phytoplankton biomass (r ¼ 0.7; p < 0.01), but no significant during the open phase compared to the previous period. For
correlations were observed between benthic microalgal production instance, the DIN:DIP molar ratios of the water-column and pore-
and biomass (p > 0.05). During the recovery phase, surface (r ¼ 0.8; water increased by 1–2 orders of magnitude well above the
p < 0.01) and bottom (r ¼ 0.6; p < 0.01) primary production sig- Redfield ratio. Pelagic temperature significantly increased to
nificantly correlated to the corresponding phytoplankton biomass. a maximum of 33  C, which is within the optimum range for pri-
However, once again no significant correlations were observed mary production (Blanchard et al., 1996). This was a consequence of
between benthic microalgal production and biomass (p > 0.05). the shallow waters (<1 m) of the open phase, which also brought
Correlation analysis of pooled data (n ¼ 54) showed significant about a favorable light regime for benthic and pelagic primary
correlations between pelagic chl-a and primary production (r ¼ 0.6; production. The shallow conditions of the open phase may there-
p < 0.01) and inverse correlations between pelagic chl-a and ben- fore be largely responsible for the optimal environmental condi-
thic primary production (r ¼ 0.5; p < 0.01). Significant inverse tions for primary production that were observed during this phase.
correlations were also observed between benthic chl-a and benthic Furthermore, the high salinity likely induced flocculation and
PB (r ¼ 0.8; p < 0.01). Correlation analysis of environmental sinking of suspended particles, thereby contributing to an enhanced
parameters with biotic parameters and Principle Component (PC) light regime within the water-column (Santiago, 1991; Gebhardt
scores (pooled data, n ¼ 54) is shown in Table 2. et al., 2005). High rates of benthic and pelagic PB observed during
the optimal open phase indicated an accelerated rate of microalgal
growth (Kirchman, 2002), evident from the rapid, although tem-
porary, build-up of phytoplankton and benthic microalgal biomass
1.0 observed on the 17 and 27 February. However, at the same time
A DIN the ongoing water-column flushing and sediment scouring
PAR reduced the stock of microalgal biomass.
DIP
A previous study at the Mdloti has shown no significant differ-
.5
ences in zooplankton abundance/biomass between the open and
Temperature the closed phases as well as a limited influx of marine fauna during
the open phase (Kibirige et al., 2006). This suggests limited grazing
0.0 pressure of marine fauna during the open phase of the river-
Depth dominated Mdloti. In contrast, the recovery phase promoted the
Salinity build-up of phytoplankton and benthic microalgal biomass but
reduced rates of primary production (PB). The resilience of these
-.5
microalgae to episodic ecosystem disturbances, such as breaching,
was evident following the re-closure of the Mdloti mouth.
After re-closure, mean pre-breaching levels of phytoplankton
Component 2

-1.0 and benthic microalgal biomass were reached 35–40 days follow-
-1.0 -.5 0.0 .5 ing breaching, respectively. The re-closure of the mouth precluded
further losses of microalgae through flushing and scouring, thereby
1.0
promoting biomass accumulation. The mainly flagellated nano-
B PAR
plankton cells, which also dominated this phase, can propel
Pore water DIP
themselves towards zones of greater light intensities (Kirk, 1994)
.5 and so may attain a much higher biomass than micro-
phytoplankton. Furthermore, the high surface area to volume ratio
of nanoplanktonic algae would allow them to compete more effi-
Salinity
Depth ciently in the reduced light conditions that occurred during the
0.0
recovery phase. The maximum concentration of phytoplankton
Pore water DIN Temperature
biomass was actually recorded 6 days after mouth re-closure and
benthic microalgal biomass peaked at 355 mg chl-a m2 (middle
-.5 reaches), 20 days after re-closure of the mouth. The biomass of
phytoplankton was generally lower than that of the benthic
microalgae, as recorded in previous studies (Nozais et al., 2001;
Perissinotto et al., 2003; Anandraj et al., 2007). At the onset of the
-1.0 recovery phase, benthic PB significantly decreased (two-way
-1.0 -.5 0.0 .5 1.0
ANOVA, p < 0.001) as a consequence of a drop in pore-water
Component 1
DIN:DIP molar ratios, water temperature and bottom PAR. Although
Fig. 7. Principal Component Analysis ordination of the physico-chemical parameters pore-water nutrient loading was always above the Redfield ratio
for the pelagic (A) and benthic (B) regions of the Mdloti Estuary. (16:1), benthic PB remained low because of a poor light regime at
 A. Anandraj et al. / Estuarine, Coastal and Shelf Science 79 (2008) 599–606 605

Table 2
Pearson r and partial correlation coefficients in brackets of pelagic primary production (PPP), pelagic production normalized by biomass (PPPB), benthic primary production
(BPP) and benthic primary production normalized by biomass (BPPB), pelagic principal components (pelagic PC 1 and 2) and benthic principal components (benthic PC 1 and 2)
with environmental variables (pooled data, n ¼ 45) in the Mdloti Estuary. ***p < 0.0001, **p < 0.005, *p < 0.05

Pelagic Chl-a Benthic Chl-a PPP PPPB BPP BPPB

Mouth state 0.3** (0.5)** 0.3** (0.4)* 0.2 (0.5*) 0.6** (0.7***) 0.06 (0.04) 0.2 (0.05)
Temperature 0.4** (0.2) 0.5** (0.3) 0.3* (0.02) 0.1 (0.05) 0.1 (0.05) 0.5** (0.04)
Salinity 0.2 (0.1) 0.2 (0.3) 0.2 (0.1) 0.09 (0.1) 0.1 (0.1) 0.2 (0.01)
Pelagic DIN 0.6** (0.5)** 0.5** (0.5)** 0.4** (0.5)** 0.3 (0.4) 0.1 (0.1) 0.4** (0.5)*
Pelagic DIP 0.1 (0.2) 0.1 (0.7) 0.3 (0.2) 0.1 (0.1) 0.02 (0.1) 0.1 (0.1)
Pore-water DIN 0.3* (0.1) 0.2 (0.1) 0.4** (0.5)** 0.5** (0.5)* 0.3 (0.4)* 0.1 (0.4)*
Pore-water DIP 0.4** (0.1) 0.4** (0.3)** 0.3* (0.4) 0.1 (0.1) 0.02 (0.3) 0.1 (0.3)
PAR 0.4** (0.3)* 0.5** (0.5)** 0.5** (0.6)** 0.5** (0.5)** 0.4** (0.5)* 0.6** (0.6)*
Kd 0.3* (0.2) 0.3* (0.1) 0.1 (0.4*) 0.5** (0.5**) 0.2 (0.2) 0.4** (0.2)
Pelagic PC score 1 0.6** (0.5) 0.4** (0.1) 0.5** (0.4)* 0.1 (0.4) 0.1 (0.1) 0.5** (0.1)
Pelagic PC score 2 0.4** (0.1) 0.5** (0.2) 0.03 (0.1) 0.2 (0.01) 0.1 (0.1) 0.4** (0.1)
Benthic PC score 1 0.6** (0.01) 0.5** (0.02) 0.4** (0.1) 0.05 (0.1) 0.2 (0.1) 0.5** (0.1)
Benthic PC score 2 0.1 (0.02) 0.1 (0.03) 0.2 (0.1) 0.1 (0.2) 0.3 (0.2) 0.2 (0.1)

the sediment surface. Alternatively, the slurry technique used may in previous studies, the main controlling factors of primary pro-
have induced photoinhibition of shade adapted benthic microalgae. duction are light (Alpine and Cloern, 1988; Barranguet et al., 1998;
Similarly, these sub-optimal conditions significantly lowered Perkins et al., 2001), temperature (Blanchard et al., 1996; Guarini
pelagic PB compared to the open phase (Tukey’s HSD, p < 0.001). et al., 1997; Morris and Kromkamp, 2003) and nutrients (Sundbäck
During the recovery phase, both pelagic and benthic PB significantly et al., 2004). These environmental parameters influence primary
decreased, as the corresponding biomass increased. This may be production both individually and collectively in a synergistic way
attributed to re-suspended phytoplankton cells, which contributed (Kocum et al., 2002; Anandraj et al., 2007).
to an increase in Kd and subsequently reduced light availability. In conclusion, the recovery of estuarine primary production and
Alternatively, the decrease in primary production may be the biomass following a breaching event seems to be primarily influ-
consequence of a decline in growth because of reduced nutrient enced by the state of the mouth, which in turn influences envi-
availability. This has been shown in a previous study (Han and ronmental parameters. Optimum light, temperature and nutrient
Furuya, 2000). The recovery phase may therefore represent the levels of the open phase stimulate microalgal primary production,
period when microalgal primary production returns to pre- but continuous flushing and sediment scouring preclude the build-
breaching levels but not necessarily to maximum levels. up of microalgal biomass. Accelerated rates of primary production
During this study, the state of the mouth was primarily re- observed during the open phase stimulated growth of the seed
sponsible for regulating the recovery of microalgal primary pro- community of microalgae, replenishing lost stocks only upon re-
duction and biomass within the Mdloti Estuary. The area has an closure of the estuary’s mouth. The resilience of these benthic and
energetic wave climate with high rates of long-shore and cross- pelagic microalgae following a breaching event suggests that
shore sediment transport and steep, reflective beaches. This gives availability of food for benthic and pelagic grazers may be recon-
rise to a high berm, about 2 m above high tide levels. After stituted almost immediately following the re-closure of the estuary.
breaching, the rebuilding of the berm is controlled mainly by cross- Monitoring the recovery of a TOCE is complex, as the primary
shore sediment transport processes and the magnitude of the river indicators such as biomass, primary production and mouth state
flows (Stretch and Parkinson, 2006). The breaching characteristics may not necessarily recover in synchrony.
for this estuary are discussed by Stretch and Parkinson (2006).
During the open phase, tidal exchange flows are strongly influ- Acknowledgements
enced by the high wave run-up associated with the steep beach
slope. As the sandbar is regenerated, these exchange flows gradu- This project was supported by a grant from a Joint Venture
ally reduce and water levels within the estuary re-stabilize at levels Project between the National Research Foundation (NRF, Pretoria)
above mean sea level. The duration of the open phase (and time and the Department of Environmental Affairs and Tourism (DEAT).
required to rebuild the berm) may be very short (about 1 week) if We are grateful to Mark Olbers for his invaluable assistance in the
the river flows are low but can also be significantly extended by field. We thank two anonymous referees for their constructive
sustained high flows which contribute to scouring accumulated comments on the manuscript.
marine sediments from the mouth.
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