/ 2 5 , 4 3 4 - 4 4 1 (1987)

THE ECOLOGICAL IMPLICATIONS OF GROWTH FORMS IN EPIBF.NTHIC DIATOMS'

ChristianaD e p a r t e m e n i d e B i o l o g i c U n i v e n i t e Laval, Ste-Foy, Q u e b e c , Canada G I K 7 P 4

Pierre Legendre

Dcpartcmrnt de Science* biologiqu<-», Univertit^ de Montreal. C.P. 6128. Succur&ale A. Montreal. Quebec, Canada H3C 3J7

ABSTRACT

Thii paper ei'nluates ihe utilisation of space hy epihen-thic diatom cells, as a responsf to emnronmeutal varia'tions. The aggregation pattern of fife species of epihenthicdiatoms was quantified nnd compared to prm'ide evidenrffor thr significance of cell motility as an adaptive mech-anismfor space occupation and monopoly. The epibenthicdiatoms included (1) non-mobile colonial species formingeither fan-shaped fSyncdra tabulata (Ag.) Kz.) or ar-borescent (Gomphonema kamtschaticum var. califor-nicum Grun.) colonies: (2) stou-'mm-itig f'Cocconeis cos-tata Greg, and Amphora pusioC/j, and (3)fast-movingfNaviculadirectaAV. Sm.)Ra.) non-colonialspeaes. Theaggregation pattern of S. tabulata did not vary signifi-cantly among stx different light intensities manipulatedin nature. The major patterns of aggregation were iden-tified using analyiis of cmariance and dummy-variableregresiion. Highly mobile N. directa are significantly Ifss^gg^^g*tt^d fhan the four other diatom species. Son-mobileand s^lou'-moi'ing species show a similar, highly aggregatedpattern. The occurrence of two patterns of spatial disper-sion indicates that growth forms hear far-ranging ecolog-ical implications uith retpect to colonization .strategies,immigration, and possibly impact by grazers. An inte-grated model of grmith form characteristics, biologicalproperties, and ecological implications is presented forepihenthic diatoms.

Key index words: aggregation pattern; Amphora; ona/-ysis of (oi-anance; Qxconeis: colonization strategy: dia-toms; distribution; Gomphonema; Navicula; Synedra

Hutchinion (1975) defined growth forms as the!M?t of adaptations developed by different taxa for aparticular mode of life. These adaptations allow tax-onomically unrelated species to use similar habitats,and to compete for a number of common resources.Among epibenthic diatoms, growth form can be de-fined using three characteriitics combined in variousway*: form, posture, and mobility (Hudon and Bour-get 1983).

The diversity of growth forms found among livingepibenthic diatoms was reported in early taxonomicrecords (Smith 1833, Van Heurck 1899), Charac-

p 2t p' A(ldrr\»lor reprints and preM-nt addre^i: Department olFUh-

erte«and Ocran*. Atxtic Biological Station. 555 St-Pierre Blvd.,Ste-Anne-de Bellrvue, Quel>rc H9X 5R4, Canada.

feristics such as the formation of mucous tubes ar-ranged in thallus were initially used as the basis forthe definition of genus Schizonema (Greville 1827).This genus was aU^lished due to the high variabilityof Ihc ihalli and of the valve ornamentation, amongspecies possessing the ability to produce tubes (Gru-now 188O.Clevc 1894). Anothercxampleof the useof growth form to help delimit taxonomic units iithe differentiation of genera Frngilaria and Synedraon the basis of their respective ability to form rib-bon-like filaments or rosctteson a surface. Althoughthe definition of these two genera is questioned(Lange-Bertalot 1980), the ecological significance ofthe distinction was convincingly argued by Round(198-1) who presented comparative examples fromother genera.

A growing number of studies deal with the ar-chitecture of epibenthic diatom communities (Pat-rick and Roberts 1979. Hoagland et al. 1982. Hoag-land 1983. Hudon and Bourget 1981, 1983.Luttenton and Rada 1986, Steinman and Mclntirc1986), The characteristic distribution pattern of dif-ferent species was reported from observation of cellsgrowing on agar (Lee etal. 1975), on plant material(CattaneoI978),ongIass(MunteanuandMaly 1981),and on plastic substrates (Hudon and Bourget 1981 )•However, no quantitative study of the microdistri-bution of epibenthic diuioms has been conducted toevaluate the utilisation of space as a response toenvironmental variations.

Live observatit>ns of epil>enthic diatoms led us toconsider that growth forms in general, and mobilityin particular, could influence the ecological successof a species. Growth forms and tnobility shouldmarkedly affect spaceallotation and dominance dur-ing colonization of substrates by different species-One manifestatitm of the changes in space allocationis found in the small scale distribution of these algafiwhich leads u» to expect the following results: (I)Species of epibenthic diatoms bearing differentgrowth forms should exhibit different distributionpatterns, (2) A sfx-cies may alter its distribution pat-tern in response to environmental conditions.

F.xamples of distribution patterns and of the vari-ances associated with given mean densities is givenin Figure I, for two hypothetical species of epiben-thic diatoms possessing different types of mobility-Assuming tfie same immigration and growth rates.

434

Mean (x)In cells .

GROWTH FORMS IN EPtBENTHIC DIATOMS

0.5 2.0

435

10.0

spEC

IES

Spatialdistribution

Frequency thistogram

Numbtr of c a l l t

Variance (sO 1.5 IB 350

SPEC1ES

8 oo o o o

Spatialdistribution

Frequencyhistogram

Variance

ccp - o 8coo o 0 ° ^o X*

0.5 100

Fic. I. Kxamplei of distribution patterns that could be obierved for t^-o epibenthic diatom species of different mobility, over anintTeaw in mean density.

the immobile species (A) should produce a smallnumber of very dense clumps, hence a very highly'*RS*'*'R t*"d pattern. On the other hand, the highlymobile specie* (B) should be more dispersed andform a larger number of small, scattered clumps.

Our aim is to examine the ecological implicationsof different growth forms among epibenthic diatomspecies. We first describe different growth forms ofepibenthic diatoms from observations and measure-Ticnts on living cells. Five species bearing differentgrowth forms are used to compare the distributionpatterns resulting from their varying ability to moveon the surface. We then go on to examine a common(ubiquitous) species. Synedra tabulata, to determineWhether its distribution pattern varies under differ-ent light intensities. Finally, we summarize the eco-logical implications asscx'iaied with different growthjorms and discuss the physiological adaptations re-lated to particular morphologies.

MATFKIAI.S AND METHOtJS

Sampling o( epit>rriil>it <liatnmii wjn earned out at Pointe Mit i*,^ l c (fiH-OO' W, 48*40'N). on ihe vmt l i *hore ol the St. t^w-

I-'.Muary. Bl^ick pU«tir paneU and niaii «lidr« attached to

plywood paneU were immer»ed at conMant depth* of I and 5 mfrom the surface. Some panrK were shaded wiih mosquito netscreen M» ait to modify liRhi tntrntit y while keepinf; other variable*conntant. This produced four tnratment« with different percent-age of ambient light intemitiei.. Two other *et* of paneU wereimmervd in Baie de» Sables ( I m betow mean low water \CVT\),and in Pointe Miti» (5 m below mean low water level). Thesel>aneK were located on the bottom, which subjected them to »emi-ditirnal tide* of amplitudm up to 2 m. further increasing thevariability of light conditions finable I).

Ohienations of living epibenthic diatom» (ettled on the glauslide* were done by light microwopy. For these obwnat ion*, t*tosmall plastic ring% (6 mm diam. x I mm thicknevt) delimiting aSO mm* surface were glued to each slide using tilicone sealant.M> that water c*»uM W retained in the rings during obser\^tion.Sj>ene* groMh forms, measurements of cell \Tlocity and immi-gration rates were determined at low magnifKation (* 125) andlow held illumination, within 3 h o(colle<tion. It w-asnot pauibleto evaluate if thew procctlure* altered cell activity although noobvious change was observed with incTeating held illumination.Cell \elocity was evaiuateti using an t>cu1ar micrometer and aMtipwatch. by measuring the distance travelled by the cell* onrcttilinearM-gmentsol trajeitor^. Cell immigration was evaluatedas the percentage of tells of each speci«, found on slides im-mersed htf 24 h.

The distribution patterns of epil>enthic diatoms **-ere deter-mined using replicate scanning electron microscope (SF.M) ob-M>r%'aiion« on 4-rm* umples punched out of the black plastic

436 CHRISTIANE HUUON AND PIERRE LECENDRE

TABLE I. Dftrnfttwn of ihr immrrtwn rondttions usert frr (ffonttttiorti (Synctin labuiHa)or 0/grmi-th formi ifn-r

(1> MitLS(2) Mills(3) Milt*<4) Miti»(5) Bate drs

Sables16) Mil is

Total

Urirthim}

Ib1

5-1

I5

1 Hbl <•).lluriur

nononono

ve»yes

uirfj.rtiilrltuti)

15-301-5

10-20*3-15"'

10-301-5

niimhri•.1

umplrt

10567

7I I

40

Olhrt

Tii(inlH-i »(

umpW

————

—71

+ 71 - 117

• PancN (hacltrd with mo«|uit*>'' Panel tramfcrrcd from drcp lo thallnw waicr after one month.• Amphotu frutto, Corconns coUata, Gomphonrma kamtsrhalifum, Sa-

tiruta Htrrtta.

panirU. Sample* were fnllecied werkly over an immersion periodt)f up 10 ihrcc months, »o a» to obwrvc a VJLU^V OI' (len»ilic» foreach specie* (Table 2). Earh lumple wai fixed in phwphate buff-ered (pH 7 2) Klutaraldehyde for 2 h and iran*ferred lo a Rradrd»erie% of rthamil w>lution« (25C(. 5O9t. 75*^) for tlchydniiion.Prior lo SEM obwrvation. (he umple« were transferred to ab-Miluic ethano) and air drird. The wmplr» were then glued toaluminum «ub» and coate<l with gold-paItadium (Garland ei al.1979).

Rrpltcaie c(nint« of ihe number of celU of each specie* preienton 500 X SEM fwlds (40000 iim») were made to evaluate themran drnsily <f) and variance (»•). 'I hi» maKniFicalion wa» chtMen

it could contain a lar^r number ol diatom cell* while Millp «imulianefMi» identification of common %))e(-te«. In apreliminary Mmpling. 50 random SEM field* were fir»i ob»crvcdto determine the numt>er of additional field* necesury to KeepIhe «ancUrd error of thr mean below SO";! (Elliott 1977).of thr cate*. the obwrved frequency Hittribution was noticanlly differeni from the expected frequencies of ihe negativebinomial di.Mribuii<m (Pearv>n'» chi* »tati*tic. P > 0.05). Thenegative binomial ditiribuiion model wjitelecled for iikgrnerallyytHid performance 10 de^ribe a^Krc^ation in biolofjical popu'laitrni!( (Taylor ct al. 1979). The mean {S) and the variance (t^were recorded for each diarom specie* ihal wa» sufficiently rep-resented on each of the 4-cm* vimple«. and were analysed as theinitial data trt.

'ITie immersion condition* u»ed for cnmparivins of growthconditions (lor Synrtira tahutalo) Of of firowih forms (five speciesUigetheT) are described in Table I. The spatial distribution <if.Sxtrc rd tahutnta )p-owinf( under different growth condition! wascmnfKired u*inK 46 sample* from 6 ftation» flable I). SynrriraInhutaia was the only sperirs for which the number of sample*from different ItKaiions wasiufhciently large to alUiw examining

the effect of differeni growth condiiion^ on il&spatial diMrihution.Thr samples used to compare the distribution of diatom %pecie»iM-aring different growth (orm* were taken from the samr station(Table I. I able 2).

The mean niimlx-r of cell* of each spetiesjK-r micnwcope field(JE) fnund on the samples, and thr estimated variance (t*) wereuwd 10 analyse ihr disiribulion patlern resultinn from differentgrowth conditions or different growth forms. The data was log-transformed (base 10)lolineari/e therebtionship(TayIor 1961).1 he regression line» ol the iranslormed values of rhe variance(log »•) on the mean (log *) for each data subset were comparedwith re»pect to their slope (ft) and intercept (n), which are twoways of quantifying aggregation (Fllioit 1977). The slo))es and9&'3J confidence intervals were calculated with a Model 11 regres-ition technique (reduced tnajor axis: KrrmackaiW Ilaldatic 1950),which allows for error on both the \ and Y axestSokal and Rohlf1981). When slopes are not significantly different among speciesor growih comlition*^ ihe IntercepiK of the rrgrrsitions can becttm^Kirrd using an analysisofcovariance (ANCOV A). In additionto linearity (obtained by log-trat)sformation)antl homogeneity ofslopes, the assumptions of ANCOVA include the homogeneityof the subset variances, and normality ol (he errors. These con-ditions were verihed on the transformed data using Barilett'l(Si>kal and Rohlf 1981) and Kolmogorov-Sminiov's (Lilliefors1907)ieiis.respccnvcl)'. Since ANCOVA in a Mwlcl I technique,results were double-checked with a multiple linear regressionusing the specie* or thr growth forms as dummy variables.

RESULTS

Epibcnthic diatomx can adopt cilhcr a solitary €>ra colonial form. Cells can have a prostrate or erectptjsturc oti the surfacr, or occur within the com-munily cell matrix, without direct link to the sur-face. 'l"hc capability and type of movemeni*. as wellas speed, can be mcasurea on live cells. Combina-tions of these three basic characteristics define thevarious growth forms (Table 2), Solitary cells wereofien mobile. l>eirig either slow atid prostrate on ihcsubstrate {Cocronfi.\. Amphora), or swift and capableof complex movements within ihe community ma-trix {S'itz.\chia, Sax'irufa). Colonial forms comprisednon-mobile as well as mobile species. Presented inincreasing degree of erectness, we observe Ian ofrosette-shaped colonies adherent to the surface byone apex {Synedra) (Fig. 2A): ramifted arborescentforms {Licmophora, Gomphonema, Rhmrosphfuia): fi-nally, linear chains {Fragilnria, Mehura. Biddulphin,Hhnbdonfma).

Presence or absence t>f movement, and measure-ment of speed* showed the range of "behaviours"

T A B U 2. Dtienptum of tlu growth form ihararlrmtut ohientd on ihf fnt ipft\«\ of d\atom\. \tohiltly It gn-rn at: mran (tiandnrd dnialmn}.

Sf in tr%

S'aivtita diTfdaAmpham pu\utCoffonn^ foiMtnSynritra lahulataGomfthonrmn

kamUrhattcumTotal

Fmm

HtlitarysolitaryMilitarycolonial

colonial

Pinlurr

matrikprostrateprostrateupright

upright

M»tHhhfnin » '\

12.4(2.4)7.5(1.4)3.3 (0.4)

no

Immi rjrw1*)

35.57< 1< 1-913-29

1-3

Si.n.l»

176

2946

19117

0,8-23.71.3-6.91.1-22.91.7-106.4

0.5-24.1

I ) l . t i i i i l i t l i i i i i i K i i i i w l i l o m n

U S, . ,U- h . i t € . , . . . ( ! • . HID Mill i l l l

St . i l«- l. . .t c i K - i h m i l M"i K 1 N « i l

In tii

vlu|>r<f

llit-

Ir.

V t . 'wt t .t

tUV \hl>H

fCtUJMI (

(f V.tlr

t h r |lllM<f(

)..tT <• i h r 1

•«ni,iK

t r •>! ({

100 u

Irti• •(

,mi h r• 1)1

438 CHRISTIANEHUDON AND PIERRE LEGENDRE

SUBSETSlog X-f(logS-')

Slap« and 9S% Contldence Interval

1.0 2.0SPECIES: N

t

2

3

4

5

6

m* N10

6

•

T

t l

Ftc. S. CompariKin of Uopci and of 95% confidence intenaUfor Ihe fivp tpettn of rpibcnthif diatomi (upper panel) and forthe »ix groMth condittont for Sjnedra latmlala (lower panel).

encountered among cpibcnthic diatoms. Mobilespecie* associated wtth the substrate exhibited rep-ctilious movements, slowly gliding, stopping, andreversing their direction every few minutes. Move-ments of this type did not exceed 8 ;im» ', and thenet displacement produced by the reversing motionwas small. Cocconeis and Amphara were commonlyobserved moving in such fashion; some Saviculaspecies also exhibited this type of movement (Fig.2B).

Species moving freely within the communityshowed both a higher speed and greater variety ofmovements. For thos<? cells, the presence of a slimetrail and the direct contact with the substratum usu-ally associated with diatom locomotion were not al-ways observed. Solitary cells could execute wide gy-rations and complex rotations along their long axes.When the tip of the valve CKcasionally touched ihesurface, it could terse as a gyrating point. Lineardisplacement was more important than for the pre-vious group as the measured speed was over 10 Mtn •s"'- In this group were membersof the A'i/iifAia andSaxncula genera (Fig. 2C). It is noteworthy that dif-ferent types of movement could be observed amongspecies of the same genus.

Ftu. 4. RegreiMon line^ of loff-variances over log-means, forthf five tpeciet of rpibrnlhic diatomt. The interruption of theline next to "adjusted intercepts" indicaiesa ftignifirant differencebetween thr tpctirv Intercepts arc adjusted for thelines as a rrsult nf analysis of covariance.

Cells of raphc'bearing genera such as Achnanthes,Rhoicosphenia and Gomphonema should possess theability to move (Halfen 1979). but were not observeddoing so in this study. These tyi>es were always foundbearing a mucous stalk located some distance fromneighbouring cells. The structure of the monospe-ciBc clump suggested that a short migration (1-2cell lengths) had taken place from the originatingcell (Fig. 2D).

Savicula spp. was the fastest settling group, representing from 33 to bl% of alt celU found after 24h of immersion (Table 2). Intermediate settlementrates were achieved by Synedra tahulata (13-29%)'Cocconeiscostatct {< I -9'X). Gomphonema kamtschaticuyn(1-3^). and Amphora pusio (<17c) had low immi-gration rates on glass slides.

For all species, observed frequency distributionsobtained from cell counts on the suostrate agreedwith the binomial negative distribution. Agreementwith this theoretical distribution indicateu that theorganisms were strongly aggregated and occurredinitially in patches intersper-kcd on the otherwise baresurface; this coincides with visual qualitative obser-vations during colonization reported in a previouspaper (Hudon atid Bourgct 1981),

The slope of the regression of the variance on themean (in log) provided an indication of the rate of

GROWTH FORMS IN EPIBF.NTHIC DIATOMS 439

ADJUSTED MEAN VALUES 1 3 i 1.47 i 80 1.79 183

Slonfcanl dllterences | 11 |

Species ot diatoms N.d. O.k. A.p. S.t.C.c.

Growth lorm BiologicalImDHcatloni

ADJUSTED MEAN VALUES i 31

• _

I 8« I so

Signtllcant differences

Orowin forma

Fio. 5.

Fast Non-mobOe Slowmoving colonial moving

cell 8 C0ll8 C«ll8

K oCihc a poiUrton lots of tompariMins of mcam.*i>oficn (ahbrcviaiitJii* of !h)

lablr '1). l.«wer iMiirl: iK-twcrn growth r«rm».

increase of aggregation with density. The slope ofthe rf^ression tended to be larger ("or solitar)-. slow-moving species {.\mphora pusio and Cnccotieis costata),iiuiicating ihat aggregation lends lo increase fasterwith density for these two s(>ecies than for mobileor colonial species. This difference was particularlymarked for the species located at the ends of therange {Coccojtets costata and Savicula directa), for whichthe confidence intervak of the sloi;>e& did not overlapat the 95'^ level (Fig. 3). However, this differencewas marginal and disappeared at ihe99'?f confidencelevel, which authorizes the use of the analysis ofcovariance (ANCOVA); this analysis will serve lointerpret the differences in intercepts among thefive species under study.

In the context of this study, the intercepts of theregression lines of the variance over the mean (inlog) can be used as an index of aggregation for eachspecies (Downing 1979. Taylor 1980). Differencesin the intercepts should then indicate w hich of (hefive species of diatoms was the most efficient surfaceinvader. Comparison of the intercepts using AN-COVA showed that very highly significant differ-ences (P S 0.001) existed among intercepts. A pos-teriori comparisons showed this to be due to a singledifference, between Saxicula dtrecta and the fourother species (Fig. 4, Fig. 5. upper panel). The dif-ference remained when species were re-grouped onthe basis of their mobility (Fig. 5, lower panel). Thisresult was confirmed by a multiple linear regression^ith dummy variables. On the other hand, no dif-ference in aggregation was found among growingconditions for Synedra tabulata, showing that thephysical arrangement of multiplying cells remainedconstant regardless of the light regime.

OlSCt'SStON

The ecological vignificame of growth forms is bestihowii b ' (he great plasticity of the physical arrange-'Tient of cells in space, which lessened the impor-tance of this factor in recent taxonomic studies ofdiatoms (Patrick and Reimer 1966). Relations be-

Form

Po«tuw

SoBtary

Colonial

V *

ETtCl

tnvnobilt

Mobnity vB

Fic. 6. RrUliomhip^ briwr«ii gr*»Hth form chanctcmtics.ihc hiningical properiirj i hn indurr. and ihrir ccoto^cal rmpli-rahont.

tween grow th forms and ecology were discusived forphytoplanktonic algae (Margalef 1978. Sournia1981) as well as for macroalgae (Liitler and Littler1980). This approach allows the integration of mor-phology, ecological interactions (competition, pre-dation), and physiological functions (primary pro-ductivity and respiration) and the elaboration of amodel describing the ecological implications ofgrowth forms of epibenthic diatoms.

F.pibenthic diatom populations offer many advan-tages for the quantitative study of changes occurringin the distribution of organisms as a response tochanges in their environment. Contrary to studiesdealing with macroscopic organisms, a large numberof replicate quadrats can be processed quickly toobtain estimations of mean density and its asscxriatrdvariance within a pre-selected level of precision.Short generation time also allows easy manipulationand observation of a wide range of densities. Theepibenthic diatom community thus represents anideal material for studying the implications of thedifferent growth forms with respeci to space utilis-ation, under different environmental conditions.

The aggregated distribution of epibenthic dia-toms can be explained by the rapid division of cellsthat immigrated from the ouiside medium and set-tled on the experimental surfaces. If uniform mi-crohabitat conditions prevail, migrant cells shouldsettle at random and their successive divisions shouldproduce randomly distributed clones. If local mi-crohabitats are found on the surface, due to obsta-cles (detritus, other cells) to water flow, the presenceof microeddies will enhance the probability of set-tlement of cells in their immediate neighbourhood(Stevenson 1981). and consequently increase the ag-gregation of cells. An example of this phenomenonis observed in Figure 2A. in which cells of otherdiatom sf>ecies and detritus are found within a clumpof Synedra tahulata growing on an otherwise baresurface.

440 CHRISTIANF HUDON AND PIFRRF. LF.GFNDRF.

In turn, each growth form characteristic mightbe expected to bear certain biological properties,with ecological implications that might influence thesuccess of each species (Fig. 6). These elements per-tain to three categories: nutrients and light avail-ability, susceptibility to grazing, and emigration andcolonization rates.

Our results showed that four species, two of themcolonial and non-mobile {Synedra tabulata and Com-phonema kamischaticum), and two solitary and slow-moving {Amphora pUMo and Cocconeii coslata), werecharacterized by a simitar, highly aggregated pat-tern. This suggests that the characteristic form (co-lonial or solitary) does not bear an overwhelminginfluence on species distribution patterns. However,the characteristic form affects the surface-to-volumeratio (S/V) cif the celK. Previous studies carried outon phytoplankton (Sournia 1981) showed that theincrease in size generated by the colonial form de-creased S/V. therefore allowing lower light absorp-tion and nutrient assimilation than for small solitarycells. The higher relative efficiency of small cellsmight partially explain their higher representationamong solitary slow-moving diatoms.

The similarity that we observed between distri-butions of slow-moving and of immobile species alsoindicate* that the capacity to move a little gives buta small advantage over immobile sjK'cies in terms ofsurface monopoly strategy. Mowe%er. moving a littlecan be useful for individual cells to invade cracks ofthe surface {as shown in Figure 2B). or to emergefrom under an obstacle to reach light; it certainlyfacilitates clonal expansion. This result also suggeststhat the growth rate of cells within a clone is cen-trifugal, showing an increase from the center to-wards the edges, because there is room for expan-sion only at the edge of the clone. In colonial sijecies,expansion away from the surface might be the al-ternative solution, allowing cell spacing and avoid-ing overcrowding. It has been proposed thai verticalexpansion improves light and nutrient availabilitybut makes the uppermost layer of cell* vulnerableto sloLtghing-off by currents (hloagiand 1983, Hu-don and Bourget 1983. Luttenton and Rada 1986.Steinman and Mclntire 1986) and by grazing (Hu-don 1983).

With resj)ect to grazing, the apparent selectivityor avoidance of grazers towards particular sp<'ciesof diatoms was shown to be related to diatom avail-ability, which was in turn related to their postureon the surface. A wide variety of grazer*, from cil-iate» to tadpoles, were reported to "select" arbo-rescent and filamentous colonial diatom* over small,prostrate specie* (see the review by Hudon 1983),High aggregation may al«) result in an all-or-noth-ing impact under a randomly occurring grazingpressure or local disturbances. On the other hand,nighly dispersed species will have a high probabilityof experiencing minor losses under all conditions.A frequent "cropping" of the disjjersed fxipulation

may reduce the chances of overcrowding and of ac-cumulation of excretory products, thus stimulating ,cell division.

Alternatively, the low adhesion of highly mobile 'cells (see the review by Harper 1977) and their easyresusfwnsion in the water as Iree-Moating forms maycontribute to their early colonization of freshly im-mersed surfaces (Patrick 1967). This opportunisticstrategy is supported by the high percentage of oc-currence of Xaj'irula cells on new glass slides after24 h immersion, and could represent a positive trade-off against their physical vulnerability.

From results of previous studies and from ourobservations, it appears that not all combinations ofform. |M>Mure and mobility are found in nature, pre-sumably l^ecause some of these combinations cu-muhite more cost than benefit. Solitary prostratecells are often mobile, possibly to alleviate the dis-advantages of smothering. It is notable that specieslikely to be smothered or living in low light envi-ronments have dcvehiped phvsiological a<laptationslocompensatetheeffectsoftdeir growth form. Fre-quently buried epipsxnnmic forms possess a strongtolerance to darkness and anoxia (Moss 1977)whereas most mud-dwrlMng forms, capable of fastmigration back to the surface of the mud (Harper1977). do not tolerate those conditions (N(oss 1977). '

On the other hand, colonial non-mobile forms areseldom prostrate on thr surface. This c<iuld resultfrom the positive phototropism of the growing fil-ament (Dennison 1979). making the cells grow awayfrom the surface and thus maintaining their erectposture. In this study, the aggregation of a non-mobile colonial species did not respond to changesin the environment {Synedra tohulata). This indicatesthat cells may adapt physiologically to their lightenvironment before undergoing changes in theirphysical organisation on a surface. The physiologi-cal adaptations of cells during an increase in densitywas shown for the filamentous species Tahrllaria floe-cuhna. Filament* of this species had different pho-t<i*ynthetic capacity and pigment ratio w hether theywere sampled close to the r<Kk on which they wereattached or near the apex of the filament (Hudonet aL 1987). Other mechanisms may contribute tothe vertical expansion of colonial forms, such as waterm«jvement or the entrapment of oxygen bubbleswithin the mucous matrix of the colony (C. Hudon.per*, obs.). F(»r tube-dwrlling s|>ecies, the immobilestance of the tube itself could be compensated bythe mobility of the individual cell within it. Fur-thermore, the capability of this group to survive andcoloni/e new surface* as solitary individuals or as acolony provides additional ecological llexibility.

The auihiir\ thank Ur», K. Iitturtiri. J, DoKtniiH and aiionymnii*rrvirwrr* for ihrir hc-lprtil nmirncnr* <)fi cHrlirr Hrafi* «if ihr Imanuvri|>|. I he arJvirr nf Mr. A \'au(inr «n cljla Uratinrnl wii»alfto very ap(irrciaicH. Mr. J.-P. RitUmrR. from INRSGrorr*-»ourcM. prtividrd valuable iiMitlancr wiih ihc wanning rlcctron

GROWTH FORMS IN EPIBF.NTHIC DIATOMS 441

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