Seasonality and diversity patterns of microphytobenthos in ... · Seasonality and diversity...

Arch Hydrobiol 167 1ndash4 447ndash465 Stuttgart September 2006

Seasonality and diversity patterns ofmicrophytobenthos in a mesotrophic lake

N Aberle1 2 and K H Wiltshire3

Max Planck Institute for Limnology Ploumln

With 5 figures and 3 tables

Abstract Investigations on the littoral microphytobenthos populations of lakes arevery rare Based on new sampling techniques allowing the undisturbed sampling ofsublittoral sediments we present information on limnic microphytobenthos popula-tions of the Schoumlhsee in Northern Germany (10˚ 26prime E 54˚ 13prime N) Investigations onmicrophytobenthic communities at a sandy and a muddy site provided new insightsinto the community structure and seasonal variations of limnic benthic microalgaeThe microphytobenthos was characterised by low chlorophyll-a contents (016 microg cmndash2

to 074 microg cmndash2) and low cell numbers (25 cells cmndash2 to 266 cells cmndash2) Both sitesshowed similar patterns in terms of algal biomass and seasonality no site-specificcharacteristics were observed The productivity of the sediment microflora in theSchoumlhsee was low and most likely related to the mesotrophic lake character and to re-duced light conditions in the near-shore sublittoral The algal communities at both sitesshowed high diversity distinct seasonality and succession patterns with shifts in com-munity composition in spring summer and autumn The community was dominated byFragilaria spp Navicula spp Nitzschia spp and Stauroneis spp in spring shifting toa Stauroneis spp-dominated community in summer In autumn the populations weredominated by Navicula spp Nitzschia spp and Stauroneis spp Overall the taxo-nomic composition showed a dominance of prostrate diatoms whereas cyanobacteriagreen algae and erect diatoms occurred rarely and with low abundance Thus the sedi-ment microflora of the Schoumlhsee can be characterized as a flat two-dimensional com-munity

Key words low productivity algal biomass edaphic algae epipsammon sediments

1 Authorsrsquo addresses Present address Leibniz Institute of Marine Sciences (IFM-GEOMAR) Duumlsternbrooker Weg 20 24105 Kiel Germany2 Max Planck Institute for Limnology August-Thienemann-Str 2 24306 Ploumln Ger-many3 Biologische Anstalt Helgoland Stiftung Alfred-Wegener Institute for Polar and SeaResearch P O Box 180 27483 Helgoland Germany

DOI 1011270003-913620060167-0447 0003-9136060167-0447 $ 475 2006 E Schweizerbartrsquosche Verlagsbuchhandlung D-70176 Stuttgart

448 N Aberle and K H Wiltshire

Introduction

Sediment microflora comprises of microscopic photosynthetic eukaryotic al-gae and cyanobacteria that live on or within the sediment These microorgan-isms are restricted to the surface layers of sediments due to the depth penetra-tion of light (MacIntyre et al 1996) and they therefore play an importantrole for nutrient and oxygen fluxes at the sediment water interface (Joslashrgen-sen et al 1983 Wiltshire et al 1996) Their occurrence is governed by envi-ronmental parameters making them sensitive indicators of water quality (Lan-ge-Bertalot 1979) and their key function as primary producers and as a foodsource in littoral zones has been emphasized in many studies (Colijn amp DeJonge 1984 McCormick amp Stevenson 1991 Pinckney amp Zingmark 1993Hillebrand et al 2002)

Although the diversity and functional role of microphytobenthic commu-nities has become a major topic in marine benthic research over the last twodecades (Sundbaeck amp Joensson 1988 Blanchard 1991 Montagna et al1995) its potential importance in the littoral zones of freshwater lakes has re-ceived little attention Consequently not much is known about the composi-tion fluctuation and seasonal occurrence of the sediment microflora in fresh-water habitats (Lowe 1996) Most studies carried out in freshwater benthicsystems focused on epilithic or epiphytic algae growing on solid substrates(Sumner amp McIntire 1982 McCormick amp Stevenson 1991 Kann 1993Cox 1993 Lowe 1996 Hillebrand amp Kahlert 2001) In contrast studies onepipelic algae (algae moving actively through the sediments by means of theirraphes Round 1971) or epipsammon communities (algae growing attached tosediment particles Round 1971) are rare (Round 1957 Hickman amp Round1970 Miller et al 1987 Khondker amp Dokulil 1988 Cyr 1998 Nozaki etal 2003) This is the case even though soft sediments often represent the mainsubstrate in shallow lakes and epipelic or epipsammic algae can reach highbiomass and productivity (Khondker amp Dokulil 1988 Cyr 1998)

To increase our understanding of the specific composition of microphyto-benthic communities in temperate regions a survey was conducted in Schoumlh-see (Ploumln Germany) in the summer of 2001 With respect to planktonic param-eters the Schoumlhsee is well-studied but until this study the benthos had re-ceived little attention This study was aimed at providing first baseline infor-mation on the abundance diversity and seasonal variations of benthic micro-algae in the Schoumlhsee Both sandy and muddy sediments were examined toevaluate potential differences in community structure and seasonal variationsof these poorly understood limnic microalgal communities We aimed at non-destructive sampling allowing high resolution (microm) vertical profiling in orderto determine the potential microalgal stratification in the sediments (see Wilt-shire 2000)

Microphytobenthos in a mesotrophic lake 449

Material and methods

Sampling sites

Investigations on natural microphytobenthic communities were conducted from Mayto October 2001 in the Schoumlhsee (10˚ 26prime E 54˚ 13prime N) The Schoumlhsee has a surface areaof 078 km2 with a shoreline length of 47km The mean water depth is 109 m with amaximum depth of 294 m The lake has a small catchment area (215 km2) and with itslow total phosphorous (average TP = 21microg Lndash1) and low chlorophyll-a contents (aver-age chlorophyll-a = 21microg Lndash1) (Grey et al 2004) this lake can be categorised as meso-trophic with a low productivity in the water column The organic carbon contents ofsediments range between 13ndash20 percent by weight at 10 m water depth and 85ndash30percent by weight at 15 m water depth (Grey pers comm) Two different sites werechosen in order to assess potential influence of sediment characteristics (muddy andsandy) on the structure of microalgal communities The sites were 30 m apart in the vi-cinity of the island ldquoKleiner Warderrdquo at a distance 100 m from the shore and they hadan area of 025 m2 each The sandy site was at a water depth of 08 m whereas themuddy site was at 12 m depth

Sampling and experimental design

It is imperative that the structure of microphytobenthos populations is preserved andnot disrupteddiluted in the sampling process (see Wiltshire et al 1997 Wiltshire2000) This is especially difficult in submerged sediments To this end a new samplingtechnique was developed to keep disturbance of the sediment surfaces to a minimumduring sampling Sediment caps filled with autoclaved natural sediments from the siteswere deployed prior to the experiment These caps were open-ended cylindrical plastictubes (empty 14 mm surface area 154 mm2) with a screw cap A plastic gauze (mesh widthof 500 microm) was glued to the bottom of the caps to permitting contact with the sur-

screw cap

plastic tube

gauze (500microm)

sediment

25 mm

14 mm

screw cap

plastic tube

gauze (500microm)

sediment

25 mm

14 mm

Fig 1 Sediment cap (cylindrical plastic tubes) provided with a screw cap for closingin situ


rounding sediment and allowing diffusion (Fig 1) The caps were filled with auto-claved sediment from each site closed with a lid and frozen to ensure that the structurewas maintained and the sediment did not slip out of the cap at insertion At the begin-ning of the survey 36 frozen caps were inserted by SCUBA into the sediment at eachsite The cap sediment surface layer was aligned flush with the surface of the surround-ing sediments and thereafter the lids were removed The first sampling took place fourweeks after the field deployment Thereafter once a month six caps were chosen ran-domly at each site closed under water and transferred to a tray in order to keep thesamples in an upright position The sampling caps were returned to the water surfaceand immediately preserved

Sample preservation

The original Cryolander sampling procedure described by Wiltshire et al (1997) wasused in a modified manner to sample the Schoumlhsee sediments Because the device can-not be used under water the technique was modified slightly The Cryolander consistsof a brass tube (1mm thick) which is 50 mm in diameter and 80 mm in height In orderto preserve the uppermost surface layer of the caps immediately after the return to thewater surface the Cryolander was placed on top of the sediment surface of each tubeand liquid nitrogen (3ndash5 ml) was then gently dribbled on to the absorbent cotton of theCryolander Since the cotton is at ambient temperature the liquid nitrogen vaporisesand this vapour freezes the sediment surface immediately without distortion even on amicrometer scale Once the surface was frozen the liquid nitrogen was poured onto itevenly through the Cryolander mesh The depth of frozen sediment increased rapidlyuntil an approximately 2 cm thick layer was frozen The samples were then stored inliquid nitrogen for future use

Sample processing

The frozen samples were cut into 1cm thin discs in the laboratory Subsequently thetop sediment disc was placed on the stage of a freezing microtome (Leica CM 1900)using a freezing medium to stabilize the sample thus ensuring that the sediment sur-face was absolutely horizontal Two 250 microm thick slices where then cut off the top thesurface layer from 0ndash250 microm and the deeper layer from 250ndash500 microm A description ofthe micro-slicing technique is given in Wiltshire (2000) For cell counts and taxacomposition these sediment sections were fixed with Lugolrsquos iodide solution trans-ferred to a Sedgewick-Rafter counting chamber and counted under an inverted lightmicroscope at a 200 times magnification The microphytobenthos was identified to genuslevel as a precise determination of freshwater microphytobenthos to species-level re-quires a laborious working-up of the samples and the use of an electron microscopewhich makes unsuitable for the kind of study performed here Moreover the presentstudy was geared to determining morphotypes and communities and thus such com-plexity was not required This is an accepted way to proceed in the literature (seeRound 1960 Wasmund 1984 Hillebrand amp Kahlert 2001 2002)

The results from the surface and the sub-surface layer were pooled for taxonomiccomposition thus the data presented here comprises algal cells from 0ndash500 microm sedi-


ment depth Chlorophyll-a sample processing and HPLC-analysis followed the pro-tocol described by Wiltshire (2000)

Statistical analysis

To test for significant differences in total cell numbers and chlorophyll-a contents forsurface and subsurface sediments at both sites a two-factorial ANOVA with the inde-pendent factors horizon (F1) and site (F2) and a Duncan-test were used For compari-sons of seasonality patterns within each sediment type a two-factorial ANOVA wasused with the independent factors month (F1) and sediment horizon (F2) Diversity in-dices were calculated and multivariate analyses were carried out using PRIMER 52(2001 Primer-E Ltd) and STATISTICA Diversity was measured by the Shannon-Wiener function (Hprime loge) (Shannon amp Weaver 1963) The similarity of sampleswas calculated using MDS ordination analyses based on untransformed data

Results

Chlorophyll-a contents

The chlorophyll-a concentrations showed significant variations between hori-zons and sites (Fig 2 A p lt 005 Table 1 A) The chlorophyll-a concentrationsat the sediment surface of sandy sediments were significantly higher than onmuddy sediments (p lt 005 Duncan test) but these differences disappearedwith increasing sediment depth

The seasonality patterns of total chlorophyll-a contents at the muddy siteshowed fairly uniform values throughout the whole sampling period (Ju-nendashOctober) with no significant differences between months and horizons(p gt 005 Table 2 A)

Table 1 Total chlorophyll-a (A) and total cell numbers (B) at the sandy and the muddysite Results of a two factorial ANOVA with horizon (s d) and site (mud sand) as in-dependent factors and total chlorophyll-a or total cell numbers as dependent variables

(df) MS F-ratio P-level

(A) Chlorophyll-aHorizon 1 02126 65134 00139Site 1 02505 76725 00079Horizon times site 1 00695 21291 01510Error 48 00326

(B) Cell numberHorizon 1 130314 1267690 00007Site 1 17805 173206 01927Horizon times site 1 39 000380 09510Error 66 10280


Fig

2C

hlor

ophy

ll-a

conc

entr

atio

nsin

microgcm

ndash2

(A)

and

tota

lal

gal

cell

num

bers

ince

llscm

ndash2

(B)

ofth

em

icro

alga

lco

mm

unity

onsu

rfac

e(0

ndash25

0microm

)an

dde

ep(2

50ndash

500

microm)

laye

rsof

mud

and

ofsa

ndin

the

Schouml

hsee

sam

pled

from

May

Jun

eto

Oct

ober

2001

Err

orba

rssh

owth

est

anda

rdde

viat

ions


Table 2 Seasonality patterns of chlorophyll-a on mud (A) and on sand (B) Results ofa two factorial ANOVA with month (JunendashOctober) and horizon (s d) as independentfactors and total chlorophyll-a as dependent variable


(A) MudMonth 4 00496 23980 00843Horizon 1 00230 11129 03040Month times horizon 4 00030 01449 09631Error 20 00207

(B) SandMonth 4 01049 37442 00335Horizon 1 01937 69085 00220Month times horizon 4 00465 16581 02238Error 12 00280

Chlorophyll-a concentrations at the sandy site showed significant varia-tions between months and horizons (p lt 005 Table 2 B) Significantly higherchlorophyll-a contents at the sediment surface were detected in July and Sep-tember when compared to June and the surface values in October where sig-nificantly lower than in September (p lt 005 Duncan test) In contrast to themuddy site a significant difference between surface and subsurface sedimentswas found on sand (p lt 005 Duncan test)

Total cell numbers

The total cell numbers also showed significant variations between sedimenthorizons (Fig 2 B p lt 005 Table 1 B) no differences between the sites werefound (Fig 2 B p lt 005 Table 1 B) The total cell number at both sites washighest in May and a decline during the summer and autumn period could bedetected (Fig 2 B p lt 005 Table 1A and B) At both sites algal abundancewas higher in the surface layer (0ndash250 microm) than in the deeper layer (p lt 005Table 1A and B) Lowest surface cell numbers were found for September forboth the muddy and the sandy substrate A slight increase was found in thesurface layer in October

For the muddy sediment the surface cell numbers in May surface showedsignificant differences when compared to all other months (p lt 005 Duncantest) In addition the June algal abundance in the surface layer was signifi-cantly different to May July and September (p lt 005 Duncan test) The sur-face sediments sampled in September and October were significantly differentfrom one another (p lt 005 Duncan test) For subsurface layers significantlyhigher cell numbers were detected in May compared to samples taken fromJune to October (p lt 005 Duncan test)


Table 3 Seasonality patterns of cell numbers on mud (A) and on sand (B) Results of atwo factorial ANOVA with month (MayndashOctober) and horizon (s d) as independentfactors and total chlorophyll-a as dependent variable




For the sandy site significant differences between months were found at thesurface (p lt 005 Duncan test) but not for the subsurface layer (p gt 005Duncan test) The cell numbers at the sediment surfaces showed significantdifferences between the samples taken in May June and August compared tosurface sediments sampled in July September and October (p lt 005 Duncantest)

Taxonomic composition

The sandy as well as the muddy sediments were colonized by similar algal as-semblages and both sites showed the same seasonality patterns

The ordination analysis between months on the muddy site showed similar-ities of algal communities sampled in May and June (Fig 3) In both monthsFragilaria spp (17ndash19 ) Navicula spp (12ndash19 ) Nitzschia spp (5ndash13 )Stauroneis spp (8ndash9 ) and Pinnularia spp (4ndash13 ) were dominant(Fig 4 A) The chain-forming benthopelagic Melosira spp comprised 5ndash6 of the total algal community The genus Synedra spp was present in bothmonths but showed a strong dominance only in June (35 ) In addition fila-mentous green algae comprised 5 to the total algal community in May andthe colonial green algae Pediastrum spp 1 whereas cyanobacteria were notpresent at all The numbers of green algae decreased dramatically in June InJuly a transition phase started and from this month onwards the algal commu-nity changed to a Stauroneis spp-dominated population which contributedfrom 28 to 43 to the total algal community (Fig 3) Other dominant taxawere Synedra spp (11ndash15 ) Navicula spp (11ndash19 ) and Pinnularia spp(11ndash13 ) and remained similar until September In addition the taxon Gyro-sigma spp was highly abundant in July (20 ) In October these distributionpatterns changed and a clear dominance of Nitzschia spp was seen (35 )


Fig 3 Similarities () in taxonomic composition between algal communities of differ-ent months on mud (M) and on sand (S) in the Schoumlhsee sampled from May (M5 S5)to October (M10 S10) resulting from MDS ordination analysis Absolute cell numbersin the top 500 microm of the sediments are considered

Other abundant taxa in October were Diploneis spp (15 ) Stauroneis spp(16 ) and Pinnularia spp (11) From July to October no green algae and nocyanobacteria were found a feature which most likely contributed to similar-ities between the summer and the autumn communities that were revealedfrom ordination analysis (Fig3)

On the sandy substrate similar distribution and seasonality patterns werefound to the muddy sediment Ordination analysis revealed similarities be-tween May and June samples (Fig 3) Both months showed high percentagesof Synedra spp (23ndash30 ) Fragilaria spp (14ndash17) and Navicula spp (13ndash14 ) (Fig 4B) In June Stauroneis spp had increased to 16 of the total algalcommunity and the genus Amphora appeared (5 ) In addition the green al-gae Pediastrum spp comprised of up to 5 of the total algal community inMay and up to 6 in June whereas cyanobacteria were missing With the startof the summer period the samples changed in composition In July the algalcommunity still showed patterns similar to those found in May and June(Fig 3) Cell numbers of Stauroneis spp (30 ) and Amphora spp (10 ) in-creased whereas percentages of Navicula spp Synedra spp and Fragilariaspp decreased During the summer (JulyndashSeptember) Stauroneis spp (30ndash47 ) and Synedra spp (11ndash23 ) dominated The genus Amphora spp (6ndash10 ) Navicula spp (5ndash15 ) and Pinnularia spp (8ndash9 ) contributed less to


Fig

4T

axon

omic

com

posi

tion

ofal

gal

com

mun

ities

onm

ud(A

)an

don

sand

(B)

inth

eSc

houmlhs

eesa

mpl

edfr

omM

ayto

Oct

ober

2001

All

taxa

give

nas

spec

ies

plur

al(s

pp)

asal

lge

nus

whe

rere

pres

ente

dby

seve

ral

spec

ies

Rel

ativ

eab

unda

nce

ofdi

ffer

ent

taxo

nom

icgr

oups

isca

lcul

ated

as

ofth

eto

tal

alga

lce

llsT

otal

cell

num

bers

(cel

lscm

ndash2 )

are

give

nas

the

sum

from

surf

ace

and

deep

sedi

men

tla

yers

and

are

illus

trat

edas

alin

e


the total algal community In October the microphytobenthic assemblage wasco-dominated by Navicula spp (32 ) and Stauroneis spp (31) and Syned-ra-cells decreased in number (9 ) Pinnularia spp made up 10 of the au-tumn community and Gyrosigma spp appeared (7 ) As for algal commu-nities on mud no green algal and no cyanobacteria taxa were found in thesummer and autumn leading to similarities between both seasons (Fig3)

Diversity

The diversity index Hprime (referring to changes in the number of taxa) for thesandy and the muddy substrates showed similar diversity patterns Diversitywas significantly higher in May June and July compared to August (p lt 005)where the diversity reached a minimum on mud and on sand (Fig 5) Diversityslightly increased again in September and October although the diversity inSeptember was still significantly lower than in May (p lt 005)

Discussion

This study aimed at identifying seasonal community patterns in unproductivelakes and to improve our knowledge on lake systems in general By comparingtwo different substrate types the heterogeneity of microphytobenthos wasconsidered and first high resolution vertical profiles for sublittoral micro-phytobenthos in freshwater systems are presented As investigations on micro-phytobenthic populations in limnic habitats are rare our investigations con-

Fig 5 Diversity (Hprime) of the algal community on mud and on sand in the Schoumlhseesampled from May to October 2001 Mean values and error bars as standard deviations(SD) are given


tribute to a further understanding of freshwater sediment microflora commu-nities

Sampling methodology

The successive sampling of sediments is highly disruptive and destructive insediments When addressing succession patterns in microphytobenthos com-munities it is imperative not to destroy the surface matrix of the surroundingsediment Compounding this is the fact that the methods (e g sawn-off syrin-ges or coring) are highly unreliable when it comes to the upper layer of sedi-ments (Wiltshire et al 1997 Wiltshire 2000) and furthermore they areparticularly unreliable under water Thus we had to develop a new way ofsampling underwater sediments for successional patterns of microalgae in thesurface millimetres The cylindrical caps used in this study were filled withautoclaved sediments and were transferred to the sediment site where theywere colonized by microalgae The colonization period prior to sampling wasfour weeks and due to the normally very rapid microalgae re-colonization ofsediments covered with water e g six days for intertidal sediments (Under-wood amp Paterson 1993) the bare sediment was likely in equilibrium withthe surrounding sediments after one month Furthermore our data also showedthe classical decreases in microalgal abundance after its climax populationsince the cell numbers from May to June at both sites had already declinedconsiderably


The total chlorophyll-a content (uppermost surface layer of 0ndash500 microm)showed similar concentrations at both sites Compared to other studies on lakesediments these values are at the lower end of concentrations measured inNeusiedlersee (Khondker amp Dokulil 1988) Lake Mikolajskie (Wasmund1984) Lake Biwa (Nozaki et al 2003) and at three lakes in Southern Ontario(Cyr 1998) One possible explanation for higher chlorophyll-a concentrationsdetected in previous studies might be related to the different methods usedClassical photometric or fluorometric techniques for example tend to overes-timate chlorophyll content (Gieskes amp Kraay 1982 Schanz amp Rai 1988)

We sampled the absolute surface without mixing it with sediments belowThis can either dilute a sediment with the non-chlorophyllous material in sedi-ments with sharply decreasing chlorophyll gradients or increase the values persurface unit if for example a sediment has a deep chlorophyll layer (Wilt-shire 2000) In contrast to our study previous studies used the first top centi-metre of the sediment surface in order to detect total chlorophyll-a contentsThus the pigment concentrations measured also include chlorophyll-a from


deeper sediment layers Wasmund (1989) for example found that appreciableamounts of intact chlorophyll-a could be found down to 10 cm sedimentdepths and consequently these pigments were situated below the depth towhich light penetrates However a significant portion of chlorophyll-a foundat deeper sediment layers originates from older settled planktonic material(Stevenson et al 1985 Wasmund 1989) which is not distinguishable frombenthic microalgae chlorophyll-a Therefore in lakes with a high contributionof planktonic biomass to the sediments detecting chlorophyll-a from surfacesediments at a centimetre scale may lead to an overestimation of chlorophyll-aderived from benthic microalgae alone

Additionally in studies where much higher chlorophyll-a concentrationsoccurred they were usually correlated with mass occurrence of particular algaltaxa Nozaki et al (2003) for example found that the development of fila-mentous green algae contributed to a sharp increase in algal biomass fromApril to June in Lake Biwa as a result of eutrophication This was supportedby several studies showing a strong link between mass occurrences of green orblue-green benthic microalgae in relation to high water column nutrients(Kann 1940 Kann 1993 Hillebrand amp Kahlert 2001) The absence ofsuch mat- or filament-forming algae in our study is most likely responsible forlow chlorophyll-a concentrations of sediments in the mesotrophic Schoumlhsee afeature that might be typical for unproductive lakes

The microscale vertical distribution of chlorophyll-a showed different pat-terns for the muddy and the sandy site On the muddy substrate the surfacelayer chlorophyll-a concentration was similar to the sub-surface layer valueswhereas on sandy substrate higher values were found at the sediment surfacewhen compared to deeper sediment layers As total chlorophyll-a concentra-tion are known to decline with increasing sediment depth (Wasmund 1984)and highest chlorophyll-a concentrations are usually found in the surficial mil-limetre of sediments (Gaetje 1992 Wiltshire 2000) the distribution patternsfound on mud seem surprising The high chlorophyll-a concentrations atdeeper layers are however most likely related to the physiological status ofthe microphytobenthos when depth penetration of light is low (Wasmund1984 Pinckney amp Zingmark 1991 MacIntyre et al 1996) We know fromstudies on intertidal sediments that the depth profiles even in the upper milli-metre of sediments can vary from sharp surficial gradients with all the micro-algae concentrated at the surface to diffuser gradients in sediments evincingbioturbation or turbulence (see Wiltshire 2000)

Cell numbers

At both sites cell numbers showed a maximum in spring followed by a sum-mer decline and higher numbers again in autumn The spring maximum is


consistent with seasonality patterns investigated for different lake systems allover the world (Kann 1940 Round 1960 Khondker amp Dokulil 1988 No-zaki et al 2003) as nutrient and light availability are generally high at thistime of the year During summer water column nutrients become depleted andmacrophyte growth increases in the littoral zones and reduces light availabilityto a large extent Thus due to shading a decline of sediment microalgal abun-dances must be expected In Schoumlhsee the presence of large Alder populations(Alnus sp) contribute to the shading of the littoral zone Evidence for decreas-ing light intensities at the experimental sites in summer is also evinced in theincreased development of adjacent populations of Chara aspera which isknown to be highly adapted to low light regimes (Kann 1940 Blindow1992) In addition the decline in cell numbers during summer could be relatedto grazing Most benthic consumers show high abundances in summer andthus grazing losses often exceed microalgal production at this time of theyear The distinctive grazers present at the sites were the isopod Asellus aquat-icus and the snail Potamopyrgus antipodarum These findings are supportedby several studies showing that such summer depressions of microphytoben-thic biomass are directly related to high grazer efficiencies (Colijn amp Dij-kema 1981 Gaetje 1992)

When addressing general seasonality patterns for lake microphytobenthosone is confronted with large variations in nutrient and light conditions betweenlakes However given the similarities in seasonality observed in the SchoumlhseeLake Biwa (Nozaki et al 2003) in lakes from the English Lake District(Round 1960) and in several other northern German lakes (Kann 1940) wenow have further evidence that the occurrence and composition of freshwatermicrophytobenthic communities is generally controlled by the same major dri-vers such as seasonality Similar to planktonic systems in temperate watersthis includes a spring bloom of the microphytobenthos followed by a summerdecline and a second but reduced maximum in autumn

Cell numbers at both sites were highest in the uppermost surface layer anddecreased with increasing sediment depth as the light availability is higher atthe sediment surface and photosynthesis is restricted to a very thin layer at thesediment surface (Wasmund 1984 Carlton amp Wetzel 1987)

When comparing total chlorophyll-a contents and cell numbers no positivecorrelation was found Usually both parameters are used to describe biomasscharacteristics of algal communities and good correlations have been found(Khondker amp Dokuli 1988 Mitbavkar amp Anil 2002) However the totalchlorophyll-a content of algal communities is highly variable depending one g the physiological status of algal cells cell sizes and light intensities(Wolff 1979) and thus a correlation should not be assumed or even really ex-pected


Taxonomic composition and diversity

The microphytobenthos in general includes representatives of several algalclasses (Baccilariophyceae Chlorophyceae Cyanobacteria Dinophyceae) Onsandy and muddy substrates edaphic microalgae are often dominated by dia-toms (Round 1957 1960 Hickman amp Round 1970 Admiraal 1984 Colijnamp De Jonge 1984) whereas coccal and filamentous green algae and Cyano-bacteria are usually known to occur at some seasonal stages (Hillebrand ampKahlert 2001 Nozaki et al 2003)

The taxonomic composition of the sediment microflora in our study wasalmost exclusively restricted to diatom communities a feature that is mostlikely typical for mesotrophic lakes As already mentioned before mass occur-rences of green algae or cyanobacteria are known to be directly linked to highwater column nutrient loadings (Kann 1940 1993 Hillebrand amp Kahlert2001 Nozaki et al 2003) In unproductive lakes however diatom-dominatedsediment communities seem to be favoured as they are in general assumed asnot being limited by nutrients since nutrient concentrations in the sedimentpore water are high (Cadeacutee amp Hegemann 1974 Admiraal 1984 Under-wood amp Kromkamp 1999) and furthermore they are highly effective in ac-cessing nutrients at the sediment-water interface (Admiraal 1984 Sund-baeck et al 1991 Wiltshire 1993 Paterson et al 1998 Hillebrand ampKahlert 2002) These characteristics promote a higher competitiveness ofbenthic diatoms in unproductive lakes a feature that is supported by the factthat the occurrence of blue green algae is in general restricted to the springseason when enough nutrients from the water column are still available (Hil-lebrand amp Kahlert 2001 Nozaki et al 2003)

In addition to nutrient availability light conditions can regulate coloniza-tion patterns of microalgal communities As described by Kann (1940) ben-thic diatoms have a highly adaptive photosynthetic pigment apparatus and arewell adapted to low-light regimes Depending on the light intensity seasonalshifts in the xanthophyll cycle have been shown (Wiltshire et al 1997) andthus viability of diatoms at different light regimes is related to their adaptivepotential In contrast to chlorophyll-a these pigments have more efficientphotosynthetic yields and light absorption capacities and therefore they enablediatoms to grow at low-light conditions The two investigation sites of thisstudy were situated in the upper sublittoral zone with a north-easterly orienta-tion and they were characterized by large Alder-populations and vast Charaaspera-meadows Thus it seems likely that in our study diatoms were betteradapted to shading than other algal classes due to their high resilience to lowlight conditions (Kann 1940 Wiltshire et al 1997)

The diversity detected for Schoumlhsee sediments at both sites showed highvalues similar to the only comparable data from Neusiedlersee (Khondker amp


Dokulil 1988) Most of the dominant taxa were pennate prostrate formswhich were either epipsammic or epipelic Prostrate forms are typical for vari-able environments (mixed sediments) where disturbance predominantlythrough wave action or current plays an important role in structuring the algalcommunity On highly exposed substrates however algal communities havebeen found to be dominated by epipsammic forms (Wolff 1979) In contrastto epiphytic or epilithic communities unstable sediments are usually colo-nized by prostrate diatoms forming distinctly flat two-dimensional commu-nities (Miller et al 1987) The microphytobenthic communities of the Schoumlh-see thus indicate an intermediate degree of hydrographic exposure

In this study the two sites were colonized by similar seasonality patternsand algal communities A clear succession from spring to summer was ob-served The spring populations observed in the Schoumlhsee are similar to theones described for the Neusiedlersee (Khondker amp Dokuli 1988) and for theEnglish Lake District (Round 1960) The autumn community showed clearchanges in algal populations in contrast to Lake Mikolajskie (Wasmund 1984)and the Neusiedlersee (Khondker amp Dokuli 1988) where the autumn micro-flora was similar to the one in spring

However some typical forms like Cocconeis spp or Achnanthes spp of-ten found attached to sediment particles were missing at our sites In additiononly one erect form was present in considerable amounts throughout the sea-son and this was the genus Synedra This microalga has the ability to stick tosurfaces by forming mucilage pads and apparently this feature made it pos-sible for the algae to grow well even on unstable substrates Only two othererect forms were found periodically- the chain-forming diatoms Fragilariaspp and Melosira spp The vegetative cells of both diatoms occurred mainlyin spring at the sediment surfaces and as these taxa are known to have bentho-pelagic life cycles (Round et al 1990) it seems likely that they had settledfrom the water column and inhabited for a short time period the surface ofthe sediments

In conclusion it can be said that the microphytobenthos community of thismesotrophic lake was characterized by low algal biomass comprising almostexclusively of diatoms The two-dimensional structure was related to the ab-sence of overstory algae and a higher competitiveness and resilience of dia-toms to low productivity reduced light conditions and an intermediate degreeof exposure Distinct seasonality patterns as for lakes with similar conditionswere observed Similar abiotic conditions are common for a multitude of lakesystems in temperate regions and thus the characteristics observed within thisstudy can be regarded as typical features of mesotrophic lakes at higher latitu-des


Acknowledgements

We would like to thank Arne Malzahn for his help during the field sampling as wellas for valuable discussions on the manuscript Winfried Lampert is thanked for hissupport and for helpful ideas The comments of three anonymous reviewers helped usto improve the manuscript considerably We acknowledge the funding of this work bythe ldquoDeutsche Forschungsgemeinschaftrdquo (DFG-Foumlrderzeichen WI 18102-1)

References

Admiraal W (1984) The ecology of estuarine sediment inhabiting diatoms ndash ProgPhycol Res 3 269ndash322

Blanchard G F (1991) Measurement of meiofauna grazing rates on microphyto-benthos is primary production a limiting factor ndash J Exp Mar Biol Ecol 147 37ndash46

Blindow I (1992) Long- and short-term dynamics of submerged macrophytes in twoshallow eutrophic lakes ndash Freshwat Biol 28 15ndash27

Cadeacutee G C amp Hegeman J (1974) Primary production of the benthic microflora liv-ing on tidal flats in the Dutch Wadden Sea ndash Neth J Sea Res 8 260ndash291

Carlton R G amp Wetzel R G (1987) Distributions and fates of oxygen in peri-phyton communities ndash Can J Bot 65 1031ndash1037

Colijn F amp De Jonge V N (1984) Primary production of microphytobenthos in theEms-Dollard Estuary ndash Mar Ecol Prog Ser 14 185ndash196

Colijn F amp Dijkema K S (1981) Species composition of benthic diatoms and dis-tribution of chlorophyll a on an intertidal flat in the Dutch Wadden Sea ndash MarEcol Prog Ser 4 9ndash21

Cox E J (1993) Freshwater diatom ecology Developing an experimental approachas an aid to interpreting field data ndash Hydrobiologia 269ndash270 447ndash452

Cyr H (1998) How does the vertical distribution of chlorophyll vary in littoral sedi-ments of small lakes ndash Freshwat Biol 40 25ndash40

De Jonge V N amp Colijn F (1994) Dynamics of microphytobenthos biomass in theEms estuary ndash Mar Ecol Prog Ser 104 185ndash196

Gaetje C (1992) Artenzusammensetzung Biomasse und Primaumlrproduktion des Mik-rophytobenthos des Elbe-Aumlstuars ndash Ph D Thesis 211 pp Universitaumlt Hamburg

Gieskes W W C amp Kraay G W (1982) Comparison of chromatographic methods(HPLC and TLC) with conventional methods for the measurement of chlorophyllsin oceanic waters ndash Arch Hydrobiol Beih Ergebn Limnol 16 123

Grey J Kelly A amp Jones R J (2004) High intraspecific variability in carbon andnitrogen stable isotopes of lake chironomid larvae ndash Limnol Oceanogr 49 239ndash244

Hickman M amp Round F E (1970) Primary production and standing crops of epi-psammic and epipelic algae ndash Br Phycol J 5 247ndash255

Hillebrand H amp Kahlert M (2001) Effect of grazing and nutrient supply onperiphyton biomass and nutrient stoichiometry in habitats of different productiv-ity ndash Limnol Oceanogr 46 1881ndash1898

ndash ndash (2002) Effect of grazing and water column nutrient supply on biomass and nu-trient content of sediment microalgae ndash Aquat Bot 72 143ndash159


Hillebrand H Kahlert M Haglund A L Berninger U G Nagel S ampWickham S (2002) Control of microbenthic communities by grazing and nutri-ent supply ndash Ecology 83 2205ndash2219

Joslashrgensen B Revsbech N amp Cohen Y (1983) Photosynthesis and structure ofbenthic microbial mats Microelectrode and SEM studies of four cyanobacterialcommunities ndash Limnol Oceanogr 28 1075ndash1093

Kann E (1940) Oumlkologische Untersuchungen an Litoralalgen ostholsteinischer Seenndash Arch Hydrobiol 37 177ndash269

ndash (1993) The littoral algal biocoenoses of lake Erken and its outlet (Uppland Swe-den) ndash Arch Hydrobiol Suppl 97 Algol Stud 69 91ndash112

Khondker M amp Dokulil M (1988) Seasonality biomass and primary productivityof epipelic algae in a shallow lake (Neusiedlersee Austria) ndash Acta HydrochimHydrobiol 16 499ndash515

Lange-Bertalot H (1979) Tolerance and population dynamics of benthic diatomsunder varying waste water loading ndash Arch Hydrobiol 56 184ndash219

Lowe R (1996) Periphyton patterns in lakes ndash In Lowe R (ed) Algal EcologyFreshwater benthic ecosystems ndash Academic Press San Diego pp 57ndash76

MacIntyre H L Geider R J amp Miller D C (1996) Microphytobenthos Theecological role of the ldquosecret gardenrdquo of unvegetated shallow-water marine habi-tats 1 Distribution abundance and primary production ndash Estuaries 19 186ndash201

McCormick P V amp Stevenson R J (1991) Grazer control of nutrient availabilityin the periphyton ndash Oecologia 86 287ndash291

Miller A R Lowe R L amp Rotenberry J T (1987) Succession of diatom com-munities on sand grains ndash J Ecol 75 693ndash710

Mitbavkar S amp Anil A C (2002) Diatoms of the microphytobenthic communitypopulation structure in a tropical intertidal sand flat ndash Mar Biol 140 41ndash57

Montagna P A Blanchard G F amp Dinet A (1995) Effect of production andbiomass of intertidal microphytobenthos on meiofaunal grazing rates ndash J ExpMar Biol Ecol 185 149ndash165

Nozaki K Khadbaatar D Tetsuji A Naoshige G amp Osamu M (2003) De-velopment of filamentous green algae in the benthic algal community in a littoralsand-beach zone of Lake Biwa ndash Limnology 4 161ndash165

Paterson D M Wiltshire K H Miles A Blackburn J Davidson I YatesM G McGrorty S amp Eastwood J A (1998) Microbiological mediation ofspectral reflectance from intertidal cohesive sediments ndash Limnol Oceanogr 431207ndash1221

Pinckney J L amp Zingmark R G (1991) Effects of tidal stage and sun angles onintertidal benthic microalgal productivity ndash Mar Ecol Prog Ser 76 81ndash89

ndash ndash (1993) Modelling the annual production of intertidal benthic microalgae in es-tuarine ecosystems ndash J Phycol 29 396ndash407

Round F E (1957) Studies on the bottom living algae in some lakes of the EnglishLake District II the distribution of Bacillariophyceae on the sediments ndash J Ecol45 343ndash360

ndash (1960) Studies on the bottom living algae in some lakes of the English Lake Dis-trict IV the seasonal cycle of Bacillariophyceae ndash J Ecol 48 529ndash547

ndash (1971) Benthic marine diatoms ndash Oceanogr Mar Biol Ann Rev 9 83ndash139Round F E Crawford R M amp Mann D G (1990) The diatoms Biology and

morphology of the genera Cambridge University Press Cambridge (UK)


Schanz F amp Rai H (1988) Extract preparation and comparison of fluorometricchromatographic (HPLC) and spectrophotometric determinations of chlorophyll-andash Arch Hydrobiol 112 533ndash539

Shannon C amp Weaver W (1963) The Mathematical Theory of Communication ndashUniversity of Illinois Press Urbana

Stevenson R J Singer R Roberts D A amp Boylen C W (1985) Patterns ofbenthic algal abundance with depth trophic status and acidity in poorly bufferedNew Hampshire lakes ndash Can J Fish Aquat Sci 42 1501ndash1512

Sumner W T amp McIntire C D (1982) Grazer periphyton interactions in labora-tory streams ndash Arch Hydrobiol 93 135ndash157

Sundbaeck K Enoksson V Graneli W amp Pettersson K (1991) Influence ofsublittoral microphytobenthos on the oxygen and nutrient flux between sedimentand water A laboratory continuous-flow study ndash Mar Ecol Prog Ser 74 263ndash279

Sundbaeck K amp Joensson B (1988) Microphytobenthic productivity and biomassin sublittoral sediments of a stratified bay Southeastern Kattegat North Sea ndash JExp Mar Biol Ecol 122 63ndash82

Underwood G J C amp Kromkamp J (1999) Primary production by phytoplanktonand microphytobenthos in estuaries ndash Adv Ecol Res 29 93ndash153

Underwood G J C amp Paterson D M (1993) Recovery of intertidal benthic dia-toms after biocide treatment and associated sediment dynamics ndash J Mar Biol As-soc U K 73 25ndash45

Wasmund N (1984) Production and distribution of the microphytobenthos in thesediment of Lake Mikolajskie ndash Internat Rev ges Hydrobiol 69 215ndash229

ndash (1989) Micro-autoradiographic determination of the viability of algae inhabitingdeep sediment layers ndash Est Coast Shelf Sci 28 651ndash656

Wiltshire K H (1993) The influence of photosynthetic oxygen production by mi-crophytobenthos on the oxygen and nutrient status of sediment water systems inthe Elbe estuary ndash Verh Internat Verein Limnol 25 1141ndash1146

ndash (2000) Algae and associated pigments of intertidal sediments new observationsand methods ndash Limnologica 30 205ndash214

Wiltshire K H Blackburn J amp Paterson D M (1997) The Cryolander A newmethod for fine-scale in-situ sampling of intertidal surface sediments ndash J SedRes 67 977ndash981

Wiltshire K H Schroeder F Knauth H-D amp Kausch H (1996) Oxygenconsumption and production rates and associated fluxes in sediment-water sys-tems A combination of microelectrode incubation and modelling techniques ndashArch Hydrobiol 137 457ndash486

Wolff W J (1979) Flora and Vegetation of the Wadden Sea ndash Report 3 (Final Reportof the Section Marine Biology of the Wadden Sea) Balkema A A Rotterdam(Netherlands) pp206

Submitted 28 May 2005 accepted 26 January 2006


Introduction

Sediment microflora comprises of microscopic photosynthetic eukaryotic al-gae and cyanobacteria that live on or within the sediment These microorgan-isms are restricted to the surface layers of sediments due to the depth penetra-tion of light (MacIntyre et al 1996) and they therefore play an importantrole for nutrient and oxygen fluxes at the sediment water interface (Joslashrgen-sen et al 1983 Wiltshire et al 1996) Their occurrence is governed by envi-ronmental parameters making them sensitive indicators of water quality (Lan-ge-Bertalot 1979) and their key function as primary producers and as a foodsource in littoral zones has been emphasized in many studies (Colijn amp DeJonge 1984 McCormick amp Stevenson 1991 Pinckney amp Zingmark 1993Hillebrand et al 2002)

Although the diversity and functional role of microphytobenthic commu-nities has become a major topic in marine benthic research over the last twodecades (Sundbaeck amp Joensson 1988 Blanchard 1991 Montagna et al1995) its potential importance in the littoral zones of freshwater lakes has re-ceived little attention Consequently not much is known about the composi-tion fluctuation and seasonal occurrence of the sediment microflora in fresh-water habitats (Lowe 1996) Most studies carried out in freshwater benthicsystems focused on epilithic or epiphytic algae growing on solid substrates(Sumner amp McIntire 1982 McCormick amp Stevenson 1991 Kann 1993Cox 1993 Lowe 1996 Hillebrand amp Kahlert 2001) In contrast studies onepipelic algae (algae moving actively through the sediments by means of theirraphes Round 1971) or epipsammon communities (algae growing attached tosediment particles Round 1971) are rare (Round 1957 Hickman amp Round1970 Miller et al 1987 Khondker amp Dokulil 1988 Cyr 1998 Nozaki etal 2003) This is the case even though soft sediments often represent the mainsubstrate in shallow lakes and epipelic or epipsammic algae can reach highbiomass and productivity (Khondker amp Dokulil 1988 Cyr 1998)

To increase our understanding of the specific composition of microphyto-benthic communities in temperate regions a survey was conducted in Schoumlh-see (Ploumln Germany) in the summer of 2001 With respect to planktonic param-eters the Schoumlhsee is well-studied but until this study the benthos had re-ceived little attention This study was aimed at providing first baseline infor-mation on the abundance diversity and seasonal variations of benthic micro-algae in the Schoumlhsee Both sandy and muddy sediments were examined toevaluate potential differences in community structure and seasonal variationsof these poorly understood limnic microalgal communities We aimed at non-destructive sampling allowing high resolution (microm) vertical profiling in orderto determine the potential microalgal stratification in the sediments (see Wilt-shire 2000)



Sampling sites




screw cap

plastic tube

gauze (500microm)

sediment

25 mm

14 mm

screw cap

plastic tube

gauze (500microm)

sediment

25 mm

14 mm




Sample preservation


Sample processing







Results









Fig

2C

hlor

ophy

ll-a

conc

entr

atio

nsin

microgcm

ndash2

(A)

and

tota

lal

gal

cell

num

bers

ince

llscm

ndash2

(B)

ofth

em

icro

alga

lco

mm

unity

onsu

rfac

e(0

ndash25

0microm

)an

dde

ep(2

50ndash

500

microm)

laye

rsof

mud

and

ofsa

ndin

the

Schouml

hsee

sam

pled

from

May

Jun

eto

Oct

ober

2001

Err

orba

rssh

owth

est

anda

rdde

viat

ions







Total cell numbers

















Fig

4T

axon

omic

com

posi

tion

ofal

gal

com

mun

ities

onm

ud(A

)an

don

sand

(B)

inth

eSc

houmlhs

eesa

mpl

edfr

omM

ayto

Oct

ober

2001

All

taxa

give

nas

spec

ies

plur

al(s

pp)

asal

lge

nus

whe

rere

pres

ente

dby

seve

ral

spec

ies

Rel

ativ

eab

unda

nce

ofdi

ffer

ent

taxo

nom

icgr

oups

isca

lcul

ated

as

ofth

eto

tal

alga

lce

llsT

otal

cell

num

bers

(cel

lscm

ndash2 )

are

give

nas

the

sum

from

surf

ace

and

deep

sedi

men

tla

yers

and

are

illus

trat

edas

alin

e



Diversity


Discussion














Cell numbers



















Acknowledgements


References

























































Sampling sites




screw cap

plastic tube

gauze (500microm)

sediment

25 mm

14 mm

screw cap

plastic tube

gauze (500microm)

sediment

25 mm

14 mm




Sample preservation


Sample processing







Results









Fig

2C

hlor

ophy

ll-a

conc

entr

atio

nsin

microgcm

ndash2

(A)

and

tota

lal

gal

cell

num

bers

ince

llscm

ndash2

(B)

ofth

em

icro

alga

lco

mm

unity

onsu

rfac

e(0

ndash25

0microm

)an

dde

ep(2

50ndash

500

microm)

laye

rsof

mud

and

ofsa

ndin

the

Schouml

hsee

sam

pled

from

May

Jun

eto

Oct

ober

2001

Err

orba

rssh

owth

est

anda

rdde

viat

ions







Total cell numbers

















Fig

4T

axon

omic

com

posi

tion

ofal

gal

com

mun

ities

onm

ud(A

)an

don

sand

(B)

inth

eSc

houmlhs

eesa

mpl

edfr

omM

ayto

Oct

ober

2001

All

taxa

give

nas

spec

ies

plur

al(s

pp)

asal

lge

nus

whe

rere

pres

ente

dby

seve

ral

spec

ies

Rel

ativ

eab

unda

nce

ofdi

ffer

ent

taxo

nom

icgr

oups

isca

lcul

ated

as

ofth

eto

tal

alga

lce

llsT

otal

cell

num

bers

(cel

lscm

ndash2 )

are

give

nas

the

sum

from

surf

ace

and

deep

sedi

men

tla

yers

and

are

illus

trat

edas

alin

e



Diversity


Discussion














Cell numbers



















Acknowledgements


References

























































Sample preservation


Sample processing







Results









Fig

2C

hlor

ophy

ll-a

conc

entr

atio

nsin

microgcm

ndash2

(A)

and

tota

lal

gal

cell

num

bers

ince

llscm

ndash2

(B)

ofth

em

icro

alga

lco

mm

unity

onsu

rfac

e(0

ndash25

0microm

)an

dde

ep(2

50ndash

500

microm)

laye

rsof

mud

and

ofsa

ndin

the

Schouml

hsee

sam

pled

from

May

Jun

eto

Oct

ober

2001

Err

orba

rssh

owth

est

anda

rdde

viat

ions







Total cell numbers

















Fig

4T

axon

omic

com

posi

tion

ofal

gal

com

mun

ities

onm

ud(A

)an

don

sand

(B)

inth

eSc

houmlhs

eesa

mpl

edfr

omM

ayto

Oct

ober

2001

All

taxa

give

nas

spec

ies

plur

al(s

pp)

asal

lge

nus

whe

rere

pres

ente

dby

seve

ral

spec

ies

Rel

ativ

eab

unda

nce

ofdi

ffer

ent

taxo

nom

icgr

oups

isca

lcul

ated

as

ofth

eto

tal

alga

lce

llsT

otal

cell

num

bers

(cel

lscm

ndash2 )

are

give

nas

the

sum

from

surf

ace

and

deep

sedi

men

tla

yers

and

are

illus

trat

edas

alin

e



Diversity


Discussion














Cell numbers



















Acknowledgements


References



























































Results









Fig

2C

hlor

ophy

ll-a

conc

entr

atio

nsin

microgcm

ndash2

(A)

and

tota

lal

gal

cell

num

bers

ince

llscm

ndash2

(B)

ofth

em

icro

alga

lco

mm

unity

onsu

rfac

e(0

ndash25

0microm

)an

dde

ep(2

50ndash

500

microm)

laye

rsof

mud

and

ofsa

ndin

the

Schouml

hsee

sam

pled

from

May

Jun

eto

Oct

ober

2001

Err

orba

rssh

owth

est

anda

rdde

viat

ions







Total cell numbers

















Fig

4T

axon

omic

com

posi

tion

ofal

gal

com

mun

ities

onm

ud(A

)an

don

sand

(B)

inth

eSc

houmlhs

eesa

mpl

edfr

omM

ayto

Oct

ober

2001

All

taxa

give

nas

spec

ies

plur

al(s

pp)

asal

lge

nus

whe

rere

pres

ente

dby

seve

ral

spec

ies

Rel

ativ

eab

unda

nce

ofdi

ffer

ent

taxo

nom

icgr

oups

isca

lcul

ated

as

ofth

eto

tal

alga

lce

llsT

otal

cell

num

bers

(cel

lscm

ndash2 )

are

give

nas

the

sum

from

surf

ace

and

deep

sedi

men

tla

yers

and

are

illus

trat

edas

alin

e



Diversity


Discussion














Cell numbers



















Acknowledgements


References
























































Fig

2C

hlor

ophy

ll-a

conc

entr

atio

nsin

microgcm

ndash2

(A)

and

tota

lal

gal

cell

num

bers

ince

llscm

ndash2

(B)

ofth

em

icro

alga

lco

mm

unity

onsu

rfac

e(0

ndash25

0microm

)an

dde

ep(2

50ndash

500

microm)

laye

rsof

mud

and

ofsa

ndin

the

Schouml

hsee

sam

pled

from

May

Jun

eto

Oct

ober

2001

Err

orba

rssh

owth

est

anda

rdde

viat

ions







Total cell numbers

















Fig

4T

axon

omic

com

posi

tion

ofal

gal

com

mun

ities

onm

ud(A

)an

don

sand

(B)

inth

eSc

houmlhs

eesa

mpl

edfr

omM

ayto

Oct

ober

2001

All

taxa

give

nas

spec

ies

plur

al(s

pp)

asal

lge

nus

whe

rere

pres

ente

dby

seve

ral

spec

ies

Rel

ativ

eab

unda

nce

ofdi

ffer

ent

taxo

nom

icgr

oups

isca

lcul

ated

as

ofth

eto

tal

alga

lce

llsT

otal

cell

num

bers

(cel

lscm

ndash2 )

are

give

nas

the

sum

from

surf

ace

and

deep

sedi

men

tla

yers

and

are

illus

trat

edas

alin

e



Diversity


Discussion














Cell numbers



















Acknowledgements


References





























































Total cell numbers

















Fig

4T

axon

omic

com

posi

tion

ofal

gal

com

mun

ities

onm

ud(A

)an

don

sand

(B)

inth

eSc

houmlhs

eesa

mpl

edfr

omM

ayto

Oct

ober

2001

All

taxa

give

nas

spec

ies

plur

al(s

pp)

asal

lge

nus

whe

rere

pres

ente

dby

seve

ral

spec

ies

Rel

ativ

eab

unda

nce

ofdi

ffer

ent

taxo

nom

icgr

oups

isca

lcul

ated

as

ofth

eto

tal

alga

lce

llsT

otal

cell

num

bers

(cel

lscm

ndash2 )

are

give

nas

the

sum

from

surf

ace

and

deep

sedi

men

tla

yers

and

are

illus

trat

edas

alin

e



Diversity


Discussion














Cell numbers



















Acknowledgements


References





































































Fig

4T

axon

omic

com

posi

tion

ofal

gal

com

mun

ities

onm

ud(A

)an

don

sand

(B)

inth

eSc

houmlhs

eesa

mpl

edfr

omM

ayto

Oct

ober

2001

All

taxa

give

nas

spec

ies

plur

al(s

pp)

asal

lge

nus

whe

rere

pres

ente

dby

seve

ral

spec

ies

Rel

ativ

eab

unda

nce

ofdi

ffer

ent

taxo

nom

icgr

oups

isca

lcul

ated

as

ofth

eto

tal

alga

lce

llsT

otal

cell

num

bers

(cel

lscm

ndash2 )

are

give

nas

the

sum

from

surf

ace

and

deep

sedi

men

tla

yers

and

are

illus

trat

edas

alin

e



Diversity


Discussion














Cell numbers



















Acknowledgements


References

























































Diversity


Discussion














Cell numbers



















Acknowledgements


References


































































Cell numbers



















Acknowledgements


References








































































Acknowledgements


References























































Seasonality and diversity patterns of microphytobenthos in ... · Seasonality and diversity...

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Transcript of Seasonality and diversity patterns of microphytobenthos in ... · Seasonality and diversity...