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Relationships between Zoo- and Phytoplankton in a Warm-temperate, Semi-permanently Closed Estuary, South Africa
Estuarine, Coastal and Shelf Science (2000) 51, 1–11 doi:10.1006/ecss.2000.0613, available online at http://www.idealibrary.com on
Relationships between Zoo- and Phytoplankton in a Warm-temperate, Semi-permanently Closed Estuary, South Africa R. Perissinottoa, D. R. Walkerb, P. Webbc, T. H. Wooldridgec and R. Ballyd a
School of Life & Environmental Sciences, University of Natal, Durban 4041, South Africa Department of Plant Sciences, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa c Department of Zoology, University of Port Elizabeth, P.O. Box 1600, Port Elizabeth 6000, South Africa d Department of Zoology, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa b
Received 23 April 1999 and accepted in revised form 4 March 2000 Seasonal surveys were carried out in the shallow, well-conserved temporarily open Nyara Estuary in the Eastern Cape, South Africa. Although temporarily open estuaries constitute over 70% of estuaries in South Africa, few data are available on the structure and functioning of these systems in the region. The main aim of the study was to test the hypothesis that owing to irregular nutrient input, temporarily open estuaries may exhibit poorly-developed pelagic food webs, with low phytoplankton and pelagic biomass in general. Results from the investigation indicate that phytoplankton biomass is generally low, and dominated by pico and nanophytoplankton, with almost total absence of diatoms. This may be explained in terms of the regenerated, rather than new, nutrient pool that is available to phytoplankton as a result of the semipermanently closed nature of the estuary. Chlorophyll a levels never exceeded 4·1 mg m 3. However, low levels of phytoplankton biomass were in contrast to relatively large stocks of zooplankton, which attained maximum levels of about 2 g (dry weight) m 3. Thus, there is an imbalance between the biomass of the primary producers and that of the consumers. In order to satisfy the zooplankton energy budget, either phytoplankton production rates are extremely high or a substantial proportion of their food demands must be met through utilization of alternative sources, such as detritus, protozoans and microphytobenthos. It is suggested that microphytobenthos in particular may play a major role in this regard because of the prevailing good conditions for its growth in this type of ecosystem. Microbenthic chlorophyll a concentrations in the Nyara Estuary are in the upper range of values measured in South African estuaries, with an average of ≅190 mg m 2. Further studies are needed to investigate the ability of the dominant species of zooplankton to ingest and assimilate benthic microalgae, particularly during the day when most species remain in close association with the substratum. 2000 Academic Press Keywords: plankton; detritus; microheterotrophs; microphytobenthos, temporarily open estuaries, South Africa
Introduction Of the 250 estuaries in South Africa, 182 (or 73% of the total) are currently classified as temporarily open/ closed (Whitfield, 1995). During the dry season and under low river flow conditions, these systems close off from the sea by a sandbar that forms at the mouth. Following periods of high rainfall and freshwater runoff, the water level inside the estuary may rise suddenly or gradually until it exceeds the height of the sandbar at the mouth (Whitfield, 1992; Wooldridge & McGwynne, 1996). Breaching then occurs and the water level drops very rapidly, often exposing large areas of substratum which had been submerged for long periods and colonized by a rich community of plants and animals. River conditions may briefly dominate the estuary during breaching events, but the 0272–7714/00/070001+11 $35.00/0
sandbar at the mouth is rapidly regenerated by longshore sand movement in the surf zone (usually within weeks). This leads to another closed phase during which seawater inflow is generally provided by wash-over at the peak of the spring tide or during storm surges. Although many local estuaries naturally close off from the sea for varying periods, increasing retention of freshwater by dams for domestic, industrial and agricultural purposes reduces the frequency and duration of mouth opening (Reddering & Rust, 1990; Cooper et al., 1999). This affects negatively the sediment scouring ability of estuaries and their capacity of eliminating build-ups of pollutants (Begg, 1984a; Whitfield, 1992). The long residence time of water and sediments in these estuarine basins makes their benthic, pelagic and nekton communities very 2000 Academic Press
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vulnerable to environmental degradation, compared to their counterparts in permanently open estuaries. This is compounded by the fact that temporarily open estuaries are playing an increasingly large role in the economic development of the country, either as sites of industrial/agricultural development or as ecotourism and fishing resorts. For the vast majority of South Africa’s temporarily open estuaries no information is presently available on physicochemical and biological properties (Whitfield, 1995). Of the four systems for which data are available, most is of biological nature involving taxonomic, recruitment and stock assessment studies of macroorganisms, particularly fish, molluscs, crustaceans and seagrasses of economic and conservation interest (Begg, 1978; Day, 1981; Begg, 1984a, 1984b; Wooldridge & McGwynne, 1996; Whitfield, 1996; Allanson & Baird, 1999). In permanently open estuaries, regular seawater and freshwater inflows are normally capable of supporting a large phytoplankton biomass and a well-developed pelagic food web (Adams & Bate, 1999). This is mainly associated with the steady supply of nutrients and the maintenance of stable stratified conditions (Hilmer & Bate, 1990; Allanson & Read, 1995; Jerling & Wooldridge, 1995a; Adams & Bate, 1999). Conversely, temporarily open estuaries are often dominated by submerged macrophytes that are able to take advantage of the conditions prevailing in these systems. These include low turbidity and current levels as well as a more stable sediment and salinity environment, and also the large nutrient pool available in the substratum (Adams et al., 1999). The implications of these major differences for the trophic functioning of temporarily open estuaries have not been investigated yet and could have important consequences for the management strategies that are currently applied to these ecosystems (Morant & Quinn, 1999). Our study was specifically designed with the aim of looking at the composition and seasonal variations of the stocks at the lower levels of the food web of a temporarily open estuary, in order to test the hypothesis that the plankton component of these systems may indeed be under-developed relative to that of permanently open systems. The study focuses specifically on the biomass, abundance and broad taxonomic composition of the zoo- and phytoplankton communities observed in the Nyara Estuary during 1997. Materials and methods Four 3-day surveys were carried out in the Nyara Estuary, a semi-permanently closed system on the
Eastern Cape coast of South Africa (Figure 1). The surveys took place in March, May, September and November 1997. Depth, salinity and temperature were measured at the surface, in the middle and in the near-bottom layers using a Hydrolab H20 Multiprobe. Irradiance levels (PAR) were measured at 50 cm depth intervals with a LI-COR Li-193SA Spherical Quantum Sensor. Samples for chlorophyll a (chl a) and phaeopigment determination were collected using a Van Dorn water sampler. Aliquots of 200 ml were filtered sequentially onto a 20 m Nitex filter, a 2·0 m Millipore TTTP and a GF/F Whatman glass fibre filter, in order to fractionate the total phytoplankton pigment biomass into micro, nano and pico size-fractions, respectively (Sieburth et al., 1978). Pigments were extracted in 90% acetone and fluorescence readings were taken using a Turner 111 or a Turner Designs 10-AU Fluorometer, before and after acidification (Yentsch & Menzel, 1963; Holm-Hansen et al., 1965). Chl a and phaeopigment concentrations were then obtained using the formulae of Parsons et al. (1984) as modified by Conover et al. (1986). The same water sampler was also used to collect phytoplankton/protozoan samples (250 ml) for microscopic analysis. These were immediately fixed with 2% hexamine-buffered formalin and the major taxa were later identified and counted in the laboratory under an inverted microscope, after sedimentation in 10 ml chambers (Hasle, 1978). While regular microphytobenthic chlorophyll a measurements were not made during the 1997 survey, representative samples were collected at the beginning of November 1998 at a time when the Nyara Estuary was isolated from the sea. Samples were taken using a 20 mm internal diameter corer and the chlorophyll of the upper 10 mm of sediment was extracted in 30 ml of ethanol. Chlorophyll a concentrations were then determined by HPLC following the protocol outlined in Adams and Bate (1999). Zooplankton samples were collected using a 4·5 m flat-bottomed boat. Two WP-2 nets, one fitted with 90 m and the other with 200 m mesh, were towed in parallel on each side of the boat at a speed of about 0·5–1·0 knot and at a depth of 5–10 cm below the surface. Both nets were fitted with Kahlsico 005WA130 flowmeters. Volume filtered ranged between 3 and 8 m3, with an average of approximately 5 m3 per haul. In the laboratory, subsamples for identification and enumeration were drawn off the sample which had been suspended in a 1–10 l solution, depending on the concentration of organisms. Using a 25 cm long glass tube of 10 mm diameter, duplicate subsamples of 20 ml each were withdrawn after penetrating the entire depth of the suspension and while
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South Africa DURBAN
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F 1. The Nyara Estuary with the position of the seven stations occupied during the study.
preventing settlement through constant stirring (Perissinotto & Wooldridge, 1989; Jerling & Wooldridge, 1995a). The coefficient of variation (CV) between subsamples obtained in this way was consistently below 15% and averaged about 6%.
Estimates of zooplankton biomass were obtained both volumetrically and gravimetrically, after the removal of large detrital particles under a dissecting microscope. In the first instance, the displaced volume of each sample was measured with the
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F 2. Vertical profiles of salinity (a) and temperature (b) along the Nyara Estuary during the four surveys undertaken in 1997. Salinity was measured using the Practical Salinity Scale and temperature is expresssed in C.
vacuum extraction technique, involving the removal of both solution and interstitial fluids (Beers, 1976). Wet weight (WW) was the main gravimetric parameter used, as this does not involve the destruction of the sample or part of it. However, in order to compare our results with most of those obtained in other studies, the total dry weight (DW) was also measured for several samples, generally those with high zooplankton densities. In this case, only subsamples of one-fifth to one-half of the total were processed. Where no DW could be measured directly, this was derived using the general regression equation between DW and settled volume (SV) obtained by Grindley and Wooldridge (1974), mg (DW)=18·6ml (SV). WW was obtained by weighing the sample immediately after the removal of solution and interstitial liquid under gentle vacuum (<200 mm Hg). Samples for DW measurement were oven-dried for 36 h at 60 C prior to weighing (Pakhomov & Perissinotto, 1996).
Results Physicochemical environment Prior to our first survey, in March 1997, the Nyara Estuary had been closed since December 1996. During 1996, mouth breaching occurred on two occasions due to heavy rainfalls in November and December (Bosbokstrand Private Nature Reserve, pers. comm.). During 1997, the combined effects of runoff and overwash from the sea resulted in a progressive increase in the average depth of the estuary. This increased from about 1·5 m in March–May to 2·2 m in September. Heavy rains caused the mouth to open and the estuary to drain to a maximum depth of 1 m on the 28 of November (Figure 2). In March 1997, the estuary exhibited a horizontal salinity gradient in surface waters [Figure 2(a)], but below 1 m depth salinity levels were consistently high (26·5–31·5). A strongly stratified water-column was
Zoo- and phytoplankton relationships
Phytoplankton and microphytobenthos In terms of total numerical abundance, the phytoplankton community was dominated by small flagellates of <2 m in size. The largest cells (>10 m) were mainly dinoflagellates, Protoperidinium spp. and unidentified species of 10-15 m size. Diatoms were present in very low numbers and diversity throughout the water-column (Walker et al., submitted). Total phytoplankton chl a concentration exhibited a maximum of 4·1 mg m 3 in May 1997 and a minimum of 0·007 mg m 3 in November (Figure 3). Average values were consistently low, with the highest
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observed in May, with salinity values ranging from 23 at the surface to over 30 at the bottom. Due to the lack of freshwater inflow during the dry winter months, no horizontal gradient in salinity was observed during this period. In September, the bottom salinity decreased to a maximum of about 27 [Figure 2(a)], while surface levels showed a diffuse gradient (24 to 22) from the mouth to the head. The November survey coincided with the flood event, which caused the opening of the mouth and the flushing of the estuary [salinity c0·5, Figure 2(a)]. High water temperatures of 28–30 C were recorded in March [Figure 2(b)]. By May, values had dropped by an average of about 10 C and remained much the same in September, with warmer waters found higher up in the estuary on both occasions. Because of the flooding, water temperature was uniform in November, showing only a slight warming by about 1 C as the water moved through the estuary [Figure 2(b)]. Surface irradiance levels (PAR) ranged from a maximum of about 2300 mol m 2 s 1 to minima of about 550 mol m 2 s 1, depending on weather conditions and time of the day. During the closed phase of the estuary, average values of the light attenuation coefficient (k) were low, in the range of 0·42–1·49 m 1. The lowest levels were recorded near the mouth (Stns 1 and 2) and the highest at the head of the estuary (Stns 6 and 7). Given the shallow depth, this resulted in high irradiance been recorded at the bottom, where light intensities were normally 30–60% of surface levels. PAR values of less than 300 mol m 2 s 1 were recorded at the bottom only on two occasions. However, during the flood in November the penetration of irradiance in the water was virtually non-existent due to the high density of suspensoids. On this occasion, no PAR could be detected at 15–20 cm depth and extinction coefficients attained levels of 8–14 m 1.
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F 3. Total phytoplankton chlorophyll a concentration (mg m 3) measured in the Nyara Estuary during March, May, September and November 1997.
in March (1·180·58 SD, N=11) and the lowest in November (0·0150·009 SD, N=4). In March, the highest levels were recorded near the bottom, in May in the middle layer and in September near the surface, while during the November flood chl a levels were low throughout the water-column. Chl a values decreased horizontally from the mouth to the head in March, while the opposite trend was observed in May and September (Figure 3). The distribution of chl a into <2 m (pico-), 2-20 m (nano-) and >20 m (micro-) size-classes varied with season, and was characterized by the dominance of the smaller classes. Picoplankton dominated the total chl a stock in May, with 65·427% (SD) of the total, and nanoplankton likewise in September (57·117% SD) and November (67·515% SD). Microplankton contributed substantially to the total only in March, with levels close to 50% of the total chl a stock. Benthic microalgae chl a concentration (measured in November 1998) was uniform at the three stations sampled. Mean values ranged from 170 mg m 2 at Station 2 to about 200 mg m 2 at Stations 1 and 4. The average value for the three stations was 18916·5 SD, N=6.
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Zooplankton and protozoans The zooplankton community was composed largely of micro-sized (<200 m) larval stages during daytime. These included copepod nauplii, barnacle cypris, and gastropod veligers (Table 1). In the night-time samples, on the other hand, the calanoid copepods Pseudodiaptomus hessei and Acartia natalensis were dominant, and an unidentified species of Halicyclops sp. and a large variety of harpacticoid copepods, comprising at least 12 different species, were also abundant (Table 1). Polychaetes, especially Prionospio sp., the cumacean Iphinoe truncata and amphipods were also present in substantial numbers, and occasionally dominated the night-time samples (Table 1). During the September survey only, an unidentified species of Anthomedusae (approximately 200– 800 m diameter) was in bloom phase and exhibited concentrations of up to 29·4103 ind m 3. Maximum total zooplankton densities were found in September with about 6·5106 ind m 3. Minima occurred at the time of the November flood with 3·8104 ind m 3. Zooplankton biomass in the estuary varied from a minimum of 19·2 mg wet weight (WW) m 3, during daytime in May, to a maximum of 15·2 g WW m 3 during night-time in September (Figure 4). Average night-time values were 4–35 times higher than daytime values. Displaced volumes (DV) ranged from 0·058 ml m 3, in May daytime samples, to 18·8 ml m 3 in September night-time samples. Similarly, the corresponding levels of dry weight (DW) exhibited minima and maxima of 1·08 mg m 3 and 2·03 g m 3 respectively. The highest biomasses were found in the middle/upper reaches of the estuary in March, May and November but shifted towards the mouth during September (Figure 4). Protozoan counts in the samples were low, with maxima of about 14103 cells l 1 in May and minima of 8·6103 cells l 1 in March. The most abundant groups were the nanoflagellates, aloricate ciliates and tintinnids. Details on the abundance and carbon biomass of these groups during the survey period are reported elsewhere (Walker et al., submitted).
Discussion Temporarily open estuaries lack the steady supply of macronutrients generally observed in permanently open estuaries. In open systems, this is provided by the regular input of nutrient-rich freshwater, by tidally-driven advection from the sea and by resuspension of benthic regenerated nutrients (Malone et al.,
1988; Adams & Bate, 1994; Allanson & Read, 1995). Nutrient deficiency in temporarily open estuaries may limit the productivity of phytoplankton, despite the ideal conditions of water column stratification and light intensity that are often found in these systems (Adams & Bate, 1999). Phytoplankton biomass (as chl a) measured during the Nyara study exhibited a maximum of 4·1 mg m 3 in May and a minimum of 0·007 during the November flood (Figure 3). The overall average of the four surveys was 0·440·53 (SD) mg m 3. These are among the lowest values recorded for any South African estuary (Hilmer & Bate, 1991; Campbell et al., 1991; Allanson & Read, 1995; Adams & Bate, 1999). In contrast, the maximum zooplankton dry mass levels measured in the Nyara Estuary are approximately an order of magnitude higher than the average values recorded in the most productive estuaries of the Eastern Cape (i.e. Sundays and Gamtoos Estuaries, Wooldridge, 1999). The average value over the total period of the investigation was 150 mg m 3, which is 2–5 times higher than the average values reported by Wooldridge (1999) for the most (]80 mg DW m 3) and the least (]30 mg DW m 3) productive South African estuaries, respectively. It must be stressed, however, that sampling in the Nyara Estuary took place only seasonally and on four occasions. The zooplankton data show a large variation, with concentrations ranging from the highest ever recorded in South Africa to almost the lowest (Table 1). Clearly there are aperiodic boosts in growth followed by periods of low activity. This indicates that these small systems generally fluctuate between extremes and may lack the buffering capacity observed in larger volume systems, where a relative stability is maintained in the zooplankton community throughout the year. If sampling had been carried out more frequently, it is likely that average concentrations could have been less skewed towards large values. Nevertheless, even taking this potential bias into account the figures for zooplankton biomass and abundance are still very high compared to the phytoplankton stock of the estuary. It is possible that part of this disparity may be accounted for by the higher turnover rate of phytoplankton, compared to zooplankton. Unfortunately, no measurements of primary production rates could be made during this study. Estimates from similar systems in the region are few and show a wide range of variation, from 32 to 147 mg C m 2 h 1 (Campbell et al., 1991). On an annual basis, these rates may be enough to support the energy requirements of the zooplankton community. However, the large shortterm fluctuations observed in the Nyara Estuary may result in temporal imbalances between pelagic
Pseudodiaptomus hessei Acartia natalensis Oithona spp. Oncaea spp. Halicyclops sp. Cyclopoids spp. Harpacticoids spp. Copepod nauplii Barnacle cypris Amphipod juveniles Iphinoe truncata Anthomedusae Prionospio sp. Veligers larvae Nematodes
Taxon
14 8607420 11 2987413 21267 10·910·9 1429609 596315 58481332 34 0807488 58473535 830366 677410 00 12061107 270184 23·312·8
AverageStd error
8 March 1997
19·5 13·1 0·28 0·01 1·87 0·78 7·66 44·6 7·66 1·09 0·89 0 1·58 0·35 0·03
% Total 50582051 12·58·73 3·712·32 0·580·29 1245544 77·742·6 22 7099659 39261427 697295 12688·7 18811528 00 74372921 1822643 14·411·1
AverageStd error
24 May 1997
11·1 0·03 0·01 0·01 2·74 0·17 50·1 8·64 1·53 0·28 4·14 0 16·4 4·01 0·03
% Total 385 268241 656 81143557 2·130·87 00 19 41810 917 75222929 41 10715 013 205 00953 359 27561362 357261 7·045·13 15 6252202 32441657 31461603 382249
AverageStd error 53·1 1·24 0·01 0·01 2·97 1·15 6·29 31·4 0·42 0·05 0·01 2·39 0·49 0·48 0·06
% Total
6 September 1997
39·453·6 0·830·59 57·166·7 87·983·8 518302 162108 33831006 28·653·6 1·080·96 1053308 10·88·03 00 196204 00 133249
AverageStd error
0·72 0·01 1·05 1·61 9·49 2·98 61·9 0·52 0·01 13 8 0·19 0 3·58 0·01 2·44
% Total
29 November 1997
T 1. Average abundance (no. m 3) and percent contribution of the most important components of the zooplankton community of the Nyara Estuary during 1997. Taxa were selected on the basis of their contribution to the total counts with >1% on at least one sampling occasion
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Zooplankton biomass (wet weight mg m–3)
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F 4. Mesozooplankton biomass, in units of wet weight (WW) m 3, in the Nyara Estuary during March, May, September and November 1997. Note the change of scale in the y-axis by an order of magnitude for the September data. Open bars: WW day; closed bars: night.
primary producers and consumers. This is likely to have important implications for the trophic functioning of the entire ecosystem. Assuming a general conversion factor of chlorophyll a to carbon of about 50 (Atkinson & Shreeve, 1995) and a zooplankton carbon content of C=47·1, %DW=42·6 (Ikeda & Bruce, 1986), the phytoplankton stock of the Nyara Estuary would have been able to support all the energetic requirements of the
zooplankton community only during the March and May surveys. During these periods, the estimated phytoplankton:zooplankton carbon ratios were approximately 1·64 and 3·16, respectively. However, the situation was reversed during September and November, when the ratios were 0·013 and 0·11 respectively. This implies that the available phytoplankton could at most have supplied a ration of 1·29% in September and 10·7% in November of body carbon per day to the local zooplankton. While these levels may have been just enough to sustain the basic metabolic activity of zooplankton organisms, it is very unlikely that they were sufficient to support their energy demands for growth, molting and reproduction. A recent review of the average daily rations measured in calanoid copepods (Mauchline, 1998), shows that over 85% of them are >10% body C day 1 (x=51·952·1 SD, N=79), with values below this reported almost exclusively in cold, high latitude waters (Ba˚ mstedt et al., 1991; Froneman et al., 1996). It seems most likely then, at least during September and November, that the Nyara zooplankton community was heavily supplementing its diet with other food sources. Because of the size constraints imposed by ingestion processes, there are only three options that can be considered to have played a major role at the time: detritus, microheterotrophs and microphytobenthos. Detritus and microheterotrophs are two components that are generally tightly linked in estuarine ecosystems. In the Nyara Estuary, dead and decomposing plant matter was noticeable throughout the water column. The high level of plant detritus could also be identified from the low chlorophyll:phaeopigment ratio. Only during the March survey was this ratio >1, with an average value of 2·250·69 (SD). Otherwise, the ratio was well below 1 both during May (x=0·170·09 SD), September (x=0·430·22 SD) and November, when the lowest average value of 0·060·02 (SD) was recorded (Walker et al., pers. comm.). The riparian vegetation of the estuary contributes the bulk of the detritus and is composed of dense afromontane forests and saltmarsh plants (Morant, in press). Detritus of macrophytic origin has often been reported as remaining virtually unutilized by estuarine zooplankton (Mann, 1988; Poulet, 1983; Jerling & Wooldridge, 1995b; Schlacher & Wooldridge, 1998). Microbial heterotrophs, particularly bacteria, are on the other hand capable of digesting the fibre material and other refractory carbon compounds. Although some zooplankton species are known to utilize bacteria directly (Poulet, 1983), in most cases only a minor proportion of zooplankton carbon demand is
Zoo- and phytoplankton relationships
met through their direct assimilation in the gut (Boak & Goulder, 1983; Hansen & Bech, 1996). More often, however, it is the protozoans that are able to make full use of the bacterial biomass developing on the detritus (Heip et al., 1995). Protozoans are then in turn preyed upon by larger zooplankton, within the ‘ microbial loop ’ (Azam et al., 1983; Stoecker & Capuzzo, 1990; Gifford, 1993). In the Nyara Estuary, ciliates and flagellates exhibited average cell concentrations ranging from 8·6103 cells l 1 in March to 14103 cells l 1 in May and 13103 cells l 1 in September. These concentrations are not regarded as very high (Heip et al., 1995), nevertheless, they may have been able to support a substantial proportion of the energy demands of mesozooplankton (Stoecker & Capuzzo, 1990; Fessenden & Cowles, 1994). Also, protozoan abundance could have been underestimated significantly during this work, mainly because of fixation problems. Losses of up to 40% of the total number of ciliates have been recorded in samples preserved in formalin (Kemp, 1994). The third potential source of food for the rich zooplankton community observed in the Nyara Estuary may have been the microphytobenthos. This is an algal component that is usually linked with meiobenthos feeding but is not considered among the important sources of food for the pelagic food web of permanently open, tidal estuaries (Soetaert et al., 1994; Heip et al., 1995). There are, however, a number of features of temporarily open estuaries that need to be considered in this regard, as they may suggest exploring some new pathways of trophic functioning and bentho-pelagic coupling. The positive ratio of euphotic depth to total depth of many estuaries, contributes to the high productivity rates of benthic microalgae which are observed at all seasons of the year (Hilmer, 1990). A survey of Cape estuaries has shown that in most systems benthic microalgal biomass is 2–3 orders of magnitude higher than the phytoplankton (all values standardized to m2 units), with highest levels recorded in temporarily open systems (Whitfield, 1989; Adams & Bate, 1994, 1999). Here, during the closed phase, water-column depths are usually very shallow and sediment disturbance by water currents is minimal, thus providing ideal conditions for growth. Being available all year round, benthic microalgae represent an important food source for benthic grazers and demersal fish (Masson & Marais, 1975; Whitfield, 1989). The close interaction that many vertically-migrating zooplankton species have with the substratum of these estuaries, suggest that this benthic source may be potentially important to the pelagic subsystem too (cf. also Hart, 1977).
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Chlorophyll a concentrations in the upper 10 mm of the substratum of the Nyara Estuary are in the upper range of values recorded in South African estuaries (Fielding et al., 1988; Whitfield, 1989; Adams & Bate, 1999), with maxima of 200 mg m 2 and an average of 18916·5 SD mg m 2. Thus, when compared to phytoplankton chlorophyll, benthic chlorophyll levels are about 2–4 orders of magnitude higher than those recorded in the watercolumn. This probably reflects the optimal conditions in irradiance and sediment stability that are found through most days of the year in this semipermanently closed system. During the close phase, photosynthetically available radiation (PAR) levels at the bottom of the estuary were in the range of 30–60% of surface values and above 300 mol m 2 s 1. When considering the marked diurnal migrations that the zooplankton of this and similar estuaries undergo, it seems reasonable to expect that during much of the daytime (when animals avoid the water-column and are in contact with or just above the substrate) grazing on this rich benthic microalgae resource is not only possible but highly likely. Aknowledgements This study was sponsored by the National Research Foundation (NRF, Pretoria). We wish to thank Mr J. Jemaar, Mr F. M. Ngcongca and Mr E. N. Nkoane of the Department of Zoology, University of Fort Hare (Alice), as well as students X. C. Thwala, V. Sajini, S. Pheeha, M. Zatu, M. Njili and H. N. Gunguta for their invaluable help with field work and laboratory analyses. Dr J. Adams of the Department of Botany, University of Port Elizabeth, is thanked for carrying out the HPLC measurements of microphytobenthic chlorophyll concentration and Ms V. Meaton of the Department of Zoology & Entomology, Rhodes University (Grahamstown) for identifying and counting the zooplankton taxa. We are also grateful to the Management of the Bosbokstrand Private Nature Reserve for allowing the use of their facilities during the field surveys. References Atkinson, A. & Shreeve, R. S. 1995 Response of the copepod community to a spring bloom in the Bellingshausen Sea. Deep-Sea Research 42, 1291–1311. Adams, J. B. & Bate, G. C. 1994 The freshwater requirements of estuarine plants incorporating the development of an estuarine decision support system. Water Research Commission (RSA), Report No. 292/1/94, 151 pp. Adams, J. B. & Bate, G. C. 1999 Primary producers: estuarine microalgae. In Estuaries of South Africa (Allanson, B. R. & Baird, D., eds). Cambridge University Press, Cambridge, pp. 91–100.
10 R. Perissinotto et al. Allanson, B. R. & Baird, D. 1999 Estuaries of South Africa. Cambridge University Press, Cambridge. Allanson, B. R. & Read, G. H. L. 1995 Further comment on the response of south east coast estuaries to variable freshwater flows. Southern African Journal of Aquatic Sciences 21, 56–71. Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A. & Thingstad, F. 1983 The ecological role of water-column microbes in the sea. Marine Ecology Progress Series 10, 257–263. Ba˚ mstedt, U., Eilertsen, H. C., Tande, K. S., Slagstad, D. & Skjoldal, H. R. 1991 Copepod grazing and its potential impact on the phytoplankton development in the Barents Sea. Polar Research 10, 339–353. Beers, J. R. 1976 Determination of zooplankton biomass. In Zooplankton Fixation and Preservation (Steedman, H. F., ed.). Monographs on Oceanographic Methodology, no. 4, UNESCO, Paris, pp. 35–84. Begg, G. W. 1978 The estuaries of Natal. Natal Town and Regional Planning Report, Vol. 41, Pietermaritzburg, 657 pp. Begg, G. W. 1984a The estuaries of Natal, Part 2. Natal Town and Regional Planning Report, Vol. 55, Pietermaritzburg, 631 pp. Begg, G. W. 1984b The comparative ecology of Natal’s smaller estuaries. Natal Town and Regional Planning Report, Vol. 62, Pietermaritzburg, 182 pp. Boak, A. C. & Goulder, R. 1983 Bacterioplankton in the diet of the calanoid copepod Eurytemora sp. in the Humber Estuary. Marine Biology 73, 139–149. Campbell, E. E., Knoop, W. T. & Bate, G. C. 1991 A comparison of phytoplankton biomass and primary production in three east Cape estuaries, South Africa. South African Journal of Science 87, 259–264. Conover, R. J., Durvasula, R., Roy, S. & Wang R. 1986 Probable loss of chlorophyll-derived pigments during passage through the gut of zooplankton and some of the consequences. Limnology and Oceanography 31, 878–887. Cooper, A., Wright, I. & Mason, T. 1999 Geomorphology and sedimentology. In Estuaries of South Africa (Allanson, B. R. & Baird, D., eds). University Press, Cambridge, pp. 5–25. Day, J. H. 1981 Estuarine Ecology with Particular Reference to Southern Africa. AA Balkema, Cape Town, 411 pp. Fessenden, L. & Cowles, T. J. 1994 Copepod predation on phagotrophic ciliates in Oregon coastal waters. Marine Ecology Progress Series 107, 103–111. Fielding, P. J., Damstra, K. St-J. & Branch, G. M. 1988 Benthic diatom biomass, production and sediment chlorophyll in Langebaan Lagoon, South Africa. Estuarine, Coastal and Shelf Science 27, 413–426. Froneman, P. W., Pakhomov, E. A., Perissinotto, R. & McQuaid, C. D. 1996 Role of microplankton in the diet and daily ration of Antarctic zooplankton species during the austral summer. Marine Ecology Progress Series 143, 15–23. Gifford, D. J. 1993 Protozoa in the diets of Neocalanus spp. in the oceanic subarctic Pacific Ocean. Progress in Oceanography 32, 223–237. Grindley, J. R. & Wooldridge, T. H. 1974 The plankton of Richards Bay. Hydrobiological Bulletin 8, 201–212. Hansen, B. & Bech, G. 1996 Bacteria associated with a marine planktonic copepod in culture. I. Bacterial genera in seawater, body surface, intestines and fecal pellets and succession during fecal pellet degradation. Journal of Plankton Research 18, 257–273. Hart, R. C. 1977 Feeding rhyrtmicity in a migratory copepod (Pseudodiaptomus hessei (Mra´ zek). Freshwarer Biology 7, 1–8. Hasle, G. R. 1978 The inverted microscope method. In Monographs on Oceanographic Methodology 6 (Sournia, A., ed.). Phytoplankton Manual. UNESCO, Paris, pp. 88–96. Heip, C. H. R., Goosen, N. K., Herman, P. M. J., Kromkamp, J., Middelburg, J. J. & Soetaert, K. 1995 Production and consumption of biological particles in temperate tidal estuaries. Oceanography and Marine Biology Annual Reviews 33, 1–149.
Hilmer, T. 1990 Factors Influencing the Estimation of Primary Production in Small Estuaries. Ph.D. thesis, University of Port Elizabeth, Port Elizabeth, 154 pp. Hilmer, T. & Bate, G. C. 1990 Covariance analysis of chlorophyll distribution in the Sundays River estuary, Eastern Cape. Southern African Journal of Aquatic Sciences 16, 37–59. Hilmer, T. & Bate, G. C. 1991 Vertical migration of a flagellatedominated bloom in a shallow South African estuary. Botanica Marina 34, 113–121. Holm-Hansen, O., Lorenzen, C. J., Holmes, R. W. & Strickland, J. D. H. 1965 Fluorometric determination of chlorophyll. Journal du Conseil Permanent Internatinal Exploration de la Mer 30, 3–15. Ikeda, T. & Bruce, B. 1986 Metabolic activity and elemental composition of krill and other zooplankton from Prydz Bay, Antarctica, during early summer. Marine Biology 92, 545–555. Jerling, H. L. & Wooldridge, T. H. 1995a Plankton distribution and abundance in the Sundays River Estuary, South Africa, with comments on potential feeding interactions. South African Journal of Marine Science 15, 169–184. Jerling, H. L. & Wooldridge, T. H. 1995b Relatively negative 13C ratios of mesozooplankton in the Sundays River Estuary, comments on potential carbon sources. Southern African Journal of Aquatic Sciences 21, 71–77. Kemp, P. F. 1994 Microbial carbon utilization on the continental shelf and slope during the SEEP-II Experiment. Deep-Sea Research 41, 563–581. Malone, T. C., Crocker, L. H., Pike, S. E. & Wendlerm, B. W. 1988 Influences of river flow on the dynamics of phytoplankton production in a partially stratified estuary. Marine Ecology Progress Series 48, 235–249. Mann, K. H. 1988 Production and use of detritus in various freshwater, estuarine and coastal marine ecosystems. Limnology Oceanography 33, 910–930. Masson, H. & Marais, J. F. K. 1975 Stomach content analysis of mullet from the Swartkops Estuary. Zoologica Africana 10, 193–207. Mauchline, J. 1998 The biology of calanoid copepods. Advances in Marine Biology 33, 1–710. Morant, P. D. Estuaries of the Cape, Part III: synopses of available information on individual systems; Vol. 4: Cape Recife to Kei Mouth. CSIR Research Reports, Stellenbosch (in press). Morant, P. D. & Quinn, N. 1999 Influence of man and management of South African estuaries. In Estuaries of South Africa (Allanson, B. R. & Baird, D., eds). Cambridge University Press, Cambridge, pp. 289–320. Pakhomov, E. A. & Perissinotto, R. 1996 Trophodynamics of the hyperiid amphipod Themisto gaudichaudi in the South georgia region during late austral summer. Marine Ecology Progress Series 134, 91–100. Parsons, T. R., Maita, Y. & Lalli, C. M. 1984 A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford, 173 pp. Perissinotto, R. & Wooldridge, T. H. 1989 Short-term thermal effects of a power-generating plant on zooplankton in the Swartkops Estuary, South Africa. PSZNI Marine Ecology 10, 205–219. Poulet, S. A. 1983 Factors controlling utilization of non-algal diets by particle-grazing copepods. A review. Oceanologica Acta 6, 221–234. Reddering, J. S. V. & Rust, I. C. 1990 Historical changes and sedimentary characteristics of southern African estuaries. South African Journal of Science 86, 425–428. Schlacher, T. A. & Wooldridge, T. H. 1998 Trophic Pathways at the Cross-roads—Is Detritus the Pivotal Point in all Estuarine Food Webs? ECSA 29 Conference Proceedings, University of Port Elizabeth, p. 73. Sieburth, J. McN., Smetacek, V. & Lenz, J. 1978 Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnology and Oceanography 23, 1256–1263.
Zoo- and phytoplankton relationships 11 Soetaert, K., Vincx, M., Wittoeck, J., Tulkens, M. & Van Gansbeke, D. 1994 Spatial patterns of Westerschelde meiobenthos. Estuarine, Coastal and Shelf Science 39, 367–388. Stoecker, D. K. & Capuzzo, J. M. 1990 Predation on Protozoa: its importance to zooplankton. Journal of Plankton Research 12, 891–908. Wooldridge, T. H. & McGwynne, L. 1996 The estuarine environment. Institute for Coastal Research Report No. C31, Port Elizabeth, 91 pp. Wooldridge, T. H. 1999 Estuarine zooplankton community structure and dynamics. In Estuaries of South Africa (Allanson, B. R. & Baird, D., eds). Cambridge University Press, Cambridge, pp. 141–166. Whitfield, A. K. 1989 The benthic invertebrate community of a southern Cape estuary: structure and possible food sources. Transactions of the Royal Society of South Africa 47, 159–179.
Whitfield, A. K. 1992 A characterization of southern African estuarine systems. Southern African Journal of Aquatic Sciences 18, 89–103. Whitfield, A. K. 1995 Available scientific information on individual South African estuarine systems. Water Research Commission Report No. 577/1/95, Pretoria, 204 pp. Whitfield, A. K. 1996 A review of factors influencing fish utilization of South African estuaries. Transactions of the Royal Society of South Africa 51, 115–137. Yentsch, C. S. & Menzel, D. W. 1963 A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep-Sea Research 10, 221–231.
Relationships between Zoo- and Phytoplankton in a Warm-temperate, Semi-permanently Closed Estuary, South Africa R. Perissinottoa, D. R. Walkerb, P. Webbc, T. H. Wooldridgec and R. Ballyd a
School of Life & Environmental Sciences, University of Natal, Durban 4041, South Africa Department of Plant Sciences, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa c Department of Zoology, University of Port Elizabeth, P.O. Box 1600, Port Elizabeth 6000, South Africa d Department of Zoology, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa b
Received 23 April 1999 and accepted in revised form 4 March 2000 Seasonal surveys were carried out in the shallow, well-conserved temporarily open Nyara Estuary in the Eastern Cape, South Africa. Although temporarily open estuaries constitute over 70% of estuaries in South Africa, few data are available on the structure and functioning of these systems in the region. The main aim of the study was to test the hypothesis that owing to irregular nutrient input, temporarily open estuaries may exhibit poorly-developed pelagic food webs, with low phytoplankton and pelagic biomass in general. Results from the investigation indicate that phytoplankton biomass is generally low, and dominated by pico and nanophytoplankton, with almost total absence of diatoms. This may be explained in terms of the regenerated, rather than new, nutrient pool that is available to phytoplankton as a result of the semipermanently closed nature of the estuary. Chlorophyll a levels never exceeded 4·1 mg m 3. However, low levels of phytoplankton biomass were in contrast to relatively large stocks of zooplankton, which attained maximum levels of about 2 g (dry weight) m 3. Thus, there is an imbalance between the biomass of the primary producers and that of the consumers. In order to satisfy the zooplankton energy budget, either phytoplankton production rates are extremely high or a substantial proportion of their food demands must be met through utilization of alternative sources, such as detritus, protozoans and microphytobenthos. It is suggested that microphytobenthos in particular may play a major role in this regard because of the prevailing good conditions for its growth in this type of ecosystem. Microbenthic chlorophyll a concentrations in the Nyara Estuary are in the upper range of values measured in South African estuaries, with an average of ≅190 mg m 2. Further studies are needed to investigate the ability of the dominant species of zooplankton to ingest and assimilate benthic microalgae, particularly during the day when most species remain in close association with the substratum. 2000 Academic Press Keywords: plankton; detritus; microheterotrophs; microphytobenthos, temporarily open estuaries, South Africa
Introduction Of the 250 estuaries in South Africa, 182 (or 73% of the total) are currently classified as temporarily open/ closed (Whitfield, 1995). During the dry season and under low river flow conditions, these systems close off from the sea by a sandbar that forms at the mouth. Following periods of high rainfall and freshwater runoff, the water level inside the estuary may rise suddenly or gradually until it exceeds the height of the sandbar at the mouth (Whitfield, 1992; Wooldridge & McGwynne, 1996). Breaching then occurs and the water level drops very rapidly, often exposing large areas of substratum which had been submerged for long periods and colonized by a rich community of plants and animals. River conditions may briefly dominate the estuary during breaching events, but the 0272–7714/00/070001+11 $35.00/0
sandbar at the mouth is rapidly regenerated by longshore sand movement in the surf zone (usually within weeks). This leads to another closed phase during which seawater inflow is generally provided by wash-over at the peak of the spring tide or during storm surges. Although many local estuaries naturally close off from the sea for varying periods, increasing retention of freshwater by dams for domestic, industrial and agricultural purposes reduces the frequency and duration of mouth opening (Reddering & Rust, 1990; Cooper et al., 1999). This affects negatively the sediment scouring ability of estuaries and their capacity of eliminating build-ups of pollutants (Begg, 1984a; Whitfield, 1992). The long residence time of water and sediments in these estuarine basins makes their benthic, pelagic and nekton communities very 2000 Academic Press
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vulnerable to environmental degradation, compared to their counterparts in permanently open estuaries. This is compounded by the fact that temporarily open estuaries are playing an increasingly large role in the economic development of the country, either as sites of industrial/agricultural development or as ecotourism and fishing resorts. For the vast majority of South Africa’s temporarily open estuaries no information is presently available on physicochemical and biological properties (Whitfield, 1995). Of the four systems for which data are available, most is of biological nature involving taxonomic, recruitment and stock assessment studies of macroorganisms, particularly fish, molluscs, crustaceans and seagrasses of economic and conservation interest (Begg, 1978; Day, 1981; Begg, 1984a, 1984b; Wooldridge & McGwynne, 1996; Whitfield, 1996; Allanson & Baird, 1999). In permanently open estuaries, regular seawater and freshwater inflows are normally capable of supporting a large phytoplankton biomass and a well-developed pelagic food web (Adams & Bate, 1999). This is mainly associated with the steady supply of nutrients and the maintenance of stable stratified conditions (Hilmer & Bate, 1990; Allanson & Read, 1995; Jerling & Wooldridge, 1995a; Adams & Bate, 1999). Conversely, temporarily open estuaries are often dominated by submerged macrophytes that are able to take advantage of the conditions prevailing in these systems. These include low turbidity and current levels as well as a more stable sediment and salinity environment, and also the large nutrient pool available in the substratum (Adams et al., 1999). The implications of these major differences for the trophic functioning of temporarily open estuaries have not been investigated yet and could have important consequences for the management strategies that are currently applied to these ecosystems (Morant & Quinn, 1999). Our study was specifically designed with the aim of looking at the composition and seasonal variations of the stocks at the lower levels of the food web of a temporarily open estuary, in order to test the hypothesis that the plankton component of these systems may indeed be under-developed relative to that of permanently open systems. The study focuses specifically on the biomass, abundance and broad taxonomic composition of the zoo- and phytoplankton communities observed in the Nyara Estuary during 1997. Materials and methods Four 3-day surveys were carried out in the Nyara Estuary, a semi-permanently closed system on the
Eastern Cape coast of South Africa (Figure 1). The surveys took place in March, May, September and November 1997. Depth, salinity and temperature were measured at the surface, in the middle and in the near-bottom layers using a Hydrolab H20 Multiprobe. Irradiance levels (PAR) were measured at 50 cm depth intervals with a LI-COR Li-193SA Spherical Quantum Sensor. Samples for chlorophyll a (chl a) and phaeopigment determination were collected using a Van Dorn water sampler. Aliquots of 200 ml were filtered sequentially onto a 20 m Nitex filter, a 2·0 m Millipore TTTP and a GF/F Whatman glass fibre filter, in order to fractionate the total phytoplankton pigment biomass into micro, nano and pico size-fractions, respectively (Sieburth et al., 1978). Pigments were extracted in 90% acetone and fluorescence readings were taken using a Turner 111 or a Turner Designs 10-AU Fluorometer, before and after acidification (Yentsch & Menzel, 1963; Holm-Hansen et al., 1965). Chl a and phaeopigment concentrations were then obtained using the formulae of Parsons et al. (1984) as modified by Conover et al. (1986). The same water sampler was also used to collect phytoplankton/protozoan samples (250 ml) for microscopic analysis. These were immediately fixed with 2% hexamine-buffered formalin and the major taxa were later identified and counted in the laboratory under an inverted microscope, after sedimentation in 10 ml chambers (Hasle, 1978). While regular microphytobenthic chlorophyll a measurements were not made during the 1997 survey, representative samples were collected at the beginning of November 1998 at a time when the Nyara Estuary was isolated from the sea. Samples were taken using a 20 mm internal diameter corer and the chlorophyll of the upper 10 mm of sediment was extracted in 30 ml of ethanol. Chlorophyll a concentrations were then determined by HPLC following the protocol outlined in Adams and Bate (1999). Zooplankton samples were collected using a 4·5 m flat-bottomed boat. Two WP-2 nets, one fitted with 90 m and the other with 200 m mesh, were towed in parallel on each side of the boat at a speed of about 0·5–1·0 knot and at a depth of 5–10 cm below the surface. Both nets were fitted with Kahlsico 005WA130 flowmeters. Volume filtered ranged between 3 and 8 m3, with an average of approximately 5 m3 per haul. In the laboratory, subsamples for identification and enumeration were drawn off the sample which had been suspended in a 1–10 l solution, depending on the concentration of organisms. Using a 25 cm long glass tube of 10 mm diameter, duplicate subsamples of 20 ml each were withdrawn after penetrating the entire depth of the suspension and while
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preventing settlement through constant stirring (Perissinotto & Wooldridge, 1989; Jerling & Wooldridge, 1995a). The coefficient of variation (CV) between subsamples obtained in this way was consistently below 15% and averaged about 6%.
Estimates of zooplankton biomass were obtained both volumetrically and gravimetrically, after the removal of large detrital particles under a dissecting microscope. In the first instance, the displaced volume of each sample was measured with the
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F 2. Vertical profiles of salinity (a) and temperature (b) along the Nyara Estuary during the four surveys undertaken in 1997. Salinity was measured using the Practical Salinity Scale and temperature is expresssed in C.
vacuum extraction technique, involving the removal of both solution and interstitial fluids (Beers, 1976). Wet weight (WW) was the main gravimetric parameter used, as this does not involve the destruction of the sample or part of it. However, in order to compare our results with most of those obtained in other studies, the total dry weight (DW) was also measured for several samples, generally those with high zooplankton densities. In this case, only subsamples of one-fifth to one-half of the total were processed. Where no DW could be measured directly, this was derived using the general regression equation between DW and settled volume (SV) obtained by Grindley and Wooldridge (1974), mg (DW)=18·6ml (SV). WW was obtained by weighing the sample immediately after the removal of solution and interstitial liquid under gentle vacuum (<200 mm Hg). Samples for DW measurement were oven-dried for 36 h at 60 C prior to weighing (Pakhomov & Perissinotto, 1996).
Results Physicochemical environment Prior to our first survey, in March 1997, the Nyara Estuary had been closed since December 1996. During 1996, mouth breaching occurred on two occasions due to heavy rainfalls in November and December (Bosbokstrand Private Nature Reserve, pers. comm.). During 1997, the combined effects of runoff and overwash from the sea resulted in a progressive increase in the average depth of the estuary. This increased from about 1·5 m in March–May to 2·2 m in September. Heavy rains caused the mouth to open and the estuary to drain to a maximum depth of 1 m on the 28 of November (Figure 2). In March 1997, the estuary exhibited a horizontal salinity gradient in surface waters [Figure 2(a)], but below 1 m depth salinity levels were consistently high (26·5–31·5). A strongly stratified water-column was
Zoo- and phytoplankton relationships
Phytoplankton and microphytobenthos In terms of total numerical abundance, the phytoplankton community was dominated by small flagellates of <2 m in size. The largest cells (>10 m) were mainly dinoflagellates, Protoperidinium spp. and unidentified species of 10-15 m size. Diatoms were present in very low numbers and diversity throughout the water-column (Walker et al., submitted). Total phytoplankton chl a concentration exhibited a maximum of 4·1 mg m 3 in May 1997 and a minimum of 0·007 mg m 3 in November (Figure 3). Average values were consistently low, with the highest
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observed in May, with salinity values ranging from 23 at the surface to over 30 at the bottom. Due to the lack of freshwater inflow during the dry winter months, no horizontal gradient in salinity was observed during this period. In September, the bottom salinity decreased to a maximum of about 27 [Figure 2(a)], while surface levels showed a diffuse gradient (24 to 22) from the mouth to the head. The November survey coincided with the flood event, which caused the opening of the mouth and the flushing of the estuary [salinity c0·5, Figure 2(a)]. High water temperatures of 28–30 C were recorded in March [Figure 2(b)]. By May, values had dropped by an average of about 10 C and remained much the same in September, with warmer waters found higher up in the estuary on both occasions. Because of the flooding, water temperature was uniform in November, showing only a slight warming by about 1 C as the water moved through the estuary [Figure 2(b)]. Surface irradiance levels (PAR) ranged from a maximum of about 2300 mol m 2 s 1 to minima of about 550 mol m 2 s 1, depending on weather conditions and time of the day. During the closed phase of the estuary, average values of the light attenuation coefficient (k) were low, in the range of 0·42–1·49 m 1. The lowest levels were recorded near the mouth (Stns 1 and 2) and the highest at the head of the estuary (Stns 6 and 7). Given the shallow depth, this resulted in high irradiance been recorded at the bottom, where light intensities were normally 30–60% of surface levels. PAR values of less than 300 mol m 2 s 1 were recorded at the bottom only on two occasions. However, during the flood in November the penetration of irradiance in the water was virtually non-existent due to the high density of suspensoids. On this occasion, no PAR could be detected at 15–20 cm depth and extinction coefficients attained levels of 8–14 m 1.
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4 5 Station number
F 3. Total phytoplankton chlorophyll a concentration (mg m 3) measured in the Nyara Estuary during March, May, September and November 1997.
in March (1·180·58 SD, N=11) and the lowest in November (0·0150·009 SD, N=4). In March, the highest levels were recorded near the bottom, in May in the middle layer and in September near the surface, while during the November flood chl a levels were low throughout the water-column. Chl a values decreased horizontally from the mouth to the head in March, while the opposite trend was observed in May and September (Figure 3). The distribution of chl a into <2 m (pico-), 2-20 m (nano-) and >20 m (micro-) size-classes varied with season, and was characterized by the dominance of the smaller classes. Picoplankton dominated the total chl a stock in May, with 65·427% (SD) of the total, and nanoplankton likewise in September (57·117% SD) and November (67·515% SD). Microplankton contributed substantially to the total only in March, with levels close to 50% of the total chl a stock. Benthic microalgae chl a concentration (measured in November 1998) was uniform at the three stations sampled. Mean values ranged from 170 mg m 2 at Station 2 to about 200 mg m 2 at Stations 1 and 4. The average value for the three stations was 18916·5 SD, N=6.
6
R. Perissinotto et al.
Zooplankton and protozoans The zooplankton community was composed largely of micro-sized (<200 m) larval stages during daytime. These included copepod nauplii, barnacle cypris, and gastropod veligers (Table 1). In the night-time samples, on the other hand, the calanoid copepods Pseudodiaptomus hessei and Acartia natalensis were dominant, and an unidentified species of Halicyclops sp. and a large variety of harpacticoid copepods, comprising at least 12 different species, were also abundant (Table 1). Polychaetes, especially Prionospio sp., the cumacean Iphinoe truncata and amphipods were also present in substantial numbers, and occasionally dominated the night-time samples (Table 1). During the September survey only, an unidentified species of Anthomedusae (approximately 200– 800 m diameter) was in bloom phase and exhibited concentrations of up to 29·4103 ind m 3. Maximum total zooplankton densities were found in September with about 6·5106 ind m 3. Minima occurred at the time of the November flood with 3·8104 ind m 3. Zooplankton biomass in the estuary varied from a minimum of 19·2 mg wet weight (WW) m 3, during daytime in May, to a maximum of 15·2 g WW m 3 during night-time in September (Figure 4). Average night-time values were 4–35 times higher than daytime values. Displaced volumes (DV) ranged from 0·058 ml m 3, in May daytime samples, to 18·8 ml m 3 in September night-time samples. Similarly, the corresponding levels of dry weight (DW) exhibited minima and maxima of 1·08 mg m 3 and 2·03 g m 3 respectively. The highest biomasses were found in the middle/upper reaches of the estuary in March, May and November but shifted towards the mouth during September (Figure 4). Protozoan counts in the samples were low, with maxima of about 14103 cells l 1 in May and minima of 8·6103 cells l 1 in March. The most abundant groups were the nanoflagellates, aloricate ciliates and tintinnids. Details on the abundance and carbon biomass of these groups during the survey period are reported elsewhere (Walker et al., submitted).
Discussion Temporarily open estuaries lack the steady supply of macronutrients generally observed in permanently open estuaries. In open systems, this is provided by the regular input of nutrient-rich freshwater, by tidally-driven advection from the sea and by resuspension of benthic regenerated nutrients (Malone et al.,
1988; Adams & Bate, 1994; Allanson & Read, 1995). Nutrient deficiency in temporarily open estuaries may limit the productivity of phytoplankton, despite the ideal conditions of water column stratification and light intensity that are often found in these systems (Adams & Bate, 1999). Phytoplankton biomass (as chl a) measured during the Nyara study exhibited a maximum of 4·1 mg m 3 in May and a minimum of 0·007 during the November flood (Figure 3). The overall average of the four surveys was 0·440·53 (SD) mg m 3. These are among the lowest values recorded for any South African estuary (Hilmer & Bate, 1991; Campbell et al., 1991; Allanson & Read, 1995; Adams & Bate, 1999). In contrast, the maximum zooplankton dry mass levels measured in the Nyara Estuary are approximately an order of magnitude higher than the average values recorded in the most productive estuaries of the Eastern Cape (i.e. Sundays and Gamtoos Estuaries, Wooldridge, 1999). The average value over the total period of the investigation was 150 mg m 3, which is 2–5 times higher than the average values reported by Wooldridge (1999) for the most (]80 mg DW m 3) and the least (]30 mg DW m 3) productive South African estuaries, respectively. It must be stressed, however, that sampling in the Nyara Estuary took place only seasonally and on four occasions. The zooplankton data show a large variation, with concentrations ranging from the highest ever recorded in South Africa to almost the lowest (Table 1). Clearly there are aperiodic boosts in growth followed by periods of low activity. This indicates that these small systems generally fluctuate between extremes and may lack the buffering capacity observed in larger volume systems, where a relative stability is maintained in the zooplankton community throughout the year. If sampling had been carried out more frequently, it is likely that average concentrations could have been less skewed towards large values. Nevertheless, even taking this potential bias into account the figures for zooplankton biomass and abundance are still very high compared to the phytoplankton stock of the estuary. It is possible that part of this disparity may be accounted for by the higher turnover rate of phytoplankton, compared to zooplankton. Unfortunately, no measurements of primary production rates could be made during this study. Estimates from similar systems in the region are few and show a wide range of variation, from 32 to 147 mg C m 2 h 1 (Campbell et al., 1991). On an annual basis, these rates may be enough to support the energy requirements of the zooplankton community. However, the large shortterm fluctuations observed in the Nyara Estuary may result in temporal imbalances between pelagic
Pseudodiaptomus hessei Acartia natalensis Oithona spp. Oncaea spp. Halicyclops sp. Cyclopoids spp. Harpacticoids spp. Copepod nauplii Barnacle cypris Amphipod juveniles Iphinoe truncata Anthomedusae Prionospio sp. Veligers larvae Nematodes
Taxon
14 8607420 11 2987413 21267 10·910·9 1429609 596315 58481332 34 0807488 58473535 830366 677410 00 12061107 270184 23·312·8
AverageStd error
8 March 1997
19·5 13·1 0·28 0·01 1·87 0·78 7·66 44·6 7·66 1·09 0·89 0 1·58 0·35 0·03
% Total 50582051 12·58·73 3·712·32 0·580·29 1245544 77·742·6 22 7099659 39261427 697295 12688·7 18811528 00 74372921 1822643 14·411·1
AverageStd error
24 May 1997
11·1 0·03 0·01 0·01 2·74 0·17 50·1 8·64 1·53 0·28 4·14 0 16·4 4·01 0·03
% Total 385 268241 656 81143557 2·130·87 00 19 41810 917 75222929 41 10715 013 205 00953 359 27561362 357261 7·045·13 15 6252202 32441657 31461603 382249
AverageStd error 53·1 1·24 0·01 0·01 2·97 1·15 6·29 31·4 0·42 0·05 0·01 2·39 0·49 0·48 0·06
% Total
6 September 1997
39·453·6 0·830·59 57·166·7 87·983·8 518302 162108 33831006 28·653·6 1·080·96 1053308 10·88·03 00 196204 00 133249
AverageStd error
0·72 0·01 1·05 1·61 9·49 2·98 61·9 0·52 0·01 13 8 0·19 0 3·58 0·01 2·44
% Total
29 November 1997
T 1. Average abundance (no. m 3) and percent contribution of the most important components of the zooplankton community of the Nyara Estuary during 1997. Taxa were selected on the basis of their contribution to the total counts with >1% on at least one sampling occasion
Zoo- and phytoplankton relationships 7
8
R. Perissinotto et al.
Zooplankton biomass (wet weight mg m–3)
Nyara Estuary: 08 March 1997 (Near New Moon)
3000 2500 2000 1500 1000 500 0
1
2
3
4
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6
Zooplankton biomass (wet weight mg m–3)
Nyara Estuary: 24 May 1997 (Near Full Moon)
3000 2500 2000 1500 1000 500 0
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6
Zooplankton biomass (wet weight mg m–3)
Nyara Estuary: 06 September 1997 (Near New Moon)
20 000 15 000 10 000 5000 0
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Zooplankton biomass (wet weight mg m–3)
Nyara Estuary: 29 November 1997 (Near New Moon)
3000 2500 2000 1500 1000 500 0
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3 4 Station number
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6
F 4. Mesozooplankton biomass, in units of wet weight (WW) m 3, in the Nyara Estuary during March, May, September and November 1997. Note the change of scale in the y-axis by an order of magnitude for the September data. Open bars: WW day; closed bars: night.
primary producers and consumers. This is likely to have important implications for the trophic functioning of the entire ecosystem. Assuming a general conversion factor of chlorophyll a to carbon of about 50 (Atkinson & Shreeve, 1995) and a zooplankton carbon content of C=47·1, %DW=42·6 (Ikeda & Bruce, 1986), the phytoplankton stock of the Nyara Estuary would have been able to support all the energetic requirements of the
zooplankton community only during the March and May surveys. During these periods, the estimated phytoplankton:zooplankton carbon ratios were approximately 1·64 and 3·16, respectively. However, the situation was reversed during September and November, when the ratios were 0·013 and 0·11 respectively. This implies that the available phytoplankton could at most have supplied a ration of 1·29% in September and 10·7% in November of body carbon per day to the local zooplankton. While these levels may have been just enough to sustain the basic metabolic activity of zooplankton organisms, it is very unlikely that they were sufficient to support their energy demands for growth, molting and reproduction. A recent review of the average daily rations measured in calanoid copepods (Mauchline, 1998), shows that over 85% of them are >10% body C day 1 (x=51·952·1 SD, N=79), with values below this reported almost exclusively in cold, high latitude waters (Ba˚ mstedt et al., 1991; Froneman et al., 1996). It seems most likely then, at least during September and November, that the Nyara zooplankton community was heavily supplementing its diet with other food sources. Because of the size constraints imposed by ingestion processes, there are only three options that can be considered to have played a major role at the time: detritus, microheterotrophs and microphytobenthos. Detritus and microheterotrophs are two components that are generally tightly linked in estuarine ecosystems. In the Nyara Estuary, dead and decomposing plant matter was noticeable throughout the water column. The high level of plant detritus could also be identified from the low chlorophyll:phaeopigment ratio. Only during the March survey was this ratio >1, with an average value of 2·250·69 (SD). Otherwise, the ratio was well below 1 both during May (x=0·170·09 SD), September (x=0·430·22 SD) and November, when the lowest average value of 0·060·02 (SD) was recorded (Walker et al., pers. comm.). The riparian vegetation of the estuary contributes the bulk of the detritus and is composed of dense afromontane forests and saltmarsh plants (Morant, in press). Detritus of macrophytic origin has often been reported as remaining virtually unutilized by estuarine zooplankton (Mann, 1988; Poulet, 1983; Jerling & Wooldridge, 1995b; Schlacher & Wooldridge, 1998). Microbial heterotrophs, particularly bacteria, are on the other hand capable of digesting the fibre material and other refractory carbon compounds. Although some zooplankton species are known to utilize bacteria directly (Poulet, 1983), in most cases only a minor proportion of zooplankton carbon demand is
Zoo- and phytoplankton relationships
met through their direct assimilation in the gut (Boak & Goulder, 1983; Hansen & Bech, 1996). More often, however, it is the protozoans that are able to make full use of the bacterial biomass developing on the detritus (Heip et al., 1995). Protozoans are then in turn preyed upon by larger zooplankton, within the ‘ microbial loop ’ (Azam et al., 1983; Stoecker & Capuzzo, 1990; Gifford, 1993). In the Nyara Estuary, ciliates and flagellates exhibited average cell concentrations ranging from 8·6103 cells l 1 in March to 14103 cells l 1 in May and 13103 cells l 1 in September. These concentrations are not regarded as very high (Heip et al., 1995), nevertheless, they may have been able to support a substantial proportion of the energy demands of mesozooplankton (Stoecker & Capuzzo, 1990; Fessenden & Cowles, 1994). Also, protozoan abundance could have been underestimated significantly during this work, mainly because of fixation problems. Losses of up to 40% of the total number of ciliates have been recorded in samples preserved in formalin (Kemp, 1994). The third potential source of food for the rich zooplankton community observed in the Nyara Estuary may have been the microphytobenthos. This is an algal component that is usually linked with meiobenthos feeding but is not considered among the important sources of food for the pelagic food web of permanently open, tidal estuaries (Soetaert et al., 1994; Heip et al., 1995). There are, however, a number of features of temporarily open estuaries that need to be considered in this regard, as they may suggest exploring some new pathways of trophic functioning and bentho-pelagic coupling. The positive ratio of euphotic depth to total depth of many estuaries, contributes to the high productivity rates of benthic microalgae which are observed at all seasons of the year (Hilmer, 1990). A survey of Cape estuaries has shown that in most systems benthic microalgal biomass is 2–3 orders of magnitude higher than the phytoplankton (all values standardized to m2 units), with highest levels recorded in temporarily open systems (Whitfield, 1989; Adams & Bate, 1994, 1999). Here, during the closed phase, water-column depths are usually very shallow and sediment disturbance by water currents is minimal, thus providing ideal conditions for growth. Being available all year round, benthic microalgae represent an important food source for benthic grazers and demersal fish (Masson & Marais, 1975; Whitfield, 1989). The close interaction that many vertically-migrating zooplankton species have with the substratum of these estuaries, suggest that this benthic source may be potentially important to the pelagic subsystem too (cf. also Hart, 1977).
9
Chlorophyll a concentrations in the upper 10 mm of the substratum of the Nyara Estuary are in the upper range of values recorded in South African estuaries (Fielding et al., 1988; Whitfield, 1989; Adams & Bate, 1999), with maxima of 200 mg m 2 and an average of 18916·5 SD mg m 2. Thus, when compared to phytoplankton chlorophyll, benthic chlorophyll levels are about 2–4 orders of magnitude higher than those recorded in the watercolumn. This probably reflects the optimal conditions in irradiance and sediment stability that are found through most days of the year in this semipermanently closed system. During the close phase, photosynthetically available radiation (PAR) levels at the bottom of the estuary were in the range of 30–60% of surface values and above 300 mol m 2 s 1. When considering the marked diurnal migrations that the zooplankton of this and similar estuaries undergo, it seems reasonable to expect that during much of the daytime (when animals avoid the water-column and are in contact with or just above the substrate) grazing on this rich benthic microalgae resource is not only possible but highly likely. Aknowledgements This study was sponsored by the National Research Foundation (NRF, Pretoria). We wish to thank Mr J. Jemaar, Mr F. M. Ngcongca and Mr E. N. Nkoane of the Department of Zoology, University of Fort Hare (Alice), as well as students X. C. Thwala, V. Sajini, S. Pheeha, M. Zatu, M. Njili and H. N. Gunguta for their invaluable help with field work and laboratory analyses. Dr J. Adams of the Department of Botany, University of Port Elizabeth, is thanked for carrying out the HPLC measurements of microphytobenthic chlorophyll concentration and Ms V. Meaton of the Department of Zoology & Entomology, Rhodes University (Grahamstown) for identifying and counting the zooplankton taxa. We are also grateful to the Management of the Bosbokstrand Private Nature Reserve for allowing the use of their facilities during the field surveys. References Atkinson, A. & Shreeve, R. S. 1995 Response of the copepod community to a spring bloom in the Bellingshausen Sea. Deep-Sea Research 42, 1291–1311. Adams, J. B. & Bate, G. C. 1994 The freshwater requirements of estuarine plants incorporating the development of an estuarine decision support system. Water Research Commission (RSA), Report No. 292/1/94, 151 pp. Adams, J. B. & Bate, G. C. 1999 Primary producers: estuarine microalgae. In Estuaries of South Africa (Allanson, B. R. & Baird, D., eds). Cambridge University Press, Cambridge, pp. 91–100.
10 R. Perissinotto et al. Allanson, B. R. & Baird, D. 1999 Estuaries of South Africa. Cambridge University Press, Cambridge. Allanson, B. R. & Read, G. H. L. 1995 Further comment on the response of south east coast estuaries to variable freshwater flows. Southern African Journal of Aquatic Sciences 21, 56–71. Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A. & Thingstad, F. 1983 The ecological role of water-column microbes in the sea. Marine Ecology Progress Series 10, 257–263. Ba˚ mstedt, U., Eilertsen, H. C., Tande, K. S., Slagstad, D. & Skjoldal, H. R. 1991 Copepod grazing and its potential impact on the phytoplankton development in the Barents Sea. Polar Research 10, 339–353. Beers, J. R. 1976 Determination of zooplankton biomass. In Zooplankton Fixation and Preservation (Steedman, H. F., ed.). Monographs on Oceanographic Methodology, no. 4, UNESCO, Paris, pp. 35–84. Begg, G. W. 1978 The estuaries of Natal. Natal Town and Regional Planning Report, Vol. 41, Pietermaritzburg, 657 pp. Begg, G. W. 1984a The estuaries of Natal, Part 2. Natal Town and Regional Planning Report, Vol. 55, Pietermaritzburg, 631 pp. Begg, G. W. 1984b The comparative ecology of Natal’s smaller estuaries. Natal Town and Regional Planning Report, Vol. 62, Pietermaritzburg, 182 pp. Boak, A. C. & Goulder, R. 1983 Bacterioplankton in the diet of the calanoid copepod Eurytemora sp. in the Humber Estuary. Marine Biology 73, 139–149. Campbell, E. E., Knoop, W. T. & Bate, G. C. 1991 A comparison of phytoplankton biomass and primary production in three east Cape estuaries, South Africa. South African Journal of Science 87, 259–264. Conover, R. J., Durvasula, R., Roy, S. & Wang R. 1986 Probable loss of chlorophyll-derived pigments during passage through the gut of zooplankton and some of the consequences. Limnology and Oceanography 31, 878–887. Cooper, A., Wright, I. & Mason, T. 1999 Geomorphology and sedimentology. In Estuaries of South Africa (Allanson, B. R. & Baird, D., eds). University Press, Cambridge, pp. 5–25. Day, J. H. 1981 Estuarine Ecology with Particular Reference to Southern Africa. AA Balkema, Cape Town, 411 pp. Fessenden, L. & Cowles, T. J. 1994 Copepod predation on phagotrophic ciliates in Oregon coastal waters. Marine Ecology Progress Series 107, 103–111. Fielding, P. J., Damstra, K. St-J. & Branch, G. M. 1988 Benthic diatom biomass, production and sediment chlorophyll in Langebaan Lagoon, South Africa. Estuarine, Coastal and Shelf Science 27, 413–426. Froneman, P. W., Pakhomov, E. A., Perissinotto, R. & McQuaid, C. D. 1996 Role of microplankton in the diet and daily ration of Antarctic zooplankton species during the austral summer. Marine Ecology Progress Series 143, 15–23. Gifford, D. J. 1993 Protozoa in the diets of Neocalanus spp. in the oceanic subarctic Pacific Ocean. Progress in Oceanography 32, 223–237. Grindley, J. R. & Wooldridge, T. H. 1974 The plankton of Richards Bay. Hydrobiological Bulletin 8, 201–212. Hansen, B. & Bech, G. 1996 Bacteria associated with a marine planktonic copepod in culture. I. Bacterial genera in seawater, body surface, intestines and fecal pellets and succession during fecal pellet degradation. Journal of Plankton Research 18, 257–273. Hart, R. C. 1977 Feeding rhyrtmicity in a migratory copepod (Pseudodiaptomus hessei (Mra´ zek). Freshwarer Biology 7, 1–8. Hasle, G. R. 1978 The inverted microscope method. In Monographs on Oceanographic Methodology 6 (Sournia, A., ed.). Phytoplankton Manual. UNESCO, Paris, pp. 88–96. Heip, C. H. R., Goosen, N. K., Herman, P. M. J., Kromkamp, J., Middelburg, J. J. & Soetaert, K. 1995 Production and consumption of biological particles in temperate tidal estuaries. Oceanography and Marine Biology Annual Reviews 33, 1–149.
Hilmer, T. 1990 Factors Influencing the Estimation of Primary Production in Small Estuaries. Ph.D. thesis, University of Port Elizabeth, Port Elizabeth, 154 pp. Hilmer, T. & Bate, G. C. 1990 Covariance analysis of chlorophyll distribution in the Sundays River estuary, Eastern Cape. Southern African Journal of Aquatic Sciences 16, 37–59. Hilmer, T. & Bate, G. C. 1991 Vertical migration of a flagellatedominated bloom in a shallow South African estuary. Botanica Marina 34, 113–121. Holm-Hansen, O., Lorenzen, C. J., Holmes, R. W. & Strickland, J. D. H. 1965 Fluorometric determination of chlorophyll. Journal du Conseil Permanent Internatinal Exploration de la Mer 30, 3–15. Ikeda, T. & Bruce, B. 1986 Metabolic activity and elemental composition of krill and other zooplankton from Prydz Bay, Antarctica, during early summer. Marine Biology 92, 545–555. Jerling, H. L. & Wooldridge, T. H. 1995a Plankton distribution and abundance in the Sundays River Estuary, South Africa, with comments on potential feeding interactions. South African Journal of Marine Science 15, 169–184. Jerling, H. L. & Wooldridge, T. H. 1995b Relatively negative 13C ratios of mesozooplankton in the Sundays River Estuary, comments on potential carbon sources. Southern African Journal of Aquatic Sciences 21, 71–77. Kemp, P. F. 1994 Microbial carbon utilization on the continental shelf and slope during the SEEP-II Experiment. Deep-Sea Research 41, 563–581. Malone, T. C., Crocker, L. H., Pike, S. E. & Wendlerm, B. W. 1988 Influences of river flow on the dynamics of phytoplankton production in a partially stratified estuary. Marine Ecology Progress Series 48, 235–249. Mann, K. H. 1988 Production and use of detritus in various freshwater, estuarine and coastal marine ecosystems. Limnology Oceanography 33, 910–930. Masson, H. & Marais, J. F. K. 1975 Stomach content analysis of mullet from the Swartkops Estuary. Zoologica Africana 10, 193–207. Mauchline, J. 1998 The biology of calanoid copepods. Advances in Marine Biology 33, 1–710. Morant, P. D. Estuaries of the Cape, Part III: synopses of available information on individual systems; Vol. 4: Cape Recife to Kei Mouth. CSIR Research Reports, Stellenbosch (in press). Morant, P. D. & Quinn, N. 1999 Influence of man and management of South African estuaries. In Estuaries of South Africa (Allanson, B. R. & Baird, D., eds). Cambridge University Press, Cambridge, pp. 289–320. Pakhomov, E. A. & Perissinotto, R. 1996 Trophodynamics of the hyperiid amphipod Themisto gaudichaudi in the South georgia region during late austral summer. Marine Ecology Progress Series 134, 91–100. Parsons, T. R., Maita, Y. & Lalli, C. M. 1984 A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford, 173 pp. Perissinotto, R. & Wooldridge, T. H. 1989 Short-term thermal effects of a power-generating plant on zooplankton in the Swartkops Estuary, South Africa. PSZNI Marine Ecology 10, 205–219. Poulet, S. A. 1983 Factors controlling utilization of non-algal diets by particle-grazing copepods. A review. Oceanologica Acta 6, 221–234. Reddering, J. S. V. & Rust, I. C. 1990 Historical changes and sedimentary characteristics of southern African estuaries. South African Journal of Science 86, 425–428. Schlacher, T. A. & Wooldridge, T. H. 1998 Trophic Pathways at the Cross-roads—Is Detritus the Pivotal Point in all Estuarine Food Webs? ECSA 29 Conference Proceedings, University of Port Elizabeth, p. 73. Sieburth, J. McN., Smetacek, V. & Lenz, J. 1978 Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnology and Oceanography 23, 1256–1263.
Zoo- and phytoplankton relationships 11 Soetaert, K., Vincx, M., Wittoeck, J., Tulkens, M. & Van Gansbeke, D. 1994 Spatial patterns of Westerschelde meiobenthos. Estuarine, Coastal and Shelf Science 39, 367–388. Stoecker, D. K. & Capuzzo, J. M. 1990 Predation on Protozoa: its importance to zooplankton. Journal of Plankton Research 12, 891–908. Wooldridge, T. H. & McGwynne, L. 1996 The estuarine environment. Institute for Coastal Research Report No. C31, Port Elizabeth, 91 pp. Wooldridge, T. H. 1999 Estuarine zooplankton community structure and dynamics. In Estuaries of South Africa (Allanson, B. R. & Baird, D., eds). Cambridge University Press, Cambridge, pp. 141–166. Whitfield, A. K. 1989 The benthic invertebrate community of a southern Cape estuary: structure and possible food sources. Transactions of the Royal Society of South Africa 47, 159–179.
Whitfield, A. K. 1992 A characterization of southern African estuarine systems. Southern African Journal of Aquatic Sciences 18, 89–103. Whitfield, A. K. 1995 Available scientific information on individual South African estuarine systems. Water Research Commission Report No. 577/1/95, Pretoria, 204 pp. Whitfield, A. K. 1996 A review of factors influencing fish utilization of South African estuaries. Transactions of the Royal Society of South Africa 51, 115–137. Yentsch, C. S. & Menzel, D. W. 1963 A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep-Sea Research 10, 221–231.