Short-term variability during an anchor station study in the southern Benguela upwelling system: Phytoplankton dynamics

Prog. Oceanog.Vol. 28, pp.

39-64, 1991. Printed in Great Britain. All fights reserved.

0079 - 6611/91 $0.00 + ,50 © 1991 Pergamon Press plc

Short-term variability during an anchor station study in the southern Benguela upweilingsystem: Phytoplankton dynamics G.C. PITCHER l, D.R. WALKER l, B.A. M1TCHELL-INNES 1 and C.L. MOLONEY~

1SeaFisheries ResearchInstitute, Private Bag X2, Rogge Bay, 8012, Cape Town, South Africa 2Marine Biology ResearchInstitute, Departmentof Zoology, University of Cape Town, Private Bag, Rondebosch, 7700, Cape Town, South Africa

Abstract - The temporal variability of the phytoplankton and the role of sinking in such variability was examined in response to environmental changes associated with coastal upwelling during a 27day anchor station study in St Helena Bay on the South African west coast. Two phytoplankton blooms were observed, both of which were directly related to the intrusion of recently upwelled water of high nutrient concentration. Many of the observed phytoplankton changes corresponded to recognised stages of succession, as turbulence dissipated, whereas others resulted from sequential changes owing to changes in water-mass type. The system progressed from a high biomass diatom bloom in turbulent, nutrient rich water, to a flagellate community at much lower biomass levels in stratified, nutrient depleted water. Changes in the phytoplankton corresponded to changes in the vertical stability of the water column, the stratification index giving good qualitative prediction of the relative dominance of diatoms and flagellates. Phytoplankton community changes were unpredictable at the species level, but showed systematic trends in the dominance patterns of higher taxonomic levels such as diatoms, dinoflagellates and microflagellates. A number of changes in the species composition resulted from the interrelation between turbulence and the variable sinking rates of different components of the phytoplankton. Rapid sinking of diatom resting spores represented the transition from an active surface growing stage to a resting stage positioned in deeper water, thus ensuring the restoration of cells to the surface layer by restricted mixing events. Losses from the euphotic zone were nevertheless of limited importance to changes in the phytoplankton biomass. Natural mortality and breakdown of phytoplankton cells within the surface layers is thought to have been most important in accounting for the phytoplankton biomass decline.

39

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G.C. Prrow~ et al.

CONTENTS 1.

2.

5.

6. 7.

Introduction Methods 2.1 Physical,chemical and biological measurements 2.2 Examinationof phytoplankton assemblages 2.2.1 Identificationand enumeration of phytoplankton 2.2.2 Classificationanalysis of phytoplankton assemblages and the identification of indicator species 2.2.3 Collectionofphytoplankton samples from the sediments 2.3 Phytoplanktoncell, phytoplanktoncarbon and particulate organic carbon flux measurements Results 3. l Physical,chemical and biological environment 3.2 Phytoplanktonassemblages 3.2.1 Compositionof cell concentrations 3.2.2 Compositionof phytoplankton carbon 3.2.3 Classificationanalysis and the identification of indicator species 3.2.4 The genus Chaetoceros: the formation and flux of resting spores 3.2.5. The Coscinodiscus gigas bloom 3.3 Sedimentationof phytoplankton Discussion 4. l Compositionof phytoplankton assemblages 4.2 Successionalversus sequential changes 4.3 Phytoplank-tonseeding mechanisms 4.4 Sedimentation:a phytoplanktonloss process Conclusions Acknowledgements References

40 41 41 42 42 42 42 42 43 43 43 45 45 47 53 53 55 57 57 58 59 60 62 62 62

1. INTRODUCTION Upwelling is a feature of oceanic circulation along the entire west coast of southern Africa (NELSONand HUTCHINGS, 1983). South of the Orange River, there are discrete sites ofupwelling, the most active of which include the Cape Columbine zone (NELSON and HUTCHINGS, 1983). Here episodic upwelling events occur throughout the summer in response to changes in wind stress (ANDREWSand HOTCH~GS, 1980) and result in the intermittent supply of upwelled water to St Helena Bay via a cyclonic gyre (DUNCANand NELL, 1969; HOLDEN, 1985). Numerous recent studies have demonstrated regulation of planktonic ecosystems by physical oceanographic processes (MACKAS,DENIVIANand ABBOrrr, 1985) In the Cape Columbine/St Helena Bay region, changes in the intensity and frequency of southerly winds drastically alter the hydrography and plankton distributions, creating a highly variable mesoscale environment (SHANNON,HUTCHINGS,BAILEYand SHELTON, 1984). Satellite images (SHANNON,MOSTERT, WALTERSand ANDERSON, 1983) have provided striking evidence of the correlation of biological and physical processes, along the west coast of southern Africa, and the interaction of these processes with bathymetry. In St Helena Bay itself, SHANNON, HUTCHINGS, BAILEY and SHELTON (1984) have observed high concentrations of chlorophyll a throughout the year, which have been assumed by BAILEY(1985) tO reflect the enhancement of primary production through the establishment of a semiclosed system on the leeward side of the Cape Columbine upwelling centre. As a result, St Helena Bay is a comparatively homogenous area (HUTCHINGS, 1981), where standing crops of phytoplankton and zooplankton are higher and more consistent than in the active upwelling area off the Cape Peninsula.

Anchorstationstudy:Phytoplanktondynamics

41

Various groups of algae are represented in marine phytoplankton populations, and their relative and absolute abundances, in terms of both numbers and biomass, can vary greatly in time and space. Few studies have been undertaken of the phytoplankton of the southern Benguela, and even fewer of the phytoplankton of St Helena Bay (DEJAGER, 1957; GRINDLEYand Nr~.l.L,1970; HORSTMAN, 1981; PITCHER, 1986, 1988). Furthermore, the methods used limited these earlier studies, to only the larger elements of selected taxonomic groups. The importance of the smaller phytoplankton, in terms of their abundance and productivity, has emerged with the application of new methods. DEJAGER(1957)examined phytoplankton samples collected at monthly intervals during 1954 using tow-nets and consequently missed many of the smaller forms ofphytoplankton. GRINDLEY and NELL (1970) reported on a red-water outbreak caused by the dinoflagellate Protoceratium reticulatum and HORSTMAN(1981) reported on red-water events recorded along the coast of South Africa, including some in the St Helena Bay region. PITCHER(1986) examined the sedimentary flux and the formation of resting spores of selected Chaetoceros species in St Helena Bay and offElands Bay. Later, PITCHER(1988) also examined the inter-relations between variability of the hydrographic field and the phytoplankton composition and distribution in St Helena Bay following an upwelling event. However, short-term phytoplankton community changes in response to environmental changes remained unresolved in the southern Benguela system. Continuous changes in the taxonomic composition of phytoplankton communities and the abundance and relative dominance of different species and algal groups is termed succession (SMAYDA, 1980). This process of continuous community reorganization is important in influencing the coupling between the phytoplankton community and the higher trophic levels. This study, therefore, examined the temporal variability of the phytoplankton assemblages at a single fixed station in St Helena Bay, in response to the environmental changes associated with coastal upwelling. The time series approach enabled phytoplankton assemblages to be monitored during consecutive periods of upwelling and relaxation in such a way that the time scales of responses of the assemblages could be discriminated. The role of sinking in the fate of the phytoplanklon populations was also examined. 2. METHODS The RS Benguela was anchored in 46~50m of water in St Helena Bay (32 ° 33.2'S; 18°05.312) from 19 March to 15 April 1987, providing a platform for the collection of a time series of data. 2.1 Physical, chemical and biological measurements Continuous temperature readings and salinity data were obtained at midday using a NeilBrown CTD and rosette sampler. The vertical stability of the water column was described in terms of a stratification index which was calculated as the vertical density gradient over the upper 30m of the water column. Nitrate and chlorophyll a concentrations were determined every four hours. Samples for the analysis of nitrate were taken at the approximate depths of 0, 5, 10, 20, 30, 37 and 43m and analysed on board according to the methods of MOSTERT (1983). Samples for chlorophyll a analysis were taken from selected depths, frozen, and analysed by spectrophotometric analysis (SCOR UNESCO, 1966).

42

G.C. PrromR et al.

2.2 Examination of phytoplankton assemblages 2.2.1. Identification and enumeration of phytoplankton. Water samples for the identification and enumeration of phytoplankton were collected daily at 5 depths, corresponding to the 100, 50, 25, 10 and 1% light levels, using a rosette sampler. Samples were fixed in 4% borate-buffered formalin and cells of 25ml subsamples were enumerated by the Utermthl method using an inverted microscope (HASLE, 1978). The large number of samples collected meant that only phytoplankton of samples from selected days and depths (e.g. those corresponding to the 100, 25 or 10 and 1% light levels) were counted. Cells were stained with Rose Bengal to enable the nanoplankton to be more easily detected. Selected phytoplankton subsamples were prepared for scanning electron microscopy to identify correctly certain species but even so many cells could only be assigned to genus or higher taxa. Most naked nanoplankton are not readily identifiable by light microscopy and were divided on the basis of size into general categories such as "small dinoflagellates" or "microflagellates". Phytoplankton biomass in terms of carbon was estimated indirectly from cell counts. Cell dimensions were measured to give cell volumes which were then converted to cell carbon using equations of STRATHMANN (1967) modified by EPPLEY,REID and STICKLAND(1970). 2.2.2 Classification analysis ofphytoplankton assemblages and the identification of indicator species. Classification analysis was used to group samples of similar phytoplankton composition, applying the methods of FIELD, CLARKE and WARWICK (1982). Root-root transformed abundance data, expressed in terms of numbers and carbon, were classified using the Bray-Curtis measure of similarity and group average sorting. Transformation was necessary because phytoplankton abundance data are usually skewed with very abundant or large species swamping the data set. Non-specific categories were included in the analysis. In the resulting dendograms, groups of samples were distinguished at arbitrary similarity levels. Information statistic tests (FIELD, CLARKE and WARWICK, 1982) were used to identify which species differ most between the selected groups of samples and can be considered indicator species responsible for the group separation in the classification analyses. 2.2.3 Collection of phytoplankton samples from the sediments. Box core samples were taken on the final day of the anchor station study. Samples were taken from the sediment/water interface of these cores and preserved in 4% formalin.

2.3 Phytoplankton cell, phytoplankton carbon and particulate organic carbon flux measurements Sediment traps similar to those described by KNAUER, MARTIN and BRULAND (1979) were suspended below the thermocline at 29 and 39m. Two of the four collection tubes were filled with a 5% formalin saturated solution of NaCl. Traps were deployed for periods ranging from 3-5 days for the entire duration of the study. Recoveries from the collection tubes containing formalin provided estimates of both cell and phytoplankton carbon flux. Particulate organic carbon flux measurements were determined on a CHN analyser from samples in the formalin free collection tubes.

Anchor station study: Phytoplanktondynamics

43

3. RESULTS

3.1 Physical, chemical and biological environment The anchor station was situated downstream of the Cape Columbine upwelling centre. At the anchor station site recently upwelled water was advected into the area on three occasions, namely 19/20 March, 10/11 April and 14/15 April (Fig. 1a) (BAILEYand CHAPMAN, 1991). Temperature differences between the sea surface and the bottom waters were small during these periods, indicating increased mixing. During subsequent relaxation the thermal gradients increased and the water column became more stable as the water column stratified owing to warming of the surface waters (Fig. 1a). Following the first advection event (19/20 March) the stratification index was small (0.019 c~t units m-t), but increased (>0.040 o~ units m -x, 5-10 April) during the period of relaxation. It again decreased following the second (0.031 oa units m -1, 11 April) and third (0.020 o~ units m -1, 15 April) advection events as colder water was introduced into the study area (Fig. 1a). Therefore three advection or upwelling events, signified by the intrusion of colder water, were observed during the 28 day anchor station study. The first of these events was followed by an extended period of relaxation whereas the second event was followed only by a very brief quiescent period prior to interruption by the third event. Below the thermocline the temperatures were uniform, indicating a particularly well mixed bottom layer (Fig. l a). The colder water, advected to the anchor station site subsequent to upwelling off Cape Columbine, was characterized by high nitrate concentrations (>5m mol m -3) (Fig. 1b). However, not only are these nitrate concentrations lower than those of newly upwelled water but also chlorophyll a concentrations were considerably higher than those characteristic of newly upwelled water (BARLOW, 1982) (Fig.lc). Thus there is probably significant growth by phytoplankton in the upwelled water prior to its advection into St Helena Bay. Two "phytoplankton blooms" were observed which were directly related to the intrusion of recently upwelled water into the study area. Following the first upwelling event stabilization of the water column was accompanied by an initial increase in the chlorophyll a concentrations, the formation of a subsurface chlorophyll a maximum and the eventual disappearance of the phytoplankton bloom from the euphoric zone. The period of relaxation was therefore eventually marked by low chlorophyll a concentrations (< 1mg m -3)and extensive nitrate limitation (< 1m mol m -3) in the surface waters (Fig. 1b and c). The second upwelling event was also followed by an increase in the chlorophyll a concentrations and the development of a subsurface chlorophyll a maximum. The progression of events was, however, terminated by the third upwelling event prior to nutrient limitation retarding bloom development.

3.2 Phytoplankton assemblages The phytoplankton counted during the anchor station study included members of the diatoms, dinoflagellates, a group referred to here as the microflagellates and a member of the ciliates. A total of 42 diatom species were identified, belonging to 16 genera. The genus Chaetoceros included 15 species, Thalassiosira 5 species, Nitzschia and Rhizosolenia 4 species each, and Coscinodiscus and Navicula 2 species each. The remaining genera incorporated the species

Asterionella glacialis, Bacteriastrum delicatulum, Biddulphia mobiliensis, Cerataulina bergonii, Ditylum brightwellii, Guinardia flaccida, Leptocylindrus danicus, Minidiscus trioculatus, Skeletonema costatum and Thalassionema nitzschioides.

44

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Anchor station study: Phytoplanktondynamics

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Many of the small dinoflagellates (<30~tm) were not specifically identified, so were considered as a single heterogeneous category. Of the larger dinoflagellates, 3 naked forms were identified, including Noctiluca miliaris, an Amphidinium species and a Gyrodinium species. The armoured forms included 4 Ceratium species, 4 Protoperidinium species, Dinophysis acuminata,

Protoceratium reticulatum, Prorocentrum micans, Zygabikodinium lenticulatum and a Polykrikos species. The microflagellates were grouped into three size categories; <6lxm, 6-12txm and > 12btm. The majority of the microflagellates, especially within the smaller size categories, were prymnesiophytes with a Chrysochromulina species being especially abundant. Also very common were the species Imantonia rotunda and Emiliania huxleyi. Many of the larger microflagellates were either cryptophytes or euglenophytes, some chrysophytes were also present. The photosynthetic ciliate, Mesodinium rubrum was also included in the phytoplankton counts. 3.2.1 Composition of cell concentrations. The taxonomic composition and size of the phytoplankton varied from one upwelling event to the next as well as during a single event. In order to examine the contribution of the higher taxonomic levels, cell counts were analysed according to the major groups - diatoms, dinoflagellates and microflagellates (Fig.2a). Diatom concentrations were high following the upwelling events (i.e. 20-26 March and 11-15 April). Thus colder (<15°C) well mixed (density gradient <0.035 o~ units m -l) surface waters favoured the presence of diatoms. This was particularly evident during the initial stages of the first intrusion of cold water, when a number of small diatom species were dominant. Diatom concentrations reached a maximum on the 23 March when 7.863x106cells 1-1 were recorded. During subsequent relaxation prior to the second intrusion of cold water, the surface waters warmed (> 15°C) and the water column became more stable (stratification index >0.035 o~ units m-l); diatom concentrations declined dramatically, sinking through the water column, until the surface waters were virtually devoid of diatom cells. Dinoflagellates occurred at most depths during most of the study at low concentrations; the highest concentration of 0.127x106 cells 11, was recorded on 14 April. Most samples were dominated numerically by the microflagellates, the exception being the period immediately following the initial upwelling event when diatom concentrations were greater. Microflagellate concentrations increased during the subsequent period of relaxation and became particularly abundant in the surface waters. A maximum concentration of 18,245x 106 cells 1-~ was recorded on 10 April when the surface water temperatures exceeded 16°C and the water column stratification index was high (0.043 o~ units m-l). Changes in phytoplankton abundance and size, were correlated with changes in the vertical stability of the water column, with the stratification index giving good qualitative prediction of the relative dominance of diatoms and flagellates. The growth of diatoms was favoured by a mixed water column with high levels of inorganic nutrients. Bloom diatoms were therefore the characteristic flora following upwelling. As the supply of upwelled water ended and the surface waters began to warm, the increased density gradient reduced vertical mixing by turbulence. As vertical transport was reduced, concentrations of inorganic nutrients fell sharply. The diatoms ceased to bloom and small flagellates dominated the phytoplankton. 3.2.2. Composition of phytoplankton carbon. Attributes ofphytoplankton populations, based on cell numbers overemphasize the importance of smaller forms, whereas when the attributes are based on cell volume the larger forms assume much greater importance. Here population biomass estimates have been made of the higher taxonomic levels, based on estimates of cell volume (Fig.2b).

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Anchor station study:Phytoplanktondynamics

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There were marked changes in phytoplankton biomass which were correlated with the upwelling events. Following the first event phytoplankton carbon concentrations were high throughout the water column. As the water column stabilized, a subsurface phytoplankton carbon maxima developed. The maximum phytoplankton carbon concentration of 549.9~tg C 1-1 was recorded at 9m depth on 28 March. Phytoplankton carbon concentrations fell to <100~tg C 1-1 when water column stratification reached its maximum and the diatom bloom disappeared from the surface waters. The second upwelling event on the 11 April was again accompanied by an increase in phytoplankton carbon concentrations attaining a maximum of 495.51xg C 1-1 at 13m depth on 13 April. Different components of the phytoplankton, in terms of carbon, were associated with each stage of the upwelling cycle. The pulses in the phytoplankton biomass were primarily caused by the diatom carbon fraction, which tended to be greater than the pulses in microflagellate and dinoflagellate biomass. In summary, the system progressed from a high biomass diatom bloom, in turbulent, nutrient rich water, to a flagellate community at much lower biomass levels in stratified, nutrient depleted water. 3.2.3 Classification analysis and the identification of indicator species. Dendograms illustrate the results of the classification analyses of the specific composition of the samples. For the analysis based on cell numbers, 6 groups of samples were distinguished at 58% level of similarity (Fig.3a), and one group was further subdivided at the 63% similarity level. The classification based on cell biomass distinguished 4 groups at 43% similarity (Fig.4a). The distributions of these groups of samples in time and space are illustrated in Figs.3b and 4b respectively. The six species identified by the information statistic tests as most important in separating the adjacent groups (in time and space) in Figs.3b and 4b are listed in Tables 1 and 2 respectively. The distributions of selected indicator species are shown in Fig.5. For the classification based on cell numbers, the periods following the first and second upwelling events were represented by Groups 1 and 4 respectively, whereas the period of relaxation was represented by Groups 2+3+5+6 (Fig.3b). Group 1 was characterized by a number of small diatoms, e.g.M, trioculatus (Fig.5a), a Nitzschia species and two small Thalassiosira species (Fig.5b). A number of Chaetoceros species, e.g.C, sociale (Fig.5c) and C. didymum (Fig.5d) were common in both Groups 1+2, but absent from Group 5 as were most diatom species. Samples of Groups 3+6 were separated from samples of the upper water column by the presence of a number of Chaetoceros resting spores, e.g.C, sociale RS (Fig.5f). Group 5 was characterized by low diatom concentrations and high microflagellate concentrations, and was divided into Groups 5a+5b on the basis of very high microflagellate concentrations in the samples of Group 5a, e.g. microflagellates <61.tm (Fig.5h) and microflagellates 6-12~tm (Fig.5i). Group 4 was characterized by high diatom concentrations, dominated by B. delicatulum (Fig.5g) and a number of Chaetoceros species e.g.C, sociale (Fig.5c), C. didymum (Fig.5d), C. constrictum and C. radicans. The dinoflagellate C. furca (Fig.5j) was also found to be characteristic of Group 4, whereas the ciliate M. rubrum (Fig.51) was characteristic of both Groups 1+4. For the classification based on cell biomass, the periods following the first and second upwelling events were represented by Groups 1 and 2 respectively, and the period of relaxation by Groups 3+4 (Fig.4b). With the emphasis on cell size, this analysis identified the larger Chaetoceros species, e.g.C, convolutum and C. Decipiens as the highest ranking indicator species of Group l. The presence of the very large diatom C. gigas (Fig.5e) in the samples of Groups 1+3, separated them from the samples of Group 4 from which C. gigas cells were absent. The

48

G.C. PrrclmR et al.

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Anchor station study: Phytoplankton dynamics

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15

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G.C. PITCHERet al.

TABLE 1. Results of information statistic tests showing the frequency scores, based on root-root transformed abundance data expressed in terms of cells 1l, of the first six indicator species which distinguish samples of adjacent groups in Fig.3b. The species are ranked according to the magnitude of the information statistic SPECIES

ADJACENT GROUPS

Minidiscus trioculatus Nitzschia sp. 1 Thalassiosira sp. 1 Thalassiosira sp.2 Mesodinium rubrum Chaetoceros diadema

Group 1 (N=18) 216 215 342 273 125 105

Group 2 (N=3) 0 0 15 9 0 0

Chaetoceros sociale Chaetoceros didymum Nitzschia delicatissima Cerataulina bergonii Chaetoceros compressum Chaetoceros sp.2

Group 2 (N=3) 32 38 33 15 13 10

Group 5b (N---11) 0 5 11 0 0 0

Chaetoceros sociale RS Chaetoceros sp. 1.RS Thalassiosira sp. 1 Asterionella glacialis Navicula sp.3 Chaetoceros sociale

Group 5b (N=I 1) 0 0 7 0 0 0

Group 3 (N=3) 61 26 31 17 16 17

Chaetoceros sociale RS Navicula sp.2 Nitzschia closterium Skeletonema costatum Bacteriastrum delicatulum Thalassiosira sp.2

Group 5b (N=ll) 0 0 8 0 9 6

Group 6 (N=10) 59 39 53 28 45 36

Microflagellates >12gm Microflagellates <6~tm Navicula sp. 1 Coscinodiscus gigas Bacteriastrum delicatulum Microflagellates 6-12~trn

Group 5b (N=I 1) 7 381 24 38 9 190

Group 5a (N--10) 47 526 0 4 36 262

Group 3 (N=3) 31 17 61 26 12 9

Group 6 (N=10) 0 0 59 9 0 0

Thalassiosira sp. 1 Chaetoceros sociale Chaetoceros sociale RS Chaetoceros sp. 1 RS Minidiscus trioculatus Polykrikos sp. 1

Anchor station study: Phytoplankton dynamics

51

Bacteriastrum delicatulum Chaetoceros sociale Chaetoceros didymum Chaetoceros constrictum Chaetoceros rach'cans Mesodinium rubrum

Group 5a (N=10) 36 0 0 0 0 0

Group 4 (N=8) 257 92 76 66 52 34

Bacteriastrum delicatulum Chaetoceros sociale Chaetoceros radicans Chaetoceros constrictum Chaetoceros didymum Ceratium furca

Group 4 (N=8) 257 92 52 66 76 53

Group 6 (N=10) 45 0 0 6 13 5

TABLE 2. Results of information statistic tests showing the frequency scores, based on root-root transformed abundance data expressed in terms of ~tgC 1-~, of the first six indicator species which distinguish samples of adjacent groups in Fig.4b. The species are ranked according to the magnitude of the information statistic SPECIES

ADJACENT GROUPS

Chaetoceros convolutum Chaetoceros decipiens Chaetoceros sociale Nitzschia sp. 1 Ebria sp. 1 Cerataulina bergonii

Group 1 (N=20) 114 163 134 73 72 68

Group 3 (N=14) 0 4 9 0 0 0

Group 1 (N=20) 368 163 148 144 134 124

Group4 (N=21)

Coscinodiscus gigas Chaetoceros decipiens Chaetoceros didymum Chaetoceros convolutum Chaetoceros sociale Thalassiosira sp. 1

Coscinodiscus gigas Chaetoceros sociale RS Coscinodiscus sp. 1 Gyrodinium sp. 1 Dinophysis acuminata Chaetoceros didymum

Group 3 (N= 14) 202 37 36 33 0 20

Group 4 (N=21 ) 54 3 4 4 35 0

Bacteriastrum delicatulum Chaetoceros constrictum Chaetoceros didymum Ceratiumfusus Chaetoceros sociale Thalassiosira aestivalis

Group 4 (N=21) 49 0 0 0 0 0

Group 2 (N=8) 167 49 45 32 31 28

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52

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Chaetoceros sociale" RS

":

FIG.5. A time series of selected indicator species (cells Hxl03). (a) Minidiscus trioculatus, (b) Thalassiosira sp. 1., (c) Chaetoceros sociale, (d) Chaetoceros didymum, (e) Coscinodiscus gigas, (f) Chaetoceros sociale RS, (g) Bacteriastrum delicatulum, Oa)Microflagellates <61im, (i) Microflagel lares 6-1211m, (j) Ceratium furca, (k) Dinophysis acuminata, (1) Mesodinium rubrum.

(I)

Anchor station study: Phytoplanktondynamics

53

appearance of the dinoflagellate D. acuminata (Fig.5k) in the samples of Group 4 was also responsible for separating the samples of this group from those of Group 3. B. delicatulum and several of the larger Chaetoceros species were characteristic of the samples following the second upwelling event, i.e. samples of Group 2. To conclude, following the first upwelling event the water column was initially dominated by a number of small diatom species, belonging to the genera Minidiscus, Thalassiosira and Nitzschia. They were succeeded by larger Chaetoceros species. The very large C. gigaspersisted, to eventually dominate the diatom population and was responsible for the development of the very high subsurface phytoplankton biomass maximum. As the period of relaxation progressed diatoms disappeared and large populations of microflagellates developed, dominated by members of the genus Chrysochromulina. Diatoms were again abundant following the second upwelling event, and many of the species common following the first event, were again present. On this occasion B. delicatulum dominated. Low dinoflagellate concentrations persisted during most of the study period, but were most abundant following the second upweUing event. Of the larger dinoflagellates, C. furca was most common. Also of interest was the appearance of the ciliate M. rubrum, following the upwelling events. 3.2.4. The genus Chaetoceros: the formation and flux of resting spores. The anchor station study provided an ideal opportunity to study the environmental conditions under which diatoms form resting spores and to investigate the role of these resting spores in an upwelling system. Fifteen Chaetoceros species were identified in the anchor station samples. Resting spore stages were common, especially in the thermocline region and bottom mixed layer. Mean concentrations of vegetative and spore stages within the euphoric zone were determined for 10 Chaetoceros species. The flux of both vegetative and resting spore stages from the euphoric zone was determined from sediment trap recoveries (Fig.6). Vegetative cells of Chaetoceros species were abundant following the upwelling events; some were present following all events, i.e.C, constrictum, C. curvisetum, C. diadema, C. didymum, C. radicans and C. sociale, whereas the others C. compressum, C. debilis and C. teres were present only following the first event. No vegetative cells of C. lorenzianum were detected although its resting spores occurred in the sediment traps deployed following the first upwelling event. The sediment trap material contained almost no vegetative cells, the exception being small numbers ofC. compressum, C. constrictum, C. curvisetum and C. didymum. Therefore, although the water column was dominated by vegetative cells, the evidence is that the flux from the upper mixed layer occurred largely in the form of resting spores. Except for a small number of C. constrictum, C. debilis, C. didymum and C. sociale spores remarkably few resting spores were found within the euphotic zone. Spores of these species were included when the depth of sampling extended down to the thermocline region and bottom mixed layer. Few phytoplankton cells were present in the sediment samples. Thus, although resting spores were sinking from the euphotic zone, they were not settling on the sediments, but must have been maintained within the bottom mixed layer. The presence of resting spores in the sediment traps when the euphoric zone was apparently devoid of either vegetative or resting spore stages, supports this hypothesis, although the greatest flux of spores usually corresponded to periods when the vegetative stages were most abundant in the euphoric zone. This finding in turn suggested that the sediment traps were overestimating the flux from the euphoric zone as they were collecting material that was either continually suspended in the bottom mixed layer or possibly resuspended from the sediments. 3.2.5. The Coscinodiscus gigas bloom. At the onset of the study, the highest concentrations of C. gigas (2.6x103 cells 1") were found in the surface waters. By 23 March a subsurface

G.C. Prrcri~ et al.

54

DATE

March 20 22 24 26 28 30 1 3

5

vegett tive [~

DATE March 20 22 24 26 28 30 1 3 5

April 7 9 11 13 15

resting sp....

MEAN CELL CONCENTRATION 1~'3 ~Logl0cells, m-3 x 105 ) 2

C.corr~ressum :::::::::9/......... ~ t l

C.constrictum

~ J ~

~

~

April 7 9 11 13 15

13

p///////z.z/~:~

MEAN CELL FLUX (Log 10celIs.m-2.d-ix10 6 )

MEAN CELL CONCENTRATION ( Log )ocells.m-3xlOS )

4

C. Iorenzianum

MEAN CELL FLUX

( Log~ce',~.m-2.d-~xl0~) 11"~

. . . . . . .

C.'cur~ise;um '

MEAN CELL CONCENTRATION

' ' --~

3~-

C. radicans

( Log~",.m-2.d-'~O ~) ~

.......

ANCELL !f

CONCENTRATIO~I ( Loglo celis.m-3x10 ) MEAN CELL

"qi

4

~ j~

~

~

I

........... C.socia e

( Log 10cells.m-2 .d-lxlO °)

II

43

Ati 1

FIG.6.

MEAN CELL

CONCENTRATION

4 '

'

C.teres

FLUX ~ 32 { L°glocells'm-2"d-lxlO~ 1

Mean cell concentrations of the vegetative and resting spore stages of selected

Chaetoceros species within the euphotic zone and the mean flux of these cells from the upper mixed layer as determined from sediment traps suspended in the water column at 29 and 39m.

maximum had developed, with concentrations exceeding 11.0xl03 cells 1-1. During the period of relaxation, C. gigas concentrations continued to increase after most other smaller diatoms had disappeared from the euphotic zone. On 2 April a maximum concentration o f 26.9x 103 cells 1-1 was recorded at 21m (Fig.5e). These high, subsurface C. gigas concentrations were largely responsible for the formation of subsurface chlorophyll a maxima exceeding 6 0 m g m s, and also contributed >90% of the highest phytoplankton carbon concentrations. The C. gigas concentrations, contoured versus depth and time (Fig.5e), show that the population was slowly sinking through the water column. The rate o f sinking appeared fairly constant at about 1.6md -1, although the rate increased towards the end o f the bloom. The C. gigas bloom disappeared from the euphotic zone on 5 April.

Anchor station study: Phytoplankton dynamics

55

The flux of both "living" and "empty" frustules of C. gigas, from the upper mixed layer was determined from the sediment trap recoveries (Table 3). The flux of "empty" frustules almost always exceeded that of the "living" cells. The flux tended to increase until a maximum flux of "living" cells was recorded during the period 4-7 April. This corresponded to the period when the C. gigas bloom finally disappeared from the euphotic zone. The maximum flux o f " e m p t y " frustules was recorded during the period 11-15 April, at the lower trap. This high flux is thought to have resulted from resuspension from the sediment. TABLE 3. Flux of Coscinodiscusgigas cells from the euphotic zone as determined by sediment trap recoveries Period and Depth of Deployment 19-24 March 29m 39m 24-29 March 29m 39m 29 M~u'ch-IApril 29m 39m 1-4 April 29m 39m 4-7 April 29m 39m 7-11 April 29m 39m 11-15 April 29m 39m

Flux of "living cells" Cells m-2d-lxl03

Flux of "empty frustules" Cells m-2d-txl03

279 51

1,573 1,192

I 10 413

743 2,779

592 254

254 4,310

905 388

2,888 2,112

5,423

7,773

1,418

8,795

66 199

3,752 40,972

3.3 Sedimentation of phytoplankton Recoveries from sediment traps suspended at 29 and 39m, provided estimates of both particulate organic carbon (POC) and phytoplankton carbon (PPC) flux (Table 4). The flux estimates of POC derived from the lower trap nearly always exceeded those from the upper trap. This was particularly the case during the periods following the upwelling events. The interpretation is that the bottom trap included resuspended material in its collections. The very high POC flux values of 6.1 and 5.0gC m-Zd-~measured by the 39m trap during the periods 19-24 March and 11-15 April respectively, are almost certainly the result of resuspension of material from the sediments, during the advection events. It is assumed therefore that the upper trap at 29m provided more accurate estimates of the fluxes from the euphotic zone.

56

G.C. PrrcnERet al.

TABLE 4. Mean primary production, particulate organic carbon (POC) flux and phytoplankton carbon (PPC) flux (as % of primary production in parentheses), the contribution of diatom biomass to the PPC flux and the contribution of PPC to POC flux, as determined by sediment trap recoveries Period and Mean primary Depth of Production in Deployment Euphotic Zone gC m-2d-1 19-24 March 29m 39m 24-29 March 29m 39m 29 March-1 April 29m 39m 1-4 April 29m 39m 4-7 April 29m 39m 7-11 April 29m 39m 11-15 April 29 39m

POC flux

PPC flux

Contribution Contribution of diatoms to of PPC to PPC flux POC flux (%) (%)

gC m2d-I

gC m2d-1

0.46 (14.0%) 6.10 (185.4%)

0.15 (4.6%) 0.21 (6.4%)

90.8 93.5

32.6 3.4

0.51 (13.2%) 0.73 (18.9%)

0.01(0.3%) 0.06 (1.6%)

83.8 93.5

2.0 8.3

0.19 (4.6%) 0.53 (12.8%)

0.04 (1.0%) 0.04 (1.0%)

82.4 88.8

21.1 7.5

0.47 (11.9%) 0.37 (9.4%)

0.05 (1.3%) 0.04 (1.0%)

89.2 87.0

10.6 10.8

0.67 (40.1%) 0.60 (35.9%)

0.23 (13.8%)

98.6 -

34.3

0.71 (32.0%) 0.80 (36.0%)

0.07 (3.2%)

95.0

8.8

0.79 (26.1%) 5.00 (165.0%)

0.03 (1.0%) 0.12 (4.0%)

60.6 83.5

3.8 2.4

3.29 3.87 4.14 3.95 1.67 2.22 3.03

When using sediment trap results to describe the fate o f phytoplankton, POC composition in the trap collections has to be considered. The percentage contribution o f intact phytoplankton cells to the total P O C flux was estimated (Table 4). Diatom cells, often in the form of resting spores, contributed usually in excess of 80%, to the PPC flux. The highest PPC flux of 0.23gC m-2d-1 corresponded to the period of mass sedimentation o f the C. gigas bloom. However, the contribution o f intact and apparently viable phytoplankton cells to the total P O C flux, was relatively small, ranging from 2.0-34.3%. In terms o f the primary production (M1TCHELL-INNES and WALKER, 1991) the flux of POC ranged from 4.6-40.1% of the organic material produced in the euphoric zone, ignoring the two values where considerable resuspension is thought to have occurred (Table 4). The PPC flux estimates were considerably less and ranged from 0.3-13.8% of the primary production (Table 4).

Anchor station study:Phytoplanktondynamics

57

4. DISCUSSION

4.1 Composition of phytoplankton assemblages Most of the phytoplankton species recorded during the anchor station study have been previously recorded in this area (DE JAGER, 1957; HORSTMAN, 1981; PITCHER, 1986, 1988), or elsewhere in similar environments. The important diatom genera found, especially following the upwelling events, included Bacteriastrum, Chaetoceros, Coscinodiscus, Minidiscus,Nitzschia, Skeletonema and Thalassiosira. DE JAGER (1957) described Chaetoceros, Nitzschia, Skeletonema and Thalassiosira as being dominant in the phytoplankton of St Helena Bay at times, and found Coscinodiscus species during most of the year but in high concentrations during March. Chaetoceros, Coscinodiscus and Thalassiosira are common to all the world's oceans and are the most species-rich and widespread genera (RINES and HARGRAVES, 1987). The genus Chaetoceros has been widely reported as seasonally dominant in diverse areas, including the Benguela Current (HARTand CURRIE, 1960). DE JAGER (1957) found Chaetoceros to be the dominant genus for most of the year, particularly during the summer months of November and December. PITCHER (1986) found the diatom population in both St Helena Bay and Elands Bay to be dominated by species of Chaetoceros, and although not dominant, several Chaetoceros species were important components of the phytoplankton in St Helena Bay during the studies of PITCHER(1988). RINESand HARGRAVES(1987) mention C. compressum, C. debilis and C. didymum, all of which were recorded during the anchor station study, as especially widespread and abundant. The genus Chaetoceros is therefore an important component of the phytoplankton in St Helena Bay, as it is in many neritic areas of the world's oceans, being both well represented numerically and also rich in species composition. Although DE JAGER (1957) mentioned neither Bacteriastrum and Minidiscus, PITCHER (1988) recorded both genera. Bacteriastrum delicatulum, which dominated the diatom community following the second upwelling event during the anchor station study, was also found by PITCHER (1988) to dominate the diatom bloom at certain stations in St Helena Bay. The species Minidiscus trioculatus, a dominant during the anchor station study, is most likely cosmopolitan in its distribution, although it is often not recorded because of its small size and the difficulty of identifying it without electron microscopy. Many of the smaller dinoflagellates occurring in this study were not identified. However, most of the larger dinoflagellates have been previously recorded in this region (PITCHER, 1988). Several of the commonly observed species, namely Noctiluca miliaris, Ceratiumfurca, Dinophysis acuminata, Protoceratium reticulatum, Prorocentrum micans and Protoperidinium trochoideum, have been reported to be responsible at times for red-water outbreaks in this region (HORSTMAN, 1981). The phytoplankton communities present during the latter stages of relaxation were characterized by a ubiquitous assemblage of tiny microflagellates which represent several algal classes. The small size of these nanoplankton and their inability to withstand preservation have previously frustrated efforts to quantify their importance. Only recently have these microflagellates been counted, and only rarely have they been identified; more often, they are recorded collectively as "flagellates" or "monads". The prymnesiophytes identified during the anchor station have been found to be both qualitatively and quantitatively dominant in coastal waters as well as oceanic regions, and species of Chrysochromulina have been reported to outgrow almost all other phytoplankton organisms (THOMSEN, 1986). The cryptophytes found during the present study have also been reported as

58

G.C. PrrcrmRet al.

well represented in the marine habitat and members of the Euglenophyceae, especially species of the genus Eutreptiella, found during the anchor station have been found to form dense blooms in coastal waters (THOMSEN, 1986). Similarly, members of the silicoflagellates, found during the anchor station study, have occasionally been reported to contribute significantly to the biomass and productivity of coastal areas (THOMSEN, 1986). The photosynthetic ciliate Mesodinium rubrum, common following the upwelling events during the anchor station study, has previously been recorded by HORSTMAN (1981) as responsible for red-water outbreaks in St Helena Bay and has been recorded by several other investigators as forming dense blooms covering large areas in other upwelling regions (BARBER and SMITH, 1981). As documented by MALONE(1980), nanoplankton biomass was less variable than netplankton biomass and increases in netplankton biomass were correlated with upwelling pulses. MALONE (1980) suggested that the constancy of nanoplankton biomass compared with that of netplankton could reflect a closer coupling between nanoplankton production and zooplankton. Furthermore the observation that netplankton blooms are greater in amplitude and occur more frequently in coastal waters could reflect the availability of seed populations of netplankton in bottom waters or sediments, and the frequency and duration of resuspension resulting from vertical mixing. 4.2 Successional versus sequential changes

It is widely recognised that there are cycles of phytoplankton abundance and successional changes in species composition in regions where there are distinct hydrographical changes (MARGALEF, 1958, 1962, 1967). Although a large number of independent factors are collectively involved in controlling these changes in the phytoplankton, progression in species composition results primarily from two different mechanisms (SMAYDA, 1980). Firstly succession, the change in species composition within a given water mass resulting from progressive changes in the physical, chemical and biological factors within a given water mass. Secondly sequence, the change in species composition resulting from a change in water-mass type. In true succession, autochthonous populations (i.e. original inhabitants) are involved, whereas allochthonous populations (i.e. introduced inhabitants) are involved in sequential changes. Both types of change were evident in the phytoplankton populations at the anchor station. Following the first upwelling event and subsequent period of relaxation, a "successional cycle" was observed, which started with mixing and high nutrient availability and ended with watermass stratification and low nutrient availability. The succession of the phytoplankton communities was closely associated with the vertical stability of the water column. As proposed by MARGALEF( 195 8, 1967), succession progressed from a predominance of small-celled diatoms with large area/volume ratios, to larger species with smaller ratios, followed then by a flagellate community. As noted by SMAYDA (1980), motile species representative of several classes followed the initial dominance of non-motile species. The size composition of the phytoplankton also responded somewhat predictably, large cells dominating the periods following upwelling and small cells during the periods of water-mass stratification (HOLLIGANand HARBOUR, 1977; PETERSON, ARCOS,MACMANUS,DAM, BELLANTONI,JOHNSON and TISELIUS, 1988). The predominance of flagellate species in stratified waters and diatoms in turbulent waters has been found in many field observations (SMAYDA, 1980). During this study, progression from a diatom bloom to a flagellate dominated community occurred within a few days. The increasing abundance of flagellates as nutrient levels declined may possibly result from an increased ability of microflagellates, to take up nutrients through motility.

Anchor station study: Phytoplanktondynamics

59

The species changes observed up until the end of the period of relaxation were not accompanied by any advective event or phenomena and were therefore a result of true successional changes. However, the dramatic change in the phytoplankton assemblage which occurred at the onset of the second upwelling event, resulted from a change in watermass type which disrupted succession and was therefore sequential in nature. Patterns of species succession are expected to be influenced by the frequency of environmental perturbations. Upwelling is such a perturbation and so can be expected to play an important role in determining the phasic nature of phytoplankton succession. Within an upwelling system GARRISON (1979) found that cycles of species dominance alternated as the result of interruptions of succession by upwelling pulses. The hydrographic conditions accompanying upwelling may often be detrimental to the occurrence of an autochthonous flora and its succession (SMAYDA, 1966), as wind-driven upwelling may become so intense that the autochthonous populations are continuously translocated. The evidence during this study of both successional and sequential changes in the species composition may result from St Helena Bay being a relatively shallow and less hydrodynamically active system. Therefore the ratio of autochthonous to allochthonous species is greater as there are less periodic incursions of different water-mass types and their associated flora.

4.3 Phytoplankton seeding mechanisms As established in this and other studies (SMETACEK, 1985), bloom diatoms are the characteristic flora of nutrient-rich water introduced to the surface layers following an upwelling event. Diatoms are, however, nonmotile and sink in nonturbulent surroundings. The success, therefore, of such pioneer species lies not only in their fast growth rates in nutrient-rich, turbulent conditions (MARGALEF,1978), but also in effective seeding of newly upwelled water by vegetative or resting stages from a previous population (MALONE, 1980). Thus the environment will select for both growth and seeding performances of the various species (SMETACEK, 1985). One way that planktonic diatoms may survive unfavourable environmental conditions is to form resting spores which will sink from the surface layers and repopulate overlying waters when conditions again become favourable. Upwelling regions and dynamic coastal systems are regions where one would expect resting spores to have a role as short-term survival stages (GARRISON, 1984). The anchor station study provided an opportunity to examine the role of resting spores in natural population cycles, as the spores were easily associated with the parent population and the conditions under which the spores were formed. Many environmental variables have been implicated as contributory to the inducement of formation of resting spores. Nitrogen deficiency has been found to be a causative factor in triggering the formation of resting spores more often than any other single variable. However, as found by PITCHER (1986), the formation of resting spores was not limited to periods of low concentrations of nutrients. The greatest trap recoveries of spores corresponded to the peak abundances of the vegetative stages in the plankton. Resting spore formation therefore preceded the decline or disappearance of a species from the phytoplankton, but did not necessarily correspond to periods of poor growth conditions. During the present study and the study of PITCHER (1986), resting spores of diatoms formed a major component of the phytoplankton settling from the euphotic zone. The large number of resting spores and the virtual absence of vegetative cells in the sediment traps in both studies, suggested that the sinking rates of the resting stages far exceeded those of the vegetative stages. Alternately, the absence of resting stages in the euphotic zone, suggested that accelerated sinking

60

G.C. PrrcrmRet al.

accompanied by the formation of resting spores rapidly removed the population from the euphotic zone. This rapid sinking of diatom resting spores ensures the regional persistence of neritic assemblages. GRAN (1912) suggested that resting spores settle locally and persist through unfavourable periods as benthic resting stages. PITCHER (1986) found high concentrations of diatom resting spores in the surface sediments in St Helena Bay and off Elands Bay, so here too the sediments may retain seed stock, hence the success of the Chaetoceros species in consistently contributing to high phytoplankton standing crops in this region. During the anchor station study, although spores were common in deeper waters, they were absent from the sediments. Either the turbulence was sufficient to maintain the spores suspended within the bottom mixed layer or benthic grazers were consuming the spores as fast as they settled onto the sediments. HARGRAVESand FRENCH (1975) similarly found in sediment cores from Narragansett Bay, Rhode Island, that spores occurred in the sediments after blooms, but did not persist for more than a few weeks, either as living spores or empty thecae. Nevertheless, the accumulation of diatom resting spores in the region of the thermocline and bottom mixed layer during the anchor station study, ensured the restoration of cells to the surface layer by restricted mixing events. Thus the introduction of spores could be from a pelagic rather than a benthic environment, and spores would be able to seed water after mixing and recurrent upwelling events within a single season as suggested by GARRISON (1981 ). The presence of resting spores in newly upwelled surface waters in St Helena Bay (PITCHER, 1988) confirmed the ability of spores to utilize the prevalent mixing and current patterns to seed upwelling waters and thereby increase their reproductive success in a physically dynamic environment. The presence of a number of spore producing Chaetoceros species following the first and second upwelling events during the anchor station study, again confirms the success of these species in seeding upwelling waters. In addition to the large number of diatom resting spores collected in the sediment traps, a number of dinoflagellate cysts were also present, especially those ofProtoceratium reticulatum, a dinoflagellate species known to be responsible for red water blooms in this region (GRINDLEY and NELL, 1970). Again, the absence of motile stages and the presence of cysts only in the sediment traps suggests that cysts sink to the bottom and probably seed a new population of motile stages during favourable periods in such a fluctuating environment. Also of interest during the anchor station study, was the presence of Mesodinium rubrum during the two upwelling events, thus demonstrating its ability to seed these new environments. Although this study provided no evidence of the mechanisms involved, BARBER and SMITH (1981) have suggested that the diel vertical migration pattern of Mesodinium rubrum, whereby it may migrate downward into onshore subsurface flow, is an effective mechanism for maintaining this species in an upwelling system. 4.4 Sedimentation: a phytoplankton loss process

The disappearance of a large phytoplankton stock can be brought about by any of four factors: (1) dispersal, by horizontal and/or deep vertical mixing; (2) zooplankton grazing; (3) natural mortality and plasma breakdown within the surface layers; and (4) the sinking of cells to deeper water layers or the bottom (BODUNGEN,SMETACEK,TILZER and ZEITZSCI-IEL, 1986). Rapid, mass sedimentation of phytoplankton cells following surface blooms has been observed (SMETACEK,1985) and WALSH(1983) has provided evidence showing that this process,

Anchor station study: Phytoplanktondynamics

61

particularly along continental margins, may represent one of the major global sinks of carbon and nitrogen. The sedimentation of algae has therefore been suggested as an important controlling factor in the size of the algal standing crop, and in the production of organic matter. Furthermore, sinking may be an important factor in the succession of phytoplankton (WALSBYand REYNOLDS, 1980). Trap collections provide a measure of the potential sinking behaviour of a given phytoplankton population. Considerable caution is generally required in the interpretation of trap catches, especially in their application to phytoplankton population dynamics. During the anchor station study, the upper sediment trap usually collected less material than the lower trap. Similar findings have been made by SMETACEK,BROCKEL,ZEITZSCHELand ZENK (1978) who ascribed this paradox to diminishing current speeds with depth, concommitant with an increase in the sinking rates of phytoplankton and phytodetritus. However, during the anchor station study, differences in the flux between the upper and lower traps were sufficiently great to suggest that resuspension from the sediments was a more likely explanation. Nevertheless, the greater number of resting spores and cysts compared to vegetative cells in the trap collections compared to the water column indicates that the traps do not accumulate particles indiscriminately from their immediate environmenl. During the anchor station study, losses resulting from the sinking of intact phytoplankton of variable taxonomic composition were estimated under a variety of environmental conditions. As a result, estimates of the percentage primary production sinking from the euphotic zone ranged from 0.3-13.8%. Phytoplankton carbon flux estimates made from SETCOL measurements during the final l0 days of the anchor station (PITCHER,WALKERand MITCHELL-INN~, 1989) were in general agreement with the above estimates. During most of the study, losses from sinking were less than4% of the primary production. Only during the mass sedimentation of C. gigas cells and Chaetoceros cells in the form of resting spores did losses exceed 4%. These estimates are similar to those of other recent studies (BEINFANG, 1984, 1985) and would appear to indicate that the sinking of intact phytoplankton is of limited importance to changes in the phytoplankton biomass. In a preliminary carbon budget of the southern Benguela upwelling system, BERGH, FIELD and SHANNON (1985) suggested that 75% of the phytoplankton production is either decomposed in the water column or exported to be deposited on the sea floor. Losses during the anchor station study resulting from dispersal are suspected to have been minimal and estimates of losses resulting from grazing (VERHEYE, 1991) were also low. Therefore the natural mortality and breakdown of phytoplankton cells within the surface layers may have been the most important factor in accounting for the phytoplankton biomass decline. This is supported by the finding that most of the C. gigas cells sank from the euphoric zone as "empty" frustules rather than "living" cells. Despite the limited importance of sinking in determining phytoplankton biomass, the passive sinking of phytoplankton may have a significant impact on the composition of the phytoplankton due to the variable sinking rates of the different components of the assemblages (PITCHER, WALKERand M1T HELL-INNES, 1989). In particular, the onset of thermal stratification often results in the replacement of heavy non-motile diatoms by motile or buoyant species (WALSBY and REYNOLDS, 1980). In this respect, a number of changes in the species composition of the phytoplankton during the anchor station study may have resulted from the interrelation between turbulence and variable sinking rates. This was particularly important in determining the vertical distribution of the Chaetoceros and Coscinodiscus cells.

62

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5. CONCLUSIONS Changes in the phytoplankton community were strongly influenced by the hydrodynamic processes, both through turbulent redistribution of existing biological variability and through the creation of variability in the richness and suitability of the physical and chemical environment. Purely biological forcing mechanisms such as predator-prey oscillations did not appear to be as important as biological-physical interactions in regulating phytoplankton changes. A sequence of populations resulted from the orderly shift of the environment, as turbulence dissipated during the period of relaxation subsequent to upwelling. Dramatic changes in species dynamics over a short period of time were associated with periods of upwelling. Changes in the phytoplankton community with time typically remained unpredictable at the species level, but showed systematic trends in the dominance patterns of higher taxonomic levels such as diatoms, dinoflagellates and microflagellates. Populations at different stages of the upwelling cycle therefore differed markedly in the size distribution of their components. This has implications for the ability o f sizeselective predators to find adequate nutritional resources, thus influencing food chain dynamics and fisheries. 6. ACKNOWLEDGEMENTS We gratefully acknowledge all the participants of the anchor station experiment, especially Mr G.W. Balley and Dr P. Chapman. Appreciation is extended to the officers and crew of the RV Benguela. We also acknowledge the criticisms of the manuscript by Drs L. Hutchings and J.J. Bolton. 7. REFERENCES ANDREWS, W.R.H. and L. HUTCHINGS (1980) Upwelling in the southern Benguela Current. Progress in Oceanography, 9, 1-81. BAILEY, G.W. (1985) Distribution and cycling of nutrients at four sites in the Benguela system. In: Simposio internacional sombre las areas de afloramiento mas importantes del Oeste Africano (Cabo Blanco y Benguela), C. BAS, R. MARGALEF and P. RUBIES, editors, Barcelona, Instituto de lnvestigaciones

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