Diel vertical migration of phytoplankton and heterotrophic flagellates in the Gulf of Riga

Ž .Journal of Marine Systems 23 1999 145–163

Diel vertical migration of phytoplankton and heterotrophicflagellates in the Gulf of Riga

Kalle Olli )

Institute of Botany and Ecology, UniÕersity of Tartu, Lai 40, EE-51005 Tartu, Estonia

Received 14 March 1997; accepted 28 August 1998

Abstract

Ž . ŽVertical distribution of a phototrophic ciliate Mesodinium rubrum , autotrophic dinoflagellates Peridiniella catenata,. Ž . ŽHeterocapsa rotundata, Dinophysis acuminata , a cryptomonad Teleaulax sp. , a filamentous cyanobacterium Aphani-

. Ž .zomenon flos-aquae , a non-motile chlorophyte Monoraphidium sp. and two heterotrophic dinoflagellates were studiedŽ . Ž .during two diel periods in spring May 1–2 and 27–28, 1995 and summer June 26–27 and July 6–7, 1994 in the southern

part of the Gulf of Riga, the Baltic Sea. The two seasons, corresponding to the vernal bloom and summer stage, differedconsiderably with respect to phytoplankton community, hydrography and vertical distribution of the species. In spring thecells stayed in the upper mixed layer above a strong thermocline at 12–15 m depth, and changes in the vertical distributionwere related to surface avoidance in the middle of the day. By using correspondence analysis, the vertical distribution of allthe motile species were shown to differ significantly from the non-motile Monoraphidium, but not from each other. Thevertical migration was reflected in a higher variability in the depth distribution patterns of the motile species, compared toMonoraphidium. In summer 1994, Aphanizomenon, Dinophysis and Teleaulax showed similar depth distribution patternsduring the first period, but different from Mesodinium and the heterotrophic dinoflagellates, while during the second periodall the autotrophic species had a species specific depth distribution pattern. Me. rubrum revealed a considerably differentdepth distribution between the two seasons, characterised by surface accumulation in spring and relatively uniform depth

Ž .distribution over the whole sampling range 0–30 m in summer. The results demonstrate different vertical niche separationstrategies between species. q 1999 Elsevier Science B.V. All rights reserved.

Keywords: Baltic Sea; Gulf of Riga; heterotrophic flagellates; phytoplankton; vertical migration

1. Introduction

The well-known concepts of phytoplankton lifeŽ .strategies from fresh waters Reynolds, 1988 and

) Woods Hole Oceanographic Institute, Biology Department,Mail Stop 32, Redfield 330, Woods Hole, MA 02543, USA. Tel.:q1-508-289-2688; Fax: q1-508-457-2134.

Ž .E-mail address: [email protected] K. Olli

Ž .marine environments Margalef, 1978 emphasisescarcity of ecological space where all the environ-mental factors are optimal for growth; a common

Ž .case is that light also due to strong vertical mixingor nutrients are limited. In temperate boreal regions

Žreduced vertical mixing e.g., due to thermal or.salinity stratification in spring prolongs the resi-

dence time of cells in the illuminated layer, leadingto increase of production and ultimately to the out-

Žbreak of the vernal bloom Sverdrup, 1953; Kahru

0924-7963r99r$ - see front matter q 1999 Elsevier Science B.V. All rights reserved.Ž .PII: S0924-7963 99 00055-X

( )K. OllirJournal of Marine Systems 23 1999 145–163146

.and Nommann, 1990 . In the absence of additional˜Ž .resources e.g., through advection or upwelling , the

stratified illuminated layer fails to meet the nutrientdemands of the exponentially growing populationsfor prolonged periods, leading to a vertical separa-tion of light and nutrients — clearly an unfavourablecondition for primary producers. Alone or togetherwith increasing water column stability, this leads to

Žsedimentation of vernal bloom diatoms Bienfangand Harrison, 1984; Bienfang et al., 1982; Davey,1988; Waite et al., 1992; Heiskanen and Kononen,

.1994 . In nutrient deplete and stratified conditions,the ability to use deep nutrient resources provides an

Ž .advantage over non-motile species e.g., diatomsand might prolong the vernal bloom.

It is commonly agreed that the potential to per-form diel vertical migration grants the micro-organisms with competitional advantage to exploithigh light levels near the surface where low concen-trations of inorganic nutrients would normally limitgrowth, while during night, the cells descend todeeper layers where nutrient demands are fulfilled

Žand intercellular reserves recharged Eppley et al.,.1968; Cullen, 1985; Lieberman and Shilo, 1994 .

Apart from deep nutrient retrieval, the control onvertical position enables the cells to exploit micro-

Žscale patchiness in the water column Hamner, 1988;.Owen, 1989 . Yet another aspect has been pointed

Ž .out by Sommer 1982 , involving variation in migra-tion as a consequence of differential light require-ments leading to ecological niche separation andrelaxation of interspecific competition. Indeed, infield conditions redispersal by turbulent motioncounteracts the behavioural adaptations of verticalmigration. Thus, the actual vertical profiles of cellabundance are a consequence of both, the be-havioural life strategies of the species to optimise thegrowth conditions and the external physical forcing.

The range of autotrophic organisms capable ofprolonged directed vertical movements involves be-sides the flagellated phytoplankton also the gas-vacuolated cyanobacteria and the autotrophic ciliateMesodinium rubrum. The species for the presentstudy were selected on the basis of previous knowl-

Žedge of migration potential Lindholm, 1985;.Passow, 1991; Heiskanen, 1995 , theoretical size

Ž .considerations Sommer, 1988 and sufficient abun-dance. We investigate the vertical profiles and migra-

tional behaviour of several dominant species ofŽphytoflagellates Peridiniella catenata, Heterocapsa

Ž . wrotundata Lohmann Hansen sKatodinium rotun-Ž . xdatum Lohmann Loeblich; see Hansen, 1995 ,

.Dinophysis acuminata, Teleaulax spp. , a filamen-Ž .tous cyanobacterium Aphanizomenon flos-aquae

Ž .and a phototrophic ciliate Me. rubrum during thevernal bloom and summer periods in the southern

Ž .part of the Gulf of Riga GOR . Two heterotrophicŽdinoflagellates Protoperidinium breÕipes and a

large naked dinoflagellate of the Gymnodiniumr.Gyrodinium type were included in the study due to

their high abundance and potential impact to theplanktonic system. As a reference point, a coccoidchlorophyte Monoraphidium sp. was included as apassive, non-motile autotroph in spring 1995.

2. Material and methods

The sampling was carried out at station 119Ž X X .57818 N; 23851 E; depth 42 m in the southern part

Ž .of the GOR, the Baltic Sea Fig. 1 . In 1994, two 24Žh sampling periods June 26–27 starting at 1600 h

.and July 6–7 starting at 0800 h were chosen whichwere the first and last full 24 h sojourns to thestation. In May 1995, the same sampling procedure

Žwas repeated during one 28 h period May 1–2.starting at 2000 h while due to weather constraints,Ž .the second period May 7–8 starting at 0100 h was

reduced to 20 h. During each period, vertical profilesof phytoplankton were taken at 4 h intervals using a

Ž .3 l Ruttner water sampler 1994 or an array of 5 lŽ .Niskin water samplers 1995 . The vertical range

Žwas from the surface to 30 m layer which was.below the primary pycnocline with 3 m vertical

Ž .intervals. Sub-samples 100 ml for phytoplanktonwere retrieved within a couple of minutes and fixedimmediately with acid Lugol solution. The cell con-centrations were determined with inverted micro-

Žscope Leica DM IL, phase contrast optics, 125=.and 500= magnification ; at least 200 counting

units were attempted to count depending on thedensity of the sample; in the case of A. flos-aquaethe length of the counted filaments was measured.

CTD profiles of salinity, temperature and in situŽ .fluorescence Q Instruments, DK were taken at least

( )K. OllirJournal of Marine Systems 23 1999 145–163 147

Ž .Fig. 1. Map of the GOR and the location of the sampling station 119 in the southern part. The shematic isobaths of 20, 30, 40 and 50 mŽ .are shown with thin line, arrow points the deepest part 60 m .

twice during each diel cycle to assess the watercolumn stability and vertical distribution of chloro-

Ž .phyll a. Photosynthetically active radiation PARreaching the sea surface was measured continuously

Ž .using a Li-Cor 190-SA sensor and a Grant UKlogger as integrator. A wind-meter was fixed at the

Župpermost top of the vessel ca. 10 m from the sea.surface and connected to the Grant data logger

Ž .wind speed was averaged for every 10 min duringthe whole cruise in 1995. Mineral nutrients weredetermined from discrete profiles taken from 0, 2.5,

5, 10, 15, 20, 30 and 40 m depths at the beginningand end of the stay at the station. Mineral nutrientsŽ .NO –N, NH –N, PO –P were analysed immedi-3 4 4

ately on board the vessel applying standard colori-Ž .metric methods Grasshoff et al., 1983 .

The depth profiles of the species were analysedŽby correspondence analysis ADE-4 software;

.anonymous ftp: biom3.univ-lyon1.fr . The cell abun-dance data were arranged in a matrix with 11 columnsŽ .corresponding to the 11 discrete depths and rowscorresponding to sampling times, arranged in blocks


Žcorresponding to the species thus, each row corre-sponds to a depth profile of a particular species on a

.given time . With correspondence analysis, the 11discrete depths were reduced to a few ordinationaxes, enabling a simultaneous visualisation of the

depth profiles of the species on a two dimensionalŽspace usually the first two axes encountered for

.)85% of the information . Correspondence analysisinvolves an initial transformation of the raw datamatrix by double multiplicative centering, giving

Ž . Ž . Ž 2 y1.Fig. 2. Temperature 8C , in situ fluorescence relative units , and stratification square of the Brunt–Vaisala frequency: N , s in May 2,¨ ¨ ¨Ž 2 . Ž 21995 A; Temp begin 0730 h; N and Temp end 2050 h; Fluor begin 0930 h; Fluor end 2230 h , May 7, 1995 B; Temp begin 0815 h; N

. Ž 2and Temp end 1950 h; Fluor begin 0830 h; Fluor end 2030 h , June 27, 1994 C; Temp and N , 0745 h; Fluor begin — June 26, 1830 h;. Ž 2 .Fluor end — June 27, 1930 h and June 7, 1994 D; Temp and N , 0020 h; Fluor begin — July 6, 0800 h; Fluor end — July 7, 0415 h .

Measurements taken at the beginning and end are given separately only in case of substantial difference.


thus more weight to values which differ considerablyfrom their respective column and row means. Afterthe analysis it is possible to define groups of profiles

Žby species profiles of one species belonging to one.group or symmetrically by sampling time, and cal-

culate a centre of gravity for each group. Further, thetotal variation in the data set can be partitioned into

Žwithin-groups i.e., differences between centres of.gravity of groups are ignored and between-groups

Žvariability i.e., the scatter between centres of gravity.of groups . The significance of the between-groups

variability can be tested statistically with a randompermutation test. This involves a random exchange

Žof data points corresponding to the vertical profiles

Ž . Ž . Ž . Ž y1 .Fig. 3. Vertical distribution of phosphate PO –P , nitrate NO –N and ammonium NH –N concentrations mg l during May 2–3,4 3 4Ž . Ž . Ž . Ž .1995 A , May 7–8, 1995 B , June 27–28, 1994 C and July 6, 1994 D . Filled symbols denote measurements taken at the end of the

sojourn.


.of the micro-organisms between the defined groups,calculating centres of gravity for the new groups and

Žrecalculating the between-groups variability i.e.,.variability between the new centres of gravity . At

least 1000 permutations were performed, each timerecalculating the between-groups variability, whichdistribute approximately normally. This enables thecomparison of the original between-groups variabil-

Ž . Ž . Ž . Ž . Ž .Fig. 4. Diel vertical distribution of P. catenata A , H. rotundata B , Me. rubrum C , Teleaulax spp. D and Monoraphidium sp. E cellŽ y1 . Ž y2 y1.concentrations cells ml on May 1–2, 1995. Respective sampling times are on A panel, surface radiation mE m s in parenthesis.

Ž . Ž 7 2 .Numbers in lower parts of the graphs depict the standing stock 0–30 m of phytoplankton cells=10 m . Numbers in the upper partŽ .represent out of scale values. Diamonds show the weighted average depth of the population i.e., the centre of gravity on the vertical axis .


ity with the frequency distribution of simulated val-ues. If the original variability exceeded the q95%confidence limit of the simulated variability distribu-tion, the original groups were considered to be statis-tically significantly different from each other.

3. Results

3.1. Weather, hydrography, nutrients

During both cruises the average wind speed wasŽ y1 .relatively moderate generally 3–6 m s . On May

Ž .Fig. 5. Diel vertical distribution of phytoplankton on May 7, 1995. Notation as in Fig. 4, except concentration of H. rotundata B is incells=102 mly1 , and standing stock in cells=108 m2.



2, 1995, a cloudless and calm weather prevailedŽ y2 y1maximum mid-day radiation 1700 mE m s ;

y1 .wind below 1 m s , which resulted in a formationŽof a sharp secondary thermocline at 3 m depth Fig.

.2A . The primary thermocline and main density dis-Žcontinuity measured as Brunt–Vaisala buoyancy;¨ ¨ ¨

2 . Ž .N were at the depth of 15 m Fig. 2A . During theŽsecond period a calm weather turned windy up to 8

y1 .m s towards the evening of May 7, causing adecay of the initially pronounced pycnocline at 15 mŽ . ŽMay 7, 0800 h by the evening May 7, 2000 h; see

.Fig. 2B beginning and end temperature profiles .There was a dense fog on May 7 and the maximumradiation did not exceed 500 mE my2 sy1. Theconcentrations of mineral nitrogen in the surface

Ž y1 .layer were high 80–105 mg l during the firstperiod, had decreased by the beginning of secondperiod but increased again by the end of the period

Ž .probably due to wind mixing Fig. 3A,B . Phosphateconcentration in the upper mixed layer was relatively

Ž y1 .low during the first period 5–6 mg l and de-Ž y1 .creased to the summer values -2 mg l by the

Ž .second period Fig. 3A,B .In 1994, windless weather with no or little waves

prevailed during the both periods. The maximummid-day radiation levels were 2000 and 1800 mEmy2 sy1 during the first and second periods, respec-tively. On June 27, the water temperature decreased

Žfrom 128C at the surface to 88C at the pycnocline 25.m depth , and dropped to 18C below the pycnocline

Ž .Fig. 2C . On July 7, the pycnocline was less pro-nounced and the main density discontinuities were at

Ž .12 and 30 m Fig. 2D . The nutrient conditions werecharacterised by an accumulation of ammonium,

Žwhile the surface layer nitrate typically -10 mgy1 . Ž y1 .l and phosphate -2 mg l concentrations

Ž .were low Fig. 3C,D .

3.2. Vertical distribution of the phytoplankton

For the general description of the phytoplanktonspecies composition and abundance, see the work of

Ž .Olli and Heiskanen 1999 .

In spring 1995, the bulk of the populations of theŽmotile species remained above the pycnocline Figs.

.4 and 5 . The main variation of cell abundancesoccurred generally in the upper 6 m layer, in severalcases notable accumulation of cells to the surface or

Ž .subsurface layers e.g., 1200 and 1600 h on May 2Ž .were observed Fig. 4 . The non-motile Monoraphid-

ium was relatively evenly distributed in the upper6–9 m throughout the two periods; below the con-centrations decreased gradually, but substantialamount of cells were found in the deeper layers alsoŽ .Figs. 4E, 5E . The abundance of the species had

Žincreased by the second period by a factor of 3 P.. Ž . Ž .catenata , 10 H. rotundata , 4 Me. rubrum , 2

Ž .Monoraphidium , while the abundance of Teleaulaxremained approximately the same.

The in situ fluorescence profile taken in the morn-Ž .ing 0930 h of May 2 revealed a smooth distribution

of CHL down to 10 m and a decrease at the veryŽ .surface layer Fig. 2A; Fluor begin . This agreed

Ž .well with the temperature gradient Fig. 2A . TheŽ .evening profile 2200 h showed a strong and narrow

CHL peak at the depth of 3 m, which coincided withŽ .the depth of the newly formed thermocline Fig. 2A .

During the second period, the fluorescence profileŽwas again fairly even in the upper 0–9 m layer Fig.

.2B .In 1994, the dominant phytoplankton species A.

flos-aquae had a clear bimodal distribution duringthe dark time with one maximum at about 9–12 m

Ž . Ž .and another at the surface 0 m Fig. 6A . Duringthe second period, such bimodal distribution was notnoticed and the bulk of cells was in the upper 9 mwith peak abundances varying between 6 m and the

Ž .surface Fig. 7A . The flagellates D. acuminata andTeleaulax spp. were mainly in the upper 9 m layer,with main variation just in the upper surface layerŽ .Figs. 6B,D, 7B,D . In many cases, the cells seemed

Žto avoid surface layer during light time e.g., D..acuminata, 1600 h, first period; Fig. 6B or had a

Ždeep accumulation during dark time e.g., Teleaulax.spp., 2400 h, second period; Fig. 6D . In 1994, Me.

rubrum had a somewhat uniform depth distribution

Ž . Ž . Ž . Ž .Fig. 6. Diel vertical distribution of A. flos-aquae A , D. acuminata B , Me. rubrum C , Teleaulax spp. D , naked heterotrophicŽ . Ž . y1 y1dinoflagellates E and P. breÕipes F on June 26–27, 1994. Cell concentrations in cells ml , A. flos-aquae is in 100 mm filaments ml .

Other notations as in Fig 4.


Fig. 7. Diel vertical distribution of phytoplankton in July 6–7, 1994. Notations as in Fig. 5, except naked heterotrophic dinoflagellates andP. breÕipes, standing stock in cells=106 m2.


over the whole sampling range with some maxima atŽ .30 m depth even Figs. 6C, 7C . On several occa-

sions, the species showed distinct accumulations atŽnarrow depths e.g., 1200 h on second period; 2000.h on first period . However, the uniform depth distri-

bution over the whole sampling range was in sharpcontrast to the distribution in spring, when most ofthe cells were in the upper 12 m layer. The in situfluorescence revealed a bimodal distribution in the

Ž .evening 1830 h of June 26, having peaks at 4.4 andŽ .9 m Fig. 2C; Fluor begin . On the evening of JuneŽ .27 1930 h , the fluorescence was more uniform

Ž .down to the pycnocline Fig. 2C; Fluor end . Onboth cases, a decrease of fluorescence was notable at

Ž . Ž .the pycnocline 25 m Fig. 2C . During the secondperiod, the main decrease of fluorescence was at 10m depth, which coincides with the upper density

Ž .discontinuity Fig. 2D .

3.3. Vertical distribution of heterotrophic flagellates

The naked dinoflagellates of the Gymnodi-niumrGyrodinium type were rare in the surface lay-ers from 0–3 m. The peaks occurred in the deepwaters at 24 m or in the middle layers up to 9 m.During the first period, the abundance of the organ-

Žisms decreased explicitly below the 24 m layer Fig..6E . In contrast, during the second period, the cell

abundances increased from 9 to 30 m, where also theŽ .maxima were found Fig. 7E . Indeed, possibly even

higher abundances could have been found below 30m depth. During the first period, P. breÕipes hadobvious abundance peaks at 27 m depth mainly,

Ž .below the numbers decreased Fig. 6F . During thesecond period, the species was much less abundantand the cell maxima were often found at the 30 m

Ž .depth Fig. 7F .

3.4. Data analysis

Correspondence analysis on the data set from thefirst period in spring 1995 reveals that if the profiles

Žare grouped by species connected to their respective.centres of gravity , there is no overlap between

Monoraphidium and the rest of the species, capableŽ .of active movements Fig. 8A . This indicates that

the depth distribution of the motile species weredifferent from the profiles of the non-motile Mono-raphidium. When all the species were regarded asseparate groups, the between-groups difference was

Žsignificant at 0.052 level i.e., 52 random simulationsout of 1000 resulted in higher between-groups vari-

.ability . However, when comparing Monoraphidiumagainst the motile species the difference was highly

Žsignificant i.e., none of the random permutationsresulted in between-groups variability exceeding the

.original one . From Fig. 8A, it could also be seenthat the spread of data points corresponding to thenon-motile Monoraphidium is much smaller com-pared to the motile species. This is the reflection ofthe relatively similar depth profiles of Monoraphid-ium during all the eight sampling times and suggeststhat the variation in the distributions of motile speciesis due to active movement and not caused by sam-pling errors or stochastic factors.

As a next step, the significance of differencesbetween the motile species were questioned and thebetween-groups analysis was repeated with Mono-raphidium excluded from the data matrix. No differ-ence was found between the species, the within-groups variability contributed 75% of the total vari-ability.

When the groups were defined by the samplingŽ .times eight groups , a significant difference wasŽ .found 0.008; Fig. 8B , which was not the case when

Monoraphidium was included in the data matrix.This shows that much of the variability in the datamatrix is due to differences in distribution patternsbetween different sampling times, while Mono-raphidium does not fit to the scheme. This can beinterpreted as synchronous vertical movements of themotile species in time, which can be seen as arelatively uniform distribution in the upper 12 mlayer at the beginning of the period and subsequentsurface avoidance during the day time, a similarbehaviour of all the motile species. Projection of thedata on the first factorial plane reveals that thevertical profiles taken at 1200 and 1600 h locaterelatively close to each other and separately from the

Ž .rest of the groups Fig. 8B . Additionally, the profileof P. catenata from 2000 h locates near this groupŽ .Fig. 8B . All these profiles were characterised bypronounced sub-surface peaks at three to six layersŽ .Fig. 4 .


Ž . Ž .Fig. 8. Factorial planes of correspondence analysis. Groups defined by the species A, C or sampling time B are connected to theirŽ .respective centres of gravity. Axes are defined to maximise the variability of all data points. Numbers depict the range of the axes. A

Ž . Ž . Ž . Ž .Projections of the vertical distributions of P. catenata P , H. rotundata K , Me. rubrum R , Teleaulax spp. T and Monoraphidium sp.Ž . Ž .M in May 1–2, 1995, onto the first factorial plane. B Projection of the vertical distribution of the motile species in May 1–2, 1995, onto

Ž .the first factorial plane. Groups are defined according to sampling time numbers from 1 to 8 represent temporal sampling series . ArrowsŽ . Ž . Ž .point to the profiles of P. catenata at 2000 h A , 2400 h C and Teleaulax spp. at 2400 h B . These profiles are similar to the general

Ž . Ž .distribution pattern at 1200 and 1600 h, and consequently locate near these groups 5 and 6, respectively on the factorial plane. CŽ . Ž . Ž . Ž . Ž .Projection of A. flos-aquae A , D. acuminata D , Me. rubrum M , Teleaulax spp. T , naked heterotrophic dinoflagellates G and P.

Ž . Ž .breÕipes P in June 26–27, 1994, onto the first factorial plane. D Projections of the vertical distribution of Me. rubrum onto the firstŽ . Ž . Ž .factorial plane. Groups are defined according to periods and areas: 1 GOR, May 1–2, 1995; 2 GOR, May 7, 1995; 3 GOR, June 26–27,

Ž . Ž . Ž .1994; 4 GOR, July 6–7, 1994; 5 GOF, May 5–6, 1994, 6 GOF, May 27–28, 1994. Note the similarity of the vertical profiles duringsummer in GOR and late spring in GOF.


The five species had significant differencesŽ .0.012 between vertical profiles also during thesecond spring period. However, when the four motilespecies were compared alone the between-speciesdifference was not significant any more, but a signif-

Ž .icant 0.008 difference was found when the groupswere defined by sampling time, but not when thefour motile species were compared alone. The first

Ž .sampling time 0100 h was separated from the restŽ .by the third factorial axis and the last group 2100 h

was with relatively less scatter, indicating that thewind induced mixing had redistributed all the speciesuniformly in the water column.

In further analysis, the data matrices from bothspring periods were pooled. The analysis of pooleddata showed clearly the separation of Monoraphid-ium from the motile species, which on their own didnot show significant between species differences.

The first factorial plane for the data set from theŽ .first period in 1994 Fig. 8C indicates a clear sepa-

ration of both heterotrophic dinoflagellates and Me.rubrum as groups by themselves and also from therest of the species. Relatively small spread of thegroup defined by Protoperidinium corresponds wellwith the quite similar profiles in Fig. 6F, with the

Žprofile lacking pronounced deep accumulation 0800.h extending from the rest on the factorial plane also.

The reasonably uniform depth distribution of Me.rubrum also stands separately on the factorial planeand are almost closer to the naked dinoflagellatesthan to the rest of the autotrophic species. There isno significant difference between the depth profilesof A. flos-aquae, D. acuminata and Teleaulax sp.during the first period.

Further analysis of the sampling times involvingthese three species revealed that profiles taken at2000, 2400 and 0400 h are relatively similar, also the

Ž .first and last profiles both taken at 1600 h and theprofiles taken at 0800 and 1200 h. These more orless homogenous groups differ statistically signifi-cantly. The dark time profiles were characterised by

Žbimodal depth distribution e.g., Aphanizomenon and.Teleaulax .

The second period in 1994 was characterised by aŽrelatively small within species variability 35% of

.the total is attributed to within-groups variabilityand a separation of all the species on the firstfactorial plane, except for the heterotrophs. The vari-

ability of P. breÕipes is much larger compared to theŽothers partly due to the inaccuracy of the cell counts

.due to very low cell abundances and overlaps withŽthe naked dinoflagellates both have increased cell

abundances towards deeper depths with maxima at.the 30 m layer on this period; Fig. 7E,F . The

autotrophic species have all relatively low within-group variability, compared to the between-groupsvariability.

As a next step, the data matrices from both peri-ods of the summer period were pooled. The resultingfirst factorial plane showed clearly that the hetero-trophic species formed groups by themselves, so didMesodinium and also Dinophysis from the secondperiod. The rest of the groups formed one homoge-nous cluster.

Two species, Teleaulax and Mesodinium,werestudied on both years, and thus the patterns of verti-cal distribution could be compared over a time scaleof year, involving two different annual stages. Thepooled analysis on Teleaulax showed that 87% ofthe variability was due to within-groups differencesand the remaining 13% of between-groups variabilitywas not statistically significant, i.e., the depth profilepatterns in spring were not different from those insummer. Similar analysis on the Mesodinium datagave opposite results, the depth profile pattern inspring was significantly different from the summerprofiles. This is clearly evident also from Figs. 4–7,where in spring the cells are in the upper 12 m layer,while in summer, they are distributed relativelyevenly over the sampling range.

A similar change in the depth distribution of Me.rubrum was observed during a study in the NW Gulf

Ž . Ž .of Finland GOF Olli et al., 1998 , where the cellswere concentrated to the top layer during the peak of

Ž .the spring bloom May 5–6 , but had rather continu-ous depth distribution during the decline phase of the

Ž .bloom May 27–28 . This similarity between the twoareas advocated to analyse the joint data set of Me.rubrum involving six groups. The first factorial planeŽ .Fig. 8D shows that the profiles from the declineperiod in GOF group together with the profiles fromthe summer period in the GOR, profiles from thespring period in GOR group together and the profilesfrom the peak of the spring bloom in GOF standsomewhat separately. The actual difference betweenthe bloom peak profiles from GOF compared to


those from GOR was that in GOF the cells wereconcentrated to the upper 0–6 m layer while in GORthe surface accumulation was not so sharp.

4. Discussion

4.1. General considerations

The present study revealed species specificchanges in the vertical distribution of different mi-cro-organisms in environmental conditions differingwith respect to nutrients, light and hydrography.

During the spring bloom period, a strong thermo-cline set a boundary to the depth distribution of themicro-organisms. Yet the analysis revealed a signifi-cant difference in the depth distribution profiles ofthe motile species and the non-motile Monoraphid-ium. The vertical movements of the motile specieswere demonstrated by the higher spread of the data

Žpoints on the factorial plane indicating larger change.in the vertical profile pattern in time compared to

Žthe rather uniform profiles corresponding to smaller.spread of points on the factorial plane of Mono-

raphidium. The main variation was just in the upperŽ .layers 0–6 m . As mineral nutrients were uniformly

distributed in the upper water column, it is hypothe-sised here that the observed vertical movements werethrived by search for optimal optical depth, anddemonstrate thus the behavioural flexibility of motilespecies compared to the non-motile ones.

The vertical profiles indicate a surface avoidanceof all the motile species during the light time in thefirst period, not matched with similar behaviour onthe second period. This coincides with the differ-ences in the radiation between the two periods.During the first period the radiation levels were threeto four times higher than during the second period. Itis possible that the radiation levels during the calmand cloudless day exceeded the optimal for thesemicro-organisms and downwards migration avoidedphotoinhibition. Photoinhibition is a function of radi-ation levels combined with the light history of thecells and has frequently been reported in connectionwith weak vertical mixing of the water columnŽ .Vincent et al., 1984; Elser, 1985 . Heaney and

Ž .Eppley 1981 have found that dinoflagellates toler-ate radiation levels of 1000 mE my2 sy1 in nutrientreplete conditions, above that level subsurface accu-mulation was observed, while in nutrient depleteconditions the preferred light level was 150 mE my2

sy1.The in situ fluorescence profiles from the spring

period showed a quite uniform distribution of thechlorophyll a in the upper 10 m in the beginning of

Žthe first period coinciding well with the abundance.of dominant species in this layer , while in the

evening a sharp chlorophyll a peak appeared just atthe border of the newly created thermocline at 3 m

Ž .depth Fig. 2A . The reason why such peaks appearremains unclear. As photosynthesis is temperature

Ž .dependent Davison, 1991 , it is possible that thethin warmed layer combined with optimal light ap-peared the most suitable environment for growth,resulting in a considerable accumulation of cells.Alternatively the downwards migrating cells mighthave stopped at a sharp temperature gradient. It hasbeen shown experimentally that sharp temperaturechanges can decrease the swimming speed of di-noflagellates and act as effective barriers for vertical

Ž .migration Heaney and Eppley, 1981 , although op-Ž .posite results are also known Kamykowski, 1981 .

The actual outcome depends also on the nutritionalŽ .status of the cells Heaney and Eppley, 1981 .

In the nutrient replete conditions in spring 1995,there was no difference in the depth distributionpatterns of the motile species, suggesting that all thespecies occupied the same vertical niche. In summer1994, the situation was different. Apart from Me.rubrum the other autotrophic species revealed anoverlapping vertical distribution during the first pe-riod in 1994, while there was a significant differenceduring the second period. The different behaviouralresponses to the changing environmental conditionscan be seen as strategies for optimal resource ex-ploitation through vertical niche separation leading

Žto co-existence of different species Sommer, 1982,.1984 . The results indicate the importance of species

specific behavioural adaptations in the vertical nicheseparation exemplified by accumulations to optimaloptical depth and retrieval of deep nutrients. Thevertical separation of the heterotrophic dinoflagel-lates is not surprising as they do not need light asenergy source.


Indeed, the nutritional benefits of these move-ments can be questioned due to the relatively highconcentrations of nitrogen in the upper layer. Gener-ally, the GOR is regarded as phosphorus limitedŽ .Yurkovskis et al., 1993 and considering the sum-

Ž y1 .mer phosphate concentrations often -1 mg l inthe surface layer during our study, it can be possiblethat the species got nutritional benefits by migratingbelow the surface mixed layer during the dark time.

4.2. Vertical distribution of Me. rubrum

The distribution of Me. rubrum was considerablydifferent from the rest of the autotrophic species.Indeed, Me. rubrum is a cosmopolitan species withunusual physiological and behavioural propertiesŽ .Lindholm, 1985 . Perhaps, the most remarkable isthe swimming speed which can exceed 5 mm sy1

Ž .Lindholm, 1981 . This is roughly an order of magni-tude more than reported for the dinoflagellatesŽThrondsen, 1973; Kamykowski, 1995; Kamykowski

.and McCollum, 1986 . Thus, from the point of theswimming capacity, it is realistic to cover a range of30 m during one diel cycle.

The ability for diel vertical migration of Me.Žrubrum is widely known Crawford, 1989; Passow,

.1991; Williams, 1996 . However, previous migrationstudies from the Baltic Sea indicate that part of thepopulation remains in deep layers and does not

Žmigrate, at least not on the diel scale Lindholm and.Mork, 1990; Passow, 1991 . It is known that at low¨

temperatures, the species can tolerate darkness forŽ .several days or weeks Lindholm, 1985 . This is in

accord with the present findings in the vertical distri-bution of the species in summer 1994. The reasonsof the remarkable difference in the vertical distribu-tion of Me. rubrum in spring and summer remainunclear. However, these results are in good agree-ment with those obtained from a comparable coastal

Ž .area in the GOF Olli et al., 1998 where the verticaldistribution of Me. rubrum revealed a clear accumu-lation to the upper 9 m during the peak of the vernalbloom, while during the late decline phase the cellswere distributed fairly evenly over the range of 0–36m with some maxima at 24–27 m depth. The simi-larity of the summer profiles from the GOR and theprofiles from the decline phase of the vernal bloom

from the GOF was apparent also from the factorialplane. Further investigations are needed to verify ifthis is a general rule in the Baltic and in other areas,and also to clarify the reasons and mechanisms ofsuch behaviour.

4.3. Vertical distribution of A. flos-aquae

During the present study, the vertical distributionof A. flos-aquae revealed a bimodal distributionduring the first period in 1994, where at least part ofthe population was found below the secondary ther-

Ž .mocline 9 m , while during the light time, the wholepopulation was concentrated to a subsurface layerwith a peak at 3 m. During the second period asignificant biomass of A. flos-aquae had beenformed, yet no major bloom was observed and thewhole population remained buoyant.

The gas-vacuolated filamentous cyanobacteria areknown to perform diel vertical migration by control-

Žling the buoyancy Klemer, 1985; Villareal and Car-.penter, 1990; Oliver, 1994 which appears as a major

strategy in bloom formation and in competition forŽlight and nutrients Booker and Walsby, 1981;.Reynolds et al., 1987 . There are several mecha-

nisms for buoyancy control, involving formation andcollapse of gas vacuoles, accumulation and utilisa-

Žtion of carbohydrates Walsby, 1978; Klemer et al.,.1982; Konopka et al., 1987 . A. flos-aquae is able to

Ž .fix gaseous nitrogen Lindahl and Wallstrom, 1985 ,¨thus, it is suggested that it is not limited by lack ofmineral nitrogen in the water column, while lownitrogen to phosphorus ratio provide an advantageover other species and favour bloom formationsŽ .Niemi, 1979 .

However, the results of Lindahl and Wallstrom¨Ž .1985 from SW Bothnian Sea indicate, that nitrogenfixation of A. flos-aquae corresponded to only 1%of the nitrogen requirement for the primarily produc-tion during the summer. Nitrogen limitation has beenoften reported to cause buoyancy loss of gas vacuo-

Žlated cyanobacteria Klemer et al., 1982; Spencer.and King, 1985 , primarily because the energy cap-

tured in photosynthesis could not be channelled tocell growth, but rather accumulates in the form ofhigh-molecular carbohydrates which act as ballastŽ .Konopka et al. 1987 . In the present study, it is thus


possible that the population of A. flos-aquae re-mained more buoyant during the second period dueto higher NH –N concentrations in the upper water4

column.

4.4. Vertical distribution of autotrophic flagellates

The vertical migration of cryptomonads has notreceived much attention in the marine environments,although even small species can have high swim-

Ž .ming speed Throndsen, 1973 . In lakes, the verticalŽmigration of cryptomonads is well known Pick and

Lean, 1984; Jones, 1988, 1991; Smolander and Ar-.vola, 1988 and has been shown to be important in

Žhypolimnetic phosphorus retrieval Salonen et al.,.1984 . During the present study, the vertical distribu-

tion of Teleaulax sp. was investigated during thespring bloom and summer stage. The comparison ofthe profiles from the two seasons revealed no signifi-cant differences. However, the depth profiles fromthe summer period reveal a deeper distribution dur-

Žing the dark time 2400 h, a maximum at 18 m.during the second period suggesting a deep nutrient

retrieval.The vertical distribution of D. acuminata un-

veiled some deep accumulation at the lower depthsof the sampling range during the second period.These deep residing cells were found in all theoccasions during the second period and according tothe poor appearance, were not probably part of theactive population, but rather sinking or dead cellswhich had accumulated to the density gradient. Thesedeep residing cells, however, influenced the statisti-cal analysis and positioned the whole group sepa-rately from the others, and also from the profiles ofD. acuminata from the first period. Yet a closelyrelated species, Dinophysis norÕegica has been foundto form healthy deep maxima at the depth of thermo-

Ž .cline in the Baltic Sea Carpenter et al., 1995 . Thelow light level at the depth of the maximum cell

Ž .densities 12–15 m suggested mixotrophic nutritionŽ .Carpenter et al., 1995 . D. acuminata is a commonspecies in the Baltic Sea, but has not been reportedto be dominant, form blooms or cause any toxicproblems. However, it has been hazardous in thecoastal areas of France, where the diel vertical mi-gration has been observed and accounts probably to

Ž .it’s ecological success Clement et al., 1988 . Also,

other species of the genus are reported to cause toxicŽred tides Subba Rao and Pan, 1993; Reguera et al.,

.1995 .

4.5. Vertical distribution of heterotrophic dinoflagel-lates

There was also a considerable variation in thedepth distribution of an abundant population of nakedheterotrophic dinoflagellates between the depths of 9and 24 m during the first period in 1994. Thedistribution was less variable during the second pe-riod, with abundance increasing possibly below thesampling range. The thecate heterotrophic dinoflagel-late P. breÕipes had distribution maxima in the coldwater below the pycnocline.

Little is known about the ecology and trophic roleof planktonic heterotrophic dinoflagellates in marinecoastal ecosystems. Few data exist on what couldguide the vertical population distribution of theseorganisms. Often, the maxima of heterotrophic di-noflagellates are associated to blooms of their prey

Ž .organisms Hansen, 1991; Lessard, 1991 giving thusclues to diet preferences. The organisms are knownto form subsurface maxima at or below the pycno-

Žcline, associated with sinking diatoms Lessard,.1991 . During summer 1994, there were not many

diatoms in the middle layers of the water column,clearly insufficient to support the abundant popula-tion of the naked heterotrophic dinoflagellates. The

Ž .ingested prey items Olli and Heiskanen, 1999 sug-gested that the population was not specialised to oneprey type.

It has been claimed that species from the hetero-trophic genus Protoperidinium feed exclusively on

Ž .diatoms Jacobson and Anderson, 1986 . There werealways large numbers of Thalassiosira baltica cells

Žbelow the pycnocline in 1994 Olli and Heiskanen,.1999 . Th. baltica is an abundant vernal bloom

species in the area, and after sedimentation maintainsa large dormant population in the bottom nepheloid

Ž .layer pers. obs. where it is resuspended to thewhole water column below the primary pycnocline.These resuspended cells were also found in largequantities below the pycnocline. However, the dor-mant cells were never found in the water column andsediment traps above the pycnocline, indicating thatthe water column was efficiently separated into two


distinct water bodies. Thus, it appears that separationof the water column by a strong pycnocline indi-rectly determined the vertical distribution of P. bre-Õipes, and supports the view that the genus feedsonly on diatoms.

4.6. Sources of uncertainty

Indeed, the above conclusions can be sensitive toseveral limitations in the used methods and errorslike inaccuracy in sampling, turbulent mixing andvertical redistribution of the cells and horizontaladvection of the water mass.

The relative precision of cell abundance estimatesŽis related to the number of cells counted Duarte et

.al., 1990 . In all but the case of P. breÕipes duringthe second period in 1994, the cell counts weresufficiently high not to cause significant alterationsin the shape of the depth distributions. Additionalvariation is introduced with the procedures of sam-

Ž .pling and subsampling Vernick, 1971 . A compara-ble investigation during a vernal bloom period from

Ž .the GOF Olli et al., 1998 revealed that counts fromreplicate samples and sub-samples had a coefficientof variation between 5% and 8%, which gives arelatively good estimate of the cell abundance.

An additional aspect of the sampling error isrelated to the vertical and temporal resolution of thediscrete samples. It is usual that autotrophic micro-

Žorganisms accumulate in relatively thin layers Lin-.dholm, 1985 , making it difficult to reveal the actual

maxima with pre-set sampling schedule. Indeed, dur-ing the present study the narrow fluorescence peak atthe secondary thermocline suggests that the 3 mvertical resolution might miss some important fea-tures in the vertical distribution, which may alsochange significantly the shape of the depth profiles.Moreover, it was observed that such distinct peakswere relatively short lived and disappeared within anhour. However, the narrow temporal peaks are un-likely to change the main conclusions based onlarger scale and more general depth distribution pat-terns.

Another likely source of inconstancy is turbulentmixing and horizontal patchiness. Wind induced tur-bulent mixing causes vertical redistribution of cellsin the water column. Even more, Langmuir rotationcauses both, horizontal and vertical patchiness of

Žmotile cells in the scale of the rotation cells Smayda,.1970; Reynolds, 1984 . Nevertheless, during the pre-

sent study, the weather was windless during most ofthe time, except the end of the second period in 1995when the original sampling schedule was not ful-filled. The last profile from that sampling seriesrevealed relatively uniform vertical distribution ofcells in the mixed layer and relatively high similaritybetween the species. The horizontal mesoscale distri-bution of phytoplankton is patchy in the BalticŽ .Kuosa, 1988; Kuuppo-Leinikki, 1993 , but in thescale of 100–200 m errors caused by sampling pro-

Žcedures have shown to override this Kuuppo-.Leinikki, 1993 .

Acknowledging these possible ambiguities, it isstill obvious that if the physical forcing overrules theadaptational behaviour of the motile micro-organisms, we would not expect to see significantdifferences in the vertical distribution patterns be-tween the species, particularly when compared to anon-motile one as was the case in the 1995. Indeed,the results would be different in the case of con-trolled laboratory experiments, yet in nature the ac-tual vertical distribution of micro-organisms is acombination of water movements counteracted bythe active response of the cells to fulfil their physio-

Ž .logical requirements Sommer, 1985 .

Acknowledgements

The author is grateful for the whole team of theproject Pelagic Eutrophication and Sedimentation;particularly P. Wassmann for co-ordination and A.-S.Heiskanen for introduction to the subject, valuablecomments on the early version of the manuscript andmoral support. I also wish to thank M. Mazmacs, foranalysis of inorganic dissolved nutrients, M. Olesenfor CTD and fluorescence data, and the crew ofRrV Marina for help with the sampling. I thank P.Wassmann, T. Tamminen and H. Kuosa for com-ments on the early version of the manuscript, andtwo anonymous referees for critical reading and con-structive remarks. This study was financed by NordicCouncil of Ministers; Nordic Environmental Re-search Programme, The GOR Project. I am also verythankful for the personal grants provided by Nordic


Ž .Academy of Advanced Studies NorFa and IDEArSalen Foundation.

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Diel vertical migration of phytoplankton and heterotrophic flagellates in the Gulf of Riga