Phytoplankton and foraminiferal frequencies in northern Indian Ocean and Red Sea surface waters

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Netherlands Journal of Sea Research 24 (4): 531-539 (1989)

PHYTOPLANKTON AND FORAMINIFERAL FREQUENCIES IN NORTHERN INDIAN OCEAN AND RED SEA SURFACE WATERS ANNELIES KLEIJNE 1, DICK KROON 1 and WANDA ZEVENBOOM 2, 3* IGeomarine Centre Amsterdam, Institute of Earth Sciences, Free University, RO. Box 7161, 1007 MC Amsterdam, The Netherlands 2Laboratory for Microbiology, University of Amsterdam, Nieuwe Achtergracht 127, 1018 WS Amsterdam, The Netherlands 3Netherlands Institute for Sea Research, RO. Box 59, 1790 AB Den Burg, Texel, The Netherlands

ABSTRACT

1. INTRODUCTION

This paper describes the distribution patterns of living planktonic foraminifers, coccolithophorids and picocyanobacteria along an east-west traverse in northern Indian Ocean and Red Sea surface waters during the southwestern monsoon. The absolute frequencies of coccoiithophorids and foraminifers more or less correlated with temperature in the western Arabian Sea and South of India, where deeper waters well up into the photic zone. The increased frequencies in these upweUing zones were especially accounted for by the coccolithophorids Emiliania huxleyi (Lohmann) Hay & Mohler, Gephyrocapsa oceanica Kamptner and the foraminifer Globigerina bulloides d'Orbigny. The coccolithophorids Umbellosphaera irregularis Paasche and U. tenuis (Kamptner) Paasche showed a preference for warm, oligotrophic waters, and were absent in the upwelling areas. The small, red-pigmented picocyanobacteria in surface waters (depth 0 to 5 m) formed an important part of the primary production. Their relative frequency was more or less constant, on an average of 2.10 7 cells.dm -3 along the entire transect, so their relative contribution to biomass was higher in nutrient-poor environments than in nutrient-rich upwelling waters. Both carbonate producing foraminifera and coccolithophorids increase in number with improved nutrient availability in the upwelling areas. Their relative frequencies in sediments underlying the upwelling zones will reflect the varying upwelling conditions, caused by fluctuations in monsoonal atmospheric circulation, and thus allow for the reconstruction of past climatic change in this area.

Northern Indian Ocean surface water circulation is characterized by a seasonal reversal in flow direction, as a result of the changes in monsoonal winds. During the southwestern monsoon (June-September) cyclonic circulation in the Arabian Sea and the Bay of Bengal causes nutrient-poor Red Sea surface water to flow into the Arabian Sea (WYRTKI, 1973) and a strong eastward drift occurs in the equatorial area. As a result upwelling takes place off the African, Arabian and southwestern Indian coasts. During the northeastern monsoon (December-March) the circulation is anticyclonic. These changing hydrographical conditions were expected to have a direct biological response in the plankton composition. To determine this effect, cruise Gx of the Snellius-II Expedition (homeward voyage of R.V. 'Tyro' from Indonesia to The Netherlands, June-July 1985) took surface samples from the northern Indian Ocean and Red Sea during upwelling conditions. We studied the distribution of foraminifers and of two phytoplankton groups: the coccolithophorids (Prymnesiophyceae) and the small coccoid cyanobacteria (picocyanobacteria). The red-pigmented picocyanobacteria (<1 #rn) only recently have been shown to form an important component of low latitude ocean primary productivity (WATERBURY et al., 1979; JOHNSON & SIEBURTH, 1979), especially in the lower part of the euphotic zone (ZEVENBOOM, 1986a; 1989). Their abundance is probably related to relatively high temperatures (EL HAG & FOGG, 1986; GUlLLARD et al., 1985; MURPHY & HAUGEN, 1985). Their contribution to the biomass is thought to be greater in oligotrophic, low chlorophyll a waters than in waters with higher nutrient availability (inshore waters) (TAKAHASHI et al., 1985; WATERBURY & VALOIS, 1982; ZEVENBOOM &

*present address: North Sea Directorate, Rijkswaterstaat, RO. Box 5807, 2280 HV Rijswijk, The Netherlands

532

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Fig. 1. Location map of sampling stations during R.V. 'Tyro' cruise Gx, in the Indian Ocean and Red Sea surface waters. Numbered dots (Gx-) and squares (P-) represent studied coccolithophorid samples and picocyanobacteria/biomass samples respectively. Foraminifers were studied of samples Gx-84 to Gx-160 only. WETSTEYN, 1990). Coccolithophorids are one of the characteristic phytoplankton groups in marine tropical environments, and in e.g. the equatorial Pacific Ocean the standing crop is relatively high (OKADA & HONJO, 1973). They may occasionally form blooms, usually composed of one or two species, at middle and high latitudes, and in upwelling areas (MITCHELL-INNES & WINTER, 1987). Coccolithophorids have been shown to be sensitive indicators of water masses (MCINTYRE & BE, 1967), but their behaviour in upwelling areas is still poorly known. Emiliania huxleyi (Lohmann) Hay & Mohler is the most wide-spread and numerically important species (MCINTYRE & BE, 1967; OKADA & MCINTYRE, 1977), which blooms in areas with improved nutrient availability, especially in middle and high latitudes (MITCHELL-INNES & WINTER, 1987). Gephyrocapsa oceanica Kamptner is characteristic for tropical to transitional zones (MCINTYRE & BE, 1967) and prefers warm waters and marginal seas (OKADA & HONJO, 1975), but may also be found in upwelling areas, especially at low latitudes (VMINTER, 1982; MITCHELL-INNES & WINTER, 1987). The planktonic foraminifer Globigerina bulloides d'Orbigny is known to bloom in areas of enhanced productivity and high nutrient levels (BE, 1977; AURA$-SCHUDNAGIES et al., 1990; KROON, 1990). The absolute frequency of this species is negatively relat-

ed to temperature values (AURAS-SCHUDNAGIES et al., 1990), which have been used as an indicator of upwelling waters during cruise Gx. The northern Indian Ocean, with important upwelling areas South of India and off the Somalian and Arabian coasts, provides an ideal setting for studying the effects of changing hydrographical conditions on the distribution of the plankton groups. The calcareous skeletons of coccolithophorids and foraminifers in the sediments are extensively used in biostratigraphy, palaeoecological studies and palaeoceanography. The objective of this study is to quantify relationships of species frequencies with hydrographic properties, to improve the resolution of palaeoenvironmental reconstruction. Acknowledgements.--We are indebted to J.E. van Hinte for initiating cruise Gx, and to the captain and crew of the R.V. 'Tyro' and B. Engbrenghof for their help during cruise Gx. We thank the staffs of the Department of Electron Microscopy and Molecular Cytology of the University of Amsterdam, and of the Netherlands Geological Survey, for permission to use their SEM. We thank G.J. Boekschoten, J.E. van Hinte, and J.J. Zijlstra for valuable comments on the manuscript. Research was carried out as part of the Snellius-II Expedition, organized by the Indonesian Institute of

PLANKTON FREQUENCIES IN INDIAN OCEAN AND RED SEA

Science (LIPI) and the Netherlands Council of Oceanic Research (NRZ), and was supported by the Netherlands Foundation for the Advancement of Tropical Research (WOTRO, grant W83-71) and the Netherlands Organisation for the Advancement of Pure Science (ZWO, grant W84-76). 2. MATERIAL AND METHODS Samples were taken aboard the Dutch R.V. 'Tyro', between June 16 and July 11 1985, during cruise Gx from Indonesia to The Netherlands, as part of the Indonesian-Dutch Snellius-II Expedition (Fig.l). Two sets of plankton net and water samples, which were prefiltered through a 5 mm sieve, were obtained with a seawater pump from the upper five metres of the water column, at regular time intervals during the non-stop journey; one set for biomass and cyanobacterial determinations (P-1 to P-48) and one set for foraminifer and coccolithophorid determinations (Gx-1 to Gx-160). Seawater temperature and salinity were measured at every station. Nutrient data are taken from WYRTKI (1971). 2.1. PHYTOPLANKTON BIOMASS AND PICOCYANOBACTERIA Samples were immediately passed through a 30 #m filter, and then concentrated using a continuous flow system (ZEVENBOOM, 1986a). A high concentration factor (200 to 500 times) and large sample volumes (100 to 300 dm 3) were required, since the biomass content was relatively low. The microbial biomass was determined in #g.dm -3 by weighing washed, freeze-dried pellets of a measured volume of concentrated ( < 3 0 #m) sample. Samples 27, 32, 33 and 45 were not analysed. In vivo absorption spectra of concentrated ( < 3 0 #m) samples were examined over a range of wavelengths (500 to 750 nm). Most of the marine picocyanobacteria are phycoerythrin (red-pigment)containing Synechococcus-type species (WATERBURY et al., 1979). The peak-height of the distinct maximum at 545 nm was used as a tracer, to enumerate the concentration of these species present in natural phytoplankton communities, according to the methods described by ZEVENBOOM (1986a). 2.2. COCCOLITHOPHORIDS By means of a vacuum pump 10 to 45 dm 3 of the surface samples were passed through 1.0 #m Nuclepore filters. The filters of 77 samples (numbered 6-160 in Fig. 1) were examined with a Scanning Electron Microscope. The standing crop per dm 3 of water was determined by counting and identifying coc-

533

cospheres as well as coccoliths, converting the latter to coccosphere numbers (KLEIJNE, 1990). 2.3. FORAMINIFERS Per surface sample 9 to 107 m 3 of seawater were filtered through plankton nets ( > 7 5 ~.m). The residues were preserved in alcohol (for full procedures see KROON & KLEIJNE, 1986). We determined total planktonic foraminiferal numbers and the frequency of G. bulloides of all 77 samples between locations Gx-84 and Gx-160 (Fig. 1). 3. RESULTS 3.1. TEMPERATURE AND NUTRIENTS Surface water temperature values decreased from the northeastern Indian Ocean towards the area south of India, with a gradual decrease in the eastern part and a stronger gradient from station Gx-44 onwards (Fig. 2a). Following a sharp rise, a second drop in temperature was found in the western Arabian Sea, from India towards the Somalian coast of Africa. These temperature gradients record the influence of the injected, relatively cold sub-surface waters of the upwelling centres off the African coast and South of India, which are transported eastward by the Monsoon Drift. Highest temperatures were measured in the southern part of the Red Sea, while in the northern part temperature values decreased towards the Gulf of Suez. Avarage July phosphate and nitrate values in the surface water (Figs 2b and 2c) are highest in the areas south of India and in the western Arabian Sea and Gulf of Aden (from: WYRTKI, 1971). However, the in situ nutrient concentrations are no reliable indicators for nutrient limiting conditions, since they are the resultants of the nutrient fluxes, determined by supply and uptake rates (ZEVENBOOM, 1986b). 3.2. BIOMASS Microbial biomass values ( < 3 0 #m) ranged from 12 to 153 #g.dm-3, as shown in Fig. 2d. The figure also shows that the values were in general higher at the end of the day (17.00 h, evening samples) than in morning samples (7.00 h), which is due to increase of cellular carbohydrate levels by photosynthesis (POSTMA & ROMMETS, 1984; ZEVENBOOM & WETSTEYN, 1990). In the northern Indian Ocean biomass values increased towards India, showing a broad peak in the area south of India and decreased in the Arabian Sea. In the western Arabian Sea a smaller increase of the biomass was found near Africa. The

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PLANKTON FREQUENCIES IN INDIAN OCEAN AND RED SEA

535

3.3.2. COCCOLITHOPHORIDS

Gulf of Aden and Red Sea samples had low values, except for stations P-41, just north of the Strait of Bab-eI-Mandeb, and P-48, in the Gulf of Suez.

The coccolithophorid standing crop ranged from 2 to 110-103 cells.dm-3, and tends to show an inverse relation with the temperature curve. The geographical distributions of the four most frequent species is given in Fig. 3. Emiliania huxleyi (Fig. 3a) and Gephyrocapsa oceanica (Fig. 3b) largely accounted for the high standing crops. Both species increased in frequency, and are indicative for upwelling conditions, but E. huxleyi was the predominant species in the western Arabian Sea and G. oceanica in the area South of India. Our data suggest that G. oceanica blooms at lower salinities than E. huxleyi. This is confirmed by a sharp increase in frequency of E. huxleyi in Gulf of Suez waters, at relatively low temperatures and extremely high salinities (40.8-41.8 S). In the Gulf of Aden, where G. oceanica and E. huxleyi were only scarcely recorded, Umbellosphaera irregularis Paasche and Umbellosphaera tenuis (Kamptner) Paasche increased in frequency towards the Red Sea, and also away from the upwelling area in the northeastern Indian Ocean (Figs 3c and 3d).

3.3. ABUNDANCE OF PLANKTON GROUPS 3.3.1. PICOCYANOBACTERIA The small(< 1 /tiT1) red-pigmented picocyanobacteria were observed at all stations in concentrations up to 3.3 -107cells.dm -3, except for stations P-3 and P-48 with concentrations below 103 cells.dm -3 (Fig. 2e). In the northeastern Indian Ocean the morning samples showed higher values than the evening samples. The opposite was found in the Red Sea, while between stations P-15 and P-38 no general trend was observed. Fig. 2e shows little variation in concentrations along the transect: only a gradual decrease towards the Strait of Bab-eI-Mandeb, somewhat higher values in the Red Sea stations P-41 and P-43, and a decrease in the Red Sea to undetectable levels in Gulf of Suez inshore waters.

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3.3.3. FORAMINIFERS

4.1. MICROBIAL BIOMASS

Foraminifers showed highest frequencies in the upwelling waters of the western Arabian Sea and north of the Strait of Bab-eI-Mandeb (Fig. 2g). The presence of the non-spinose species Globorotalia menardii (Parker, Jones and Brady) and Neogloboquadrina dutertrei (d'Orbigny) in Red Sea surface waters documents a net inflow of surface waters from the Arabian Sea into the Gulf of Aden and subsequently over the Strait of Bab-eI-Mandeb into the Red Sea (AURAS-SCHUDNAGIES et al., 1990). G. bulloides was the predominant species in Arabian Sea upwelling waters (Fig. 2h).

Microbial biomass ( < 3 0 #m) showed increased values in the upwelling areas. It is known that 1 #g of picocyanobacterial cells contains 106 cells (ZEVENBOOM, 1986a). If we assume an average weight for a picocyanobacterial cell of 10 -3 times that of a coccolithophorid cell (diameter 1:10), then it follows that 1 /~g of coccolithophorid cells contains 103 cells. Since picocyanobacterial numbers are on average 500 to 1000 times the coccolithophorid numbers (Figs 2e and 2f), the coccolithophorid biomass contribution is equal, to twice that of the picocyanobacteria. However, in the upwelling areas south of India and in the western Arabian Sea, coccolithophorids form up to about 5 times the picocyanobacterial contribution to the biomass. Differences between calculated contributions by the two phytoplankton groups and measured biomass values (Fig. 4) may be caused by small cells of other plankton groups. They may also be the result of spatial patchiness in the distribution of these phytoplankton groups.

4. DISCUSSION The cruise results indicate southwest-monsoon upwelling conditions in the western Arabian Sea and the area south of India, characterized by decreased temperature and increased biomass values (Figs 2a and 2d). We compared distribution patterns and frequencies of various plankton groups in different sets of samples. P- and Gx-samples were collected from different stations on the transect, with varying physico-chemical conditions, and represent only temporary situations over a period of 26 days. Therefore, the observed variation in picocyanobacteria and coccolithophorid frequencies and biomass values, as is shown in Fig. 4, may well be caused by spatial and temporal patchiness.

4.2. PICOCYANOBACTERIA The picocyanobacteria concentration was more or less constant along the entire transect, regardless of variation in environmental conditions. The picocyanobacterial concentration at the surface does not even respond to the upwelling conditions along the transect. Different results were obtained by ZEVEN-

PLANKTON FREQUENCIES IN INDIAN OCEAN AND RED SEA

BOOM (1990) in the eastern Banda Sea, where higher absolute numbers but a lower relative importance of picocyanobacteria occurred during the upwelling season than during the downwelling season. The fact that we only sampled the surface layer (0 to 5 m), and that picocyanobacteria show a preference for deeper layers of the euphotic zone (ZEVENBOOM, 1986a; ZEVENBOOM & WETSTEYN, 1990), may explain the absence of a correlation with upwelling. The alternation of highest picocyanobacterial concentrations in morning and in evening samples may be caused by patchiness in their distribution. Another explanation may be that in certain areas measurements virtually revealed lower cell numbers in the evening, due to a decrease in cellular phycoerythrin concentration (photo-bleaching) in this tropical area, where cells are fully exposed to sunlight (ZEVENBOOM, 1986a; 1990).

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mass ( < 3 0 am) peak in this area may express the presence of large numbers of small diatoms. In the western Arabian Sea, where the measured minimum temperature was somewhat higher than in the first area, we passed presumably in between the upwelling regions off the Arabian and Somalian coasts, and sampled only the outside edges of the upwelling plumes. SMITH & CODISPOTI (1980) found a dominance of diatoms in the centre of the upwelling area off the Somalian coast. More mature upwelled water at the edges of upwelling areas yields a different phytoplankton composition (DUGDALE, 1983), which is in correspondence with our results. The decreasing influence of the upwelled water in the western Arabian Sea that is transported offshore by the Somali Current, resulted in a gradual decrease in coccolithophorid frequency. The abrupt decrease in cell numbers between stations Gx-108 and Gx-110 indicates the crossing of the centre of a local upwelling 4.3. COCCOLITHOPHORIDS area in the Gulf of Aden, since again high numbers of diatoms were found at its stations Gx-110 to Gx-114; The recorded distribution patterns of the four most compare situation south of India. The high standing frequent coccolithophorid species do characterize crop at station Gx-158 in the Gulf of Suez was caused the successive unstable upwelling and stable water by E. huxleyi, also abundant in surface sediments conditions. Coccolithophorid standing crop was from the Gulf of Aqaba and the northern Red Sea highest (up to 110.103 cells.dm -3) in upwelling (WINTER, 1982). The increasing latitude and the acareas, with G. oceanica as the most frequently occurcompanying lower temperatures, in combination with ring species along the sampling transect, followed by locally occurring upwelling (diatoms were abundant E. huxleyi. This confirms results obtained from other at stations Gx-159 and Gx-160), account for the inupwelling areas (summarized by MITCHELL-INNES & creased frequency of this species. The relative frequencies of U. irregularis and U. WINTER, 1987). The recorded standing crop values are not exceptionally high, since considerably higher tenuis show a negative correlation with upwelling values at the surface were reported from other upwel- conditions, indicating that these species prefer ling areas (max. 3.15.106 cells.dm-3in low latitudes; oligotrophic waters. U. irregularis is one of the most max. 6.8.106 cells.dm -3 in mid-latitudes; 115.106 common species in tropical waters. Its known cells-dm -3 in high latitudes; MITCHELL-INNES & distribution is restricted to water temperatures of 21 WINTER, 1987). to 28°C (MClNTYRE & B~:, 1967). We found highest numbers at temperatures above 27°C in the Indian Maximum standing crop values south of India do Ocean, and especially between 29 and 31°C in the not correspond with the centre of the upwelling, while Red Sea. The distribution of U. tenuis is known to in the western Arabian Sea maximum values coincide with the lowest temperatures. This, however, overlap that of U. irregularis, and to range into higher does not necessarily indicate that we sampled the latitudes up to the 16°C-isotherm (MCINTYRE & BE, 1967; OKADA & MCINTYRE,1977). It was found in concentre of the upwelling. In the first area large numsiderable numbers in the Gulf of Aden and the Red bers of diatoms were present on the nannoplankton filters from stations with lowest temperature values, Sea, mainly at temperatures above 29°C. Neither in contrast with the latter area. Generally, diatoms are species was recorded from the upwelling areas, although temperatures stayed well within their range, the predominant phytoplankton in young upwelled indicating that they prefer oligotrophic conditions, water (SMITH & CODISPOTI, 1980; DUGDALE, 1983). and that their distribution is not determined by temCoccolithophorids bloom in more mature upwelled water, although exceptions may occur (MITCHELL- perature alone. INNES & WINTER, 1987). The differences in 4.4. FORAMINIFERS predominant phytoplankton groups between both areas may be the result of different phases in the upwelling cycle and the biological responses along the The planktonic foraminifer G. bulloides blooms in sampling transect. South of India we sampled the waters with enhanced productivity and high nutrient availablity, its frequency following the rhythm and incentre of the upwelling, with high numbers of diatoms at stations Gx-51 to Gx-56. The high and broad bio- tensity of the upwelling pulses (BE, 1977). The

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A. KLEIJNE, D. KROON & W. ZEVENBOOM

observed frequencies reflect the influence of upwelled nutrient-rich deep water to the surface layer in the western Arabian Sea. G. bulloides is enriched in (~130 in the upwelling zones (KROON & GANSSEN, 1989). This indicates that the species finds its optimum occurrence once the phytoplankton blooms have fully developed. 5. CONCLUSIONS Picocyanobacteria contribute to a large extent to the primary production, but form a relatively small part of the surface water phytoplankton biomass since they prefer deeper water layers. In our surface samples their abundance and contribution to biomass do not show a clear relation with upwelling. Frequencies of foraminifers and coccolithophorids broadly correlate with cool, eutrophic conditions of upwelling areas. Highest frequencies occurred at the edges of these areas, while in the centres, as was measured south of India, diatoms were the dominating phytoplankton group and coccotithophorids were only present in low numbers. Increased frequencies of the carbonate producing foraminifers and coccolithophorids in the surface layers of upwelled waters, as a result of the high nutrient avaliability, are reflected in the sedimentary record as high relative frequencies of opportunistic species like Emiliania huxleyi, Gephyrocapsa oceanica and Globigerina bulloides. The warm water, oligotrophic species Umbellosphaera irregularis and U. tenuis were mainly found at temperatures above 27°C, and were absent in the upwelling areas. The nutrient composition (SiO2/NO 3 ratio) depends on the source (depth) of upwelling, and determines the predominant plankton group in the upwelling area (DUGDALE, 1983). The succession of the groups and species is shown in their lateral distribution, with coccolithophorids and foraminifers at some distance from the centre of upwelling in the more mature waters that are transported offshore. Therefore, the distribution pattern of the plankton groups in the sediments of the upwelling area can be used for tracing nutrient composition. Thus, fluctuations in the upwelling system caused by changing source waters and varying atmospheric and oceanic conditions can be traced. 6. REFERENCES AURAS-SCHUDNAGIES,A., D. KROON, G. GANSSEN, C. HEMLEBEN & J.E. VAN HINTE, 1990. Biogeographic evidence for Red Sea anti-monsoonal surface currents.--Deep-Sea Res. (in press). B~:, A.W.H., 1977. An ecological, zoogeographic and taxonomic review of recent planktonic Foraminifera. In:

A.T.S. RAMSEY.Ocean micropaleontology. Acad. Press London, New York, San Francisco: 1-88. DUGDALE,R.C., 1983. Effects of source nutrient concentrations and nutrient regeneration on production of organic matter in coastal upwelling centres. In: J. THIEDE & E. SUESS. Coastal upwelling. Part A. Plenum Press, New York & London: 175-182. EL HAG, A.G.D. & G.E. FOGG, 1986. The distribution of coccoid blue-green algae (Cyanoacteria) in the Menai Straits and the Irish Sea.--Br. phycol. J. 21: 45-54. GUILLARD, R.R.L., L.S. MURPHY, P. FOSS & S. LIAAENJENSEN, 1985. Synechococcus spp. as likely zeaxanthin-dominant ultraphytoplankton in the North Atlantic.--Limnol. Oceanogr. 30: 412-414. JOHNSON, e.w. & J. MCN. SIEBURTH, 1979. Chrococcoid cyanobacteria in the sea.--Limnol. Oceanogr. 24: 928-935. KROON, D, 1990. Distribution of extant planktonic foraminiferal assemblages in Red Sea and northern Indian Ocean surface waters.--Rev. Esp. Micropal. (in press). KROON, D. & G. GANSSEN, 1989. Northern Indian Ocean upwelling cells and the stable isotope composition of living planktonic foraminifers.--Deep-Sea Res. 36: 1219-1236. KROON, O. & A. KLEIJNE, 1986. Variation of skeletal phenotypes and stable isotope ratios in different watermasses. In: Homeward voyage Tanjung Priok - Den Helder, R.V. Tyro, via Indian Ocean and Mediterranean Sea, June 14-August 2 1985. The Snellius-II Expedition Progress Report, Royal Netherlands Academy of Arts and Sciences and Indonesian Institute of Sciences: 7.1-7.48. MCINTYRE, A. & A.W.H. B~=, 1967. Modern Coccolithophoridae of the Atlantic Ocean.-1. Placoliths and Cyrtoliths.--Deep-Sea Res. 14: 561-597. MITCHELL-INNES,B.A. & A. WINTER,1987. Coccolithophores: a major phytoplankton component in mature upwelled waters off the Cape Peninsula, South Africa in march, 1983.--Mar. Biol. 95: 25-30. MURPHY, L.S. & E.M. HAUGEN, 1985. The distribution and abundance of phototrophic ultraplankton in the North Atlantic.--Limnol. Oceanogr. 30: 47-58. OKADA, H. & S. HONJO, 1973. The distribution of coccolithophorids in the Pacific.--Deep-Sea Res. 20: 355-374. , 1975. Distribution of coccolithophores in marginal seas along the western Pacific Ocean and in the Red Sea.--Mar. Biol. 31: 271-285. OKADA, H & A. MCINTYRE,1977. Modern coccolithophores of the Pacific and North Atlantic Oceans.-Micropaleontology 23: 1-55. POSTMA, H. & J.W. ROMMETS, 1984. Variations of particulate organic carbon in the central North Sea.--Neth. J. Sea Res. 18: 31-50. SMITH, S.L. & L.A. CODISPOTI,1980. Southwest monsoon of 1979: chemical and biological response of Somali Current coastal waters.--Science 209: 597-600. TAKAHASHI, M., K. KIKUCHI & Y. HARA, 1985. Importance of picocyanobacteria biomass (unicellular, blue-green algae) in the phytoplankton population of the coastal waters off Japan.--Mar. Biol. 89: 63-69.

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WATERBURY, J.B. & EW. VALOIS, 1982. The contribution of Synechococcus to oceanic primary productivity, abstr. IV Int. Symp. Photosynthetic Prokaryotes A 41. WATERBURY, J.B., S.W. WATSON, R.R. GUILLARD & L.E. BRAND, 1979. Widespread occurrence of a unicellular, marine, planktonic cyanobacterium.--Nature 277: 293-294. WINTER, A., 1982. Paleoenvironmental interpretation of Quaternary coccolith assemblages from the Gulf of 'Aqaba (Elat), Red Sea.--Rev. Esp. Micropal. 14: 291-314. WYRTKI, K., 1971. Oceanographic atlas of the International Indian Ocean Expedition. Nat. Sci. Found. Washington, D.C.: 1-542. ,1973. Physical oceanography of the Indian Ocean. In: B. ZEITZSCHEL& S.A. GERLACH.The biology of the In-

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dian Ocean. Springer Verlag, Berlin, Heidelberg, New York: 18-36. ZEVENBOOM, W., 1986a. Tracing red-pigmented marine cyanobacteria using in vivo absorption maxima.-FEMS Microbiol. Ecol. 38: 267-275. ----, 1986b. Ecophysiology of nutrient uptake, photosynthesis, and growth. In: T. PLATT & W.K.W. LI. Photosynthetic picoplankton.--Can. Bull. Fish. Aquat. Sci. 214: 391-422. ----, 1990. Picocyanobacteria in the Banda Sea during two different monsoons.--Proc. Snellius-II Symp., Neth. J. Sea Res. (in press). ZEVENBOOM, W. & F. WETSTEYN, 1990. Growth limitation and growth rates of pico-phytoplankton in the Banda Sea during two different monsoons.--Proc. Snellius-II Symp., Neth. J. Sea Res. (in press).