Phytoplankton Assemblages in the Deep Chlorophyll Maximum Layers Off the Mediterranean Coast of Israel

Journal of Plankton Research Vol.9 no.3 pp.433-443, 1987

Phytoplankton assemblages in the deep chlorophyll maximum layers off the Mediterranean coast of Israel

B.Kimor1, T.Berman2 and A.Schneller2 'Technion — Israel Institute of Technology, Haifa 32000, Israel 2Israel Oceanographic and Limnological Research, Haifa, Israel

Abstract. Phytoplankton assemblages in the deep chlorophyll maximum and near-surface layers were com-

pared at seven stations in the inshore and offshore waters of the Mediterranean coast of Israel. The study Downloaded from https://academic.oup.com/plankt/article/9/3/433/1573786 by guest on 27 September 2021 included the entire spectrum of taxonomic categories over a wide size range, comprising the nano/pico phytoplankton components down to 1 /im and the larger phytoplankters consisting primarily of diatoms and dinoflagellates. The coccolithophorids <20 »un and the monads constituted the most abundant components of the phytoplankton at the deep chlorophyll maximum (DCM) and near surface layer. Certain individual species, mainly pennate diatoms and smaller dinoflagellates, seemed to adapt to the DCM to form a characteristic association.

Introduction A quantitative species analysis of the phytoplankton populations off the Mediterranean coast of Israel was carried out during the years 1981 -1983 within the framework of a comprehensive research program dealing with the biological productivity of the eastern Mediterranean. At all pelagic stations (> 100 m) occupied during four cruises, designated as AID 1 —4 (Figure 1), a deep chlorophyll maximum (DCM) was observed at depths ranging

33° MEDITERRANEAN

2-IV

32°

31°

30° 34° Fig. 1. Location map of AID-DCM stations.

CWI"* 0,1 Q2 OJ 02 OJ 02 OJ 02

2-21 50-

O0- CO-

150-

o 0 Downloaded from https://academic.oup.com/plankt/article/9/3/433/1573786 by guest on 27 September 2021

50-

co-

B0-

Fig. 2. Chlorophyll profiles at the DCM stations (AID cruises 1-4). between 75 and 125 m (Berman et al., 1984). In these layers, the chlorophyll concentrations ranged from 0.09 to 0.21 /xg I"1 as compared to near surface (NS) concentrations of 0.03-0.07 /ig I"1 (Figure 2). The presence of a DCM layer has similarly been reported from the waters off the Egyptian coast (Dowidar, 1984). These findings are in accord with the results of an earlier study of the plankton of the eastern Mediterranean (Kimor and Wood, 1975), when it was found that the phytoplankton peaks, based on cell counts, occurred at 80—100 m. This depth corresponds roughly with the base of the euphotic zone, although the DCM is occasionally located either above or below the 1 % surface irradiance level. In view of this salient feature in the distribution of chlorophyll within the water column, it was decided to compare the species composition of the phytoplankton communities at the two layers on the basis of the numerical abundance of the principal components.

Stations and methods The samples examined in the present investigation were collected at seven stations during four cruises: AID-1 — AID-3 on the R/V Shikmona and AID-4 on the fishery trawler Nitzan (Figure 1 and Table I). Chlorophyll and phaeophytin concentrations were determined by fluorometry (Turner Designs 10 Fluorometer, calibrated with chlorophyll a by Sigma) in discrete samples which were concentrated by filtering 100 ml through BA83 0.2 /tm Schleicher and Schull membrane filters and then extracted into 90% acetone (Azov, 1986). At the low pigment concentration levels which were often en- countered (<0.1 /ig Chi al'1), the precision of this technique was about ±25% (Ber- man et al., 1984; Azov, 1986). Samples were collected at NS and 3 x Secchi depth, 434 Phytoplankton species in Mediterranean DCM layers

Table I. Dates and location of pelagic (> 100 m) stations, Secchi depth, DCM depths and chlorophyll concentrations at DCM and NSL levels (AID cruises 1 -4).

Station Date Location Secchi Z. Chi. max ChJ DCM Chi NSL (m) (m) %' %'

1-V 28 Jul 1981 32-35'57'N 37 100 (125)b 0.09 nd 0.03 nd 34°31'23"E 1-K 3OJul 1981 3!*56'38"N 41 125 (100) 0.21 nd 0.03 nd 34°27'42"E 2-IV 12 Dec 1981 32*25'00"N 45 75 (123) 0.16 76 0.07 74 32°17'OO'E 2-VI 13 Dec 1981 32°OO'OO'N 45 100 (100) 0.17 88 - 32°32'OO'E Downloaded from https://academic.oup.com/plankt/article/9/3/433/1573786 by guest on 27 September 2021 3-VI 11 Apr 1982 31°50'07"N 33 100 (100) 0.14 63 0.03 84 33°54'O8'E 3-vn 12 Apr 1982 32°18'OO"N 39 100 (125) 0.17 86 0.03 82 33°O2'OO"E 4-VI 20 Jul 1982 32°29'07'N 41 100 (100) 0.09 85 0.04 55 34°39'01"E

*% picoplsnkton < 3 /un. ''Numbers in parentheses represent the 3 x Secchi depth where sampling for phytoplankton was carried out. nd " no data. corresponding roughly to 1% of surface irradiance. As the chlorophyll determinations were performed at a later stage, the samples nearest to the DCM were subsequently analyzed for their phytoplankton composition. A total of 13 samples thus formed the basis of this study (one sample from ABD-3 was contaminated). Borate-buffered for- malin was used as a fixative and preservative, and was added to the samples on board ship to produce a final concentration of 4%. Two-liter samples were used for the subse- quent sedimentation and concentration procedures in the laboratory in accordance with Utermohl (1958). Aliquots from the concentrated samples were allowed to settle for at least 48 h in 50 ml cylinders, after which the numerical abundance of the phytoplankton components was determined in four radial transects and the results expressed as cells I"1. A Zeiss Invertoscope type D was used at x250 and X400 magnification for the counts of cells larger and smaller than 10 /an, respectively, in accordance with UNESCO (1978). Due to time constraints and the intention of the authors to study the whole size spectrum of the phytoplankton components, no special techniques were used for the enumeration of the picoplankton represented primarily by the monads. It is therefore presumed that the figures obtained in the enumeration of these forms are underestimated compared with the results of other investigators (Murphy and Haugen, 1985). Recent counts by us of the picoplankton by the epifluorescence technique described below suggest an underestimate of about three orders of magnitude. The monads, which were numerically dominant (Table II), were subsequently observed in freshly collected samples on 0.2-/xm pore size Nuclepore filters. They were iden- tified as cyanobacteria by bright orange fluorescence in observations carried out under an epifluorescence microscope type 14 with an IV—FL epifluorescence condenser fit- ted with a filter set of Exciter-510-560 nm, Dichroic mirror 580 nm and barrier filter 435 •fc.

Table II. Densities and percentage composition of the phytoplankton categories at the deep chlorophyll maxima recorded at seven stations (AID cruises 1 -4).

Station Diatoms Dinoflagellates Monads Coccolithophorids SilicoflaRellates Other groups Density % Density % Density % Density % Density % Density % (cells I"1) (cells I"1) (cells I"1) (cells 1"') (cells r1) (cells r1)

1-V 291 18 90 11 970 60 163 10 _ - 12 1 1-IX _1 - 47 5 846 89 56 4 - - 18 2 2-IV 147 2 25 0.3 9651 97 13 0.1 13 0.1 64 0.5 2-VI 70 1.6 83 1.9 2860 64 1443 32 6.4 0.1 19 0.4 3-VI 1174 76 376 24 3289 23 9979 67 - - - - 3-VI1 308 16 25 1.0 616 33 919 50 - - - - 4-VI 759 0.6 398 0.2 110 925 96 3860 3.2 26 0.1 190 0

*-, sporadic occurrence (>0.05 cells 1~').

Table in. Densities and percentage composition of the phytoplankton categories at the near surface recorded at seven stations (AID cruises 1 -4).

Station Diatoms Dinoflagellates Monads Coccolithophorids Silicoflagellates Other groups Density % Density % Density % Density % Density % Density % (cells 1"') (cells I"1) (cells I"1) (cells I"1) (cells I"1) (cells P1)

1-V 69 3.9 282 16 1035 58 388 22 _ 0 2.3 0.1 1-IX 10 1.0 20 2 900 90 10 1 - 0 60 6 2-IV 270 1.3 146 0.6 20 431 91 1553 7 6.1 0.02 12 0.04 2-VI 71 1.2 71 1.2 3902 67 1750 30 13 0.4 6.5 0.2 3-VI 382 4.0 269 2.8 1635 18 6872 75 - 0 14 0.2 3-V1I no data

4-VI 261 0.3 370 0.5 80 154 97 1840 2.2 41 0 0 0 Downloaded from https://academic.oup.com/plankt/article/9/3/433/1573786 by guest on 27 September 2021 September 27 on guest by https://academic.oup.com/plankt/article/9/3/433/1573786 from Downloaded Phytoplankton species in Mediterranean DCM layers

590 nm. Furthermore, these cells gave yellow fluorescence under a filter set of Exciter- G-436 nm, Dichroic mirror FT-150 nm and barrier filter LP-520 nm, used for the identification of chlorophyll a fluorescence. The data relating to the composition of the phytoplankton communities at the DCM layer from settled samples were supplemented by on-board qualitative examinations of live phytoplankton samples obtained by the Amiad differential filtration apparatus (Berman and Kimor, 1983). The principal literature sources used in the identification of the phytoplankton are given following the reference section of this paper. For a more detailed taxonomic listing of the phytoplankton components considered in this study, the reader is referred to Kimor and Wood (1975). Downloaded from https://academic.oup.com/plankt/article/9/3/433/1573786 by guest on 27 September 2021

Results The coccolithophorids and the monads represented the greatest percentage composition numerically of the nano and picoplankton, respectively. As such, these two were the most abundant of the six phytoplankton categories studied in the course of this investigation, and formed the bulk of the total phytoplankton (Tables II—IV and Figure 3). With the exception of two samples taken from the DCM at stations 3-VI and 3-VII (April 1982), the monads were dominant in the DCM layer. Similarly, the monads constituted the dominant component of the phytoplankton in the near surface layer (NSL), with the exception of station 3-VI where the coccolithophorids reached higher abundances at the expense of the monads. The monads were of a coccoid type, appearing either singly or in aggregates of a few cells, and varied in size between 1 and 3 tan. No attempt was made to establish the taxonomic position of these tiny cells, although in light of the absence of a well- defined nucleus and the colour of the plasma, it may be assumed that they are cyanobacteria. Fluorescence characteristics of cells containing phycoerythrin/phycocyanin, as observed by epifluorescence microscopy, tended to support this view. In order to ascertain whether the phytoplankton assemblage at the DCM differed from that at the NSL, the abundance and the species composition were compared. The results of a statistical test (one-way ANOVA) to check the differences between the two layers showed no significant differences in regard to the five major phytoplank-

Table IV. Percentage composition of the combined nanoplankton and picoplankton (Na + Pi) and chlorophyll of the total phytoplankton at seven deep chlorophyll maxima and near surface locations (AID cruises 1 -4).

Stations Na + Pi * Chi Na + Pi % Chi at DCM at NSL

1-V 71.00 n.d.1 80.00 n.d. 1-IX 95.00 n.d. 91.00 n.d. 2-rv 97.07 76 98.02 74 2-VI 96.03 88 97.40 - 3-VI 90.00 63 93.00 84 3-VII 83.00 86 n.d. 82 4-VI 99.03 85 97.00 55

•n.d. " no data. 437 B.Kimor, T.Berman and A.Schneller

Monodl M Oinoftageflarot • COUNTS OF MONADS INCLUDE COCOUITHOPHORIOS < Oum mm SUicofbgtQotac + CoccolHhophordM ™ Othtr groupi

OoTDmcoi \ | Minor continuants

AID I AID AC n AID IV

„ st V St IX St IV St. VI St. VI StVII st. VI 0 100 Otpitv I 0 125 0 00 0 125 0 100 0 00 125 Itl (m) lOO-i

80- Downloaded from https://academic.oup.com/plankt/article/9/3/433/1573786 by guest on 27 September 2021

60-

40-

20- [

Fig. 3. Percentage composition of the various plankton taxonomic groups (Utermdhl technique) at the DCM and near surface levels.

ton groups considered in this study (diatoms, dinoflagellates, monads, coccolithophorids and others) (Table IH). At the same time, the chlorophyll a levels in the two layers were significantly different, with P = 1.41 X 10~4 ) (Table I). In order to distinguish between the contribution of the phytoplankton < 65 /tm and the fraction > 65 inn, a list of taxa in decreasing order of abundance in these two size categories was drawn up for the two depth levels at the seven stations (Tables Va and b). Generally there seemed to be predominance of pennate over centric diatoms at the DCM, the latter often being more abundant at the NSL. Among the pennate diatoms, naviculoid forms were the most common, often accompanied by Thalassiothrix frauenfeldii and Nitzschia seriata. The centric diatoms recorded in the NSL were representative species of the Rhizosolenia — Chaetoceros association characteristic of the eastern Mediterranean (Kimor, 1983,1985). Among the dinoflagellates, Gymnodinium sp. prevailed in the NSL although recorded occasionally at the DCM. The presence of Oxytoxum sp. at 4 out of the 7 DCM stations does not necessarily confirm the offshore character of this genus, as stressed by Steidinger and Williams (1970). Among the taxa >65 /un, the occurrence of Halosphaera viridis phycomata was recorded chiefly at the DCM layer (5/7 stations), although the morphology of the cells at this level did not differ from that at the NSL. While its occurrence at both levels points to its eurybathic character, H. viridis shows a distinct preference for the deeper levels (Wiebe et al., 1974; Kimor and Wood, 1975). The presence of the coccolithophorid Calciosolenia murrayi at only two offshore sta-

438 Phytoplankton species in Mediterranean DCM layers

Table Va. Species composition of the phytoplankton at DCM (AID cruises 1 -4) in decreasing order of abundance (cells I"1).

Station Larger phytoplankton Density Nano/picoplankton Density (>65 Mm) (cells I"1) (cells P1)

1-V Navicula spp. 199 Monads 970 Prorocentrum scutellum 72 Coccolithophorids (10-20 urn) 126 Synedra sp. 27 Halosphaera viridis 12

i-rx Halosphaera viridis 18 Monads 846 Gymnodinium sp. 9.2 Coccolithophorids (10-20 /im) 18

Coccolithophorids (20-30 /un) 18 Downloaded from https://academic.oup.com/plankt/article/9/3/433/1573786 by guest on 27 September 2021

2-rv Naviculinae 83 Monads* 9650 Halosphaera viridis 64 Dictyocha fibula 13 Rhizosolenia spp. 26 Oxytazum sp. 19 Schroederella delicatula 19

2-VI Gymnodinium sp. 64 Monads* 2860 Naviculinae 45 Coccolithophorids (< 10 pm) 1225 Halosphaera viridis 19 Coccolithophorids (10-20 fim) 115 Rhizosolenia spp. 19 Syracosphaera sp. 45 Oxytoxum sp. 13 Rhabdosphaera claviger 26

3-VI Thalassiothrix frauenfeldii 485 Coccolithophorids (< 10 /un) 9304 Chaetoceros spp. 425 Monads 3289 Oxytoxum spp. 235 Calciosolenia murrayi 88 Nitzschia seriata 133 Discosphaera thompsonii 88 Prorocentrum micans 47 Naviculinae 44

3-vn Chaetoceros spp. 83 Coccolithophorids (<10 iim) 842 Naviculinae 45 Monads 616 Thalassiothrix frauenfeldii 58 Calciosolenia murrayi 19 Rhizosolenia sp. 51 Corythodinium constrictum 19

4-VI Asterionella glacialis 244 Monads 111 000 Naviculinae 219 Coccolithophorids (< 10 >im) 3500 Gymnodinium sp. 205 Discosphaera thompsonii 89 Oxytoxum sp. 180 Halosphaera viridis 180 Rhizosolenia spp. 89 Thalassiothrix frauenfeldii 64 Nitzschia longissima 52 Gyrosigma sp. 39

"Monads + coccolithophorids > 10 /un. tions, 3-VI and 3-VII, is of interest since this species is typically associated with warm water oceanic environments and as such was expected to be found at all stations. Reid el al. (1978) also noted the absence of this species from warm water oceanic stations

439 B.Kimor, T.Bernuui and A.Schneller

Table Vb. Species composition of the phytoplankton at near surface (AID cruises 1 -4) in decreasing order of abundance (cells I"1).

Station Larger phytoplankton Density Nano/picoplankton Density (>65 fjrn) (cells I"1) (cells I"1)

1-IV Prorocentrum compressum 111 Monads 1035 Cymnodinium sp. 74 Coccolithophorids (10-20 /im) 370

1-IX Gioeocapsa sp. 60 Monads 900 Diploneis sp. 10 Syracosphaera sp. 10

2-IV Chaetoceros spp. 110 Monads 20 430 Cymnodinium sp. 55 Coccolithophorids ( < 10 /im) 1255 Downloaded from https://academic.oup.com/plankt/article/9/3/433/1573786 by guest on 27 September 2021 Naviculinae 25 Coccolithophorids (10-20 /un) 135 Rhizosolenia spp. 18 Coccolithophorids (>20 ;un) 49

2-Vl Cymnodinium sp. 32 Monads' 3900 Oxytoxum sp. 32 Coccolithophorids ( < 10 nm) 1432 Chaetoceros spp. 19 Coccolithophorids (10-20 jim) 117 Ophiaster hydroideus 104 Rhabdosphaera claviger 45 Discosphaera sp. 39

3-VI Thalassiothrix frauenfeldii 256 Coccolithophoridae (< 10 >un) 6362 Cymnodinium sp. 207 Monads 1635 Oxytoxum sp. 41 Discosphaera thompsonii 248 Leptocylindrus danicus 28 Naviculinae 28 Halosphaera viridis 14

3-vn Sample contaminated

4-VI Gymnodinium sp. 178 Monads 80 150 Oxytoxum sp. 164 Coccolithophorids (< 10 /im) 1485 Rhizosolenia spp. 68 Naviculinae 55 Nitzschia longissima 14

•Monads + coccolithophorids > 10 /un.

off southern California where its occurrence was normally expected. The smaller phytoplankton recorded by the Amiad differential filtration apparatus in a night sample collected at station 2-VII on December 13, 1981 provided additional information (Berman and Kimor, 1983) on the structure of the phytoplankton assemblages at the DCM layer which included, among others, such known photosynthetic taxa as Corythodinium conscriptum, Prorocentrum compressum and Scrippsiella trochoidea.

Discussion and conclusions This study is a further attempt to describe the phytoplankton assemblages of the DCM layer in the eastern Mediterranean waters (Kimor and Wood, 1975). 440 Phytoplankton species in Mediterranean DCM layers

In view of the highly oligotrophic character of these waters (Berman et al., 1984), it was deemed desirable to analyze the structure of the phytoplankton populations at this level as a potential source of food and energy to herbivorous zooplankton in the pelagic food chain. The smallest particles in the phytoplankton spectrum, primarily the monads and the coccolithophorids smaller than 20 nm, proved to be predominant on the basis of their numerical abundance and their contribution to total chlorophyll concentrations and photosynthetic activity (Berman et al., 1984). Similar results have been reported for many marine regions by other investigators (Beers et al., 1975; Ber- man, 1975; Waterbury et al., 1979; Li et al., 1982; Takahashi and Hori, 1984). However, in view of the slow rate of settlement of the monads, even after 48 h prior to the enumeration procedure, it is possible that the figures obtained for this fraction Downloaded from https://academic.oup.com/plankt/article/9/3/433/1573786 by guest on 27 September 2021 of the phytoplankton may be underestimated. On a percentage composition basis, greater differences were observed between various stations occupied during the same cruise than between the two depth levels within the same water column (1-V and 1-IX, Figure 3), probably due to the variability of this aquatic environment. While no apparent differences could be established between the abundances of the major taxonomic groups in the DCM and NSL of the water column at the seven stations, significant differences between the two layers were determined for chlorophyll a. We note that the higher values of chlorophyll concentration measured in the DCM may not actually reflect greater phytoplankton biomass, but merely represent the higher intracellular chlorophyll level due to photo-adaptation to decreased light irradiance, as discussed also by Raymont (1980, p. 94). On the other hand, the species composition of the larger sized phytoplankton populations at the DCM layer differed from that of the NSL, as reported also by Beers et al. (1975), from their study of the microplank- ton of the North Pacific Central Gyre, and by Venrick (1982). Qualitative differences between the two layers are particularly apparent for the diatoms. The pennate forms such as Nitzschia seriata and Asterionella glacialis recorded at the DCM were absent from the NSL. Thalassiothrix frauenfeldii reached a concentration of 485 cells P1 at the DCM at 3-VII, but decreased considerably in numbers at the NSL. No obvious differences in species composition of the dinoflagellate populations could be observed at the two levels. The occurrence" of the prasinophycean Halosphaera viridis at only the DCM at the four stations occupied during the first two AID cruises points to the shade-adapted characteristics of this species (Kimor and Wood, 1975; Sournia, 1982). It is also worthwhile mentioning the close resemblance in the gross percentage composition of the major taxonomic groups between stations 1-IX and 4-VI. These stations are fairly close together geographically, although they were occupied at a time dif- ference of 1 year during the same season. This similar pattern in the composition of the major taxonomic groups was not supported by similar levels of chlorophyll and cell numbers of the leading taxa (Tables Va and b; Figures 2 and 3). The data gathered from the study of the phytoplankton populations in the DCM layer at the seven stations may not be sufficient for drawing definite conclusions. We have seen DCM layers on further cruises (AID-6) but not in February (AID-5 and AID-7). Maybe this layer is destroyed during winter mixing. In spite of the predominance of monads and coccolithophorids at all stations, the occurrence of some salient phyto- 441 B.Kimor, T.Berman and A.SchneUer plankton assemblages at the DCM layer would indicate the need for continuing these observations in greater detail.

Acknowledgements The authors wish to express their thanks and appreciation to J.R.Beers, S.Z.El-Sayed, F.M.H.Reid, P.D.Walline and L.Weber, for the critical reading of this manuscript.

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Becrs^.R., Reid.F.M.H. and Stewart.G.L. (1975) Micropiankton of the North Pacific Central Gyre. Population Downloaded from https://academic.oup.com/plankt/article/9/3/433/1573786 by guest on 27 September 2021 structure and abundance, June 1973. Int. Rev. Ges. Hydrobiol., 60, 607-638. Berman.T. (1975) Size fractionation of natural aquatic populations associated with autotrophk and heterotrophic carbon uptake. Mar. Biol., 33, 215-220. Berman.T. and Kimor.B. (1983) A large scale Filtration apparatus for net plankton sampling. J. Plankton Res., 5, 111-116. Berman.T., Townsend.D.W., El-Sayed,S.Z., Trees.C.C. and Azov.Y. (1984) Optical transparency, chlorophyll and primary productivity in the eastern Mediterranean near the Israeli coast. Oceanol. Acta, 7, 367-371. Dowidar.N.M. (1984) Phytoplankton biomasj and primary productivity of the southeastern Mediterranean. Deep-Sea Res., 31. 983-1000. Kimor.B. (1983) Distinctive features of the plankton of the eastern Mediterranean. Ann. Inst. Oceanogr. Paris, 59, 97-106. Kimor.B. (1985) Indicator species in marine phytoplankton. XXIX Rapp. P.-V. Reun., Comm. Int. Explor. Sci. Mer Mediterr.. Monaco, 29, 65-79. ICSEM Congress and Plenary Assembly, Lucerne, 1984. Kimor.B. and Wood.E.J.F. (1975) A plankton study in the eastern Mediterranean Sea. Mar. BioL, 29, 321-333. Li.W.K.W., Subba Rao.D.W., Harrison.W.G., SmiuV.C, CullenJ.J., Irwin.B. and Platt.T. (1982) Autotrophic picoplankton in the tropical ocean. Science, 219, 219—225. Murphy,L.S. and Haugen.E.M. (1985) The distribution and abundance of phototrophic ultraplankton in the North Atlantic. Umnol. Oceanogr., 30, 47-58. RaymonU.E.G. (ed.) (1980) Plankton and Productivity of the Oceans. Vol. 1. Phytoplankton, 2nd edn. Pergamon Press, Oxford. Reid.F.M.H., Stcwart.E., Eppley.R.W. and Goodman,D. (1978) Spatial distribution of phytoplankton species in chlorophyll maximum layers off southern California. Lunnol. Oceanogr., 23, 219—226. Soumia.A. (1982) Is there a shade flora in marine plankton? J. Plankton Res., 4, 391-399. Stcidinger.K.A. and Williams,.!. (1970) Dinoflagellates. Memoirs of the Hourglass Cruises. Marine Research Laboratory, St. Petersburg, FL, p. 251. Takahashi.M. and Hori.T. (1984) Abundance of picoplankton in the subsurface chlorophyll maximum layer in subtropical and tropical waters. Mar. Biol, 79, 177-186. UNESCO (1978) Phytoplankton manual. Monographs on Oceanographic Methodology, no. 6, Paris, pp. 337. Utermdhl.H. (1958) Zur VervoUkommnung der quantitativen Phytoplankton Methodik. Mia., Int. Ver. Theor. Angew. Umnol., 9, 1-38. Venrick.E.L. (1982) Phytoplankton in an oligotrophic ocean: observations and questions. Ecol. Monogr., 32, 129-154. Waterbury J.B., Watson.S.W., Guillard,R.R.L. and GrandX-E. (1979) Widespread occurrence of a unicellular marine planktonic Cyanobacterium. Nature, 277, 293. Wiebe.P.H., Remsen.C.C. and Vaccaro.R.F. (1974) Halosphaera viridis in the Mediterranean Sea: size range, vertical distribution and potential energy source for deep sea benthos. Deep-Sea Res., 21, 657 -667.

442 PhytopUnkton species in Mediterranean DCM layers

Principal taxonomic sources Diatoms Cupp.E.E. (1943) Marine Plankton Diatoms of the West Coast of North America. University of California Press. Hustedt.F. (1961 -1962) Die Kieselalgen Deutschland, Ostcrreichs und dcr Schweitz. In: Rabenhorst, Krypt. Flora, 7 (1-920; 2-736; 3-945) Leipzig. Dinoflagellates SchillerJ. (1933-1937) Dinoflagellatae (Peridineae). In: Rabenhorst, Krypt. Flora, 10 (1—617; 2—589). Coccolithophorids Schiller^. (1930) Coccolithinae. In: Rabenhorst, Krypt. Flora, 10 (2—88-273). Silicoflagellates Gemeinhardt.J. (1930) Silicoflagellatae. In: Rabenhorst, Krypt. Flora, 10 (2—87). Downloaded from https://academic.oup.com/plankt/article/9/3/433/1573786 by guest on 27 September 2021 Received on April 4, 1986; accepted on February 28, 1987

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