research article plankton resting stages in the marine...

Hindawi Publishing CorporationInternational Journal of EcologyVolume 2013 Article ID 101682 12 pageshttpdxdoiorg1011552013101682

Research ArticlePlankton Resting Stages in the Marine Sediments ofthe Bay of Vloreuml (Albania)

Fernando Rubino1 Salvatore Moscatello2 Manuela Belmonte12

Gianmarco Ingrosso2 and Genuario Belmonte2

1 Laboratory of Plankton Ecology IAMC CNR UOS Talassografico ldquoA Cerrutirdquo 74123 Taranto Italy2 Laboratory of Zoogeography and Fauna CoNISMa UO Lecce DiSTeBA University of the Salento 73100 Lecce Italy

Correspondence should be addressed to Genuario Belmonte genuariobelmonteunisalentoit

Received 13 December 2012 Accepted 1 April 2013

Academic Editor Sami Souissi

Copyright copy 2013 Fernando Rubino et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

In the frame of the INTERREG III CISM project sediment cores were collected at 2 stations in the Gulf of Vlore to study theplankton resting stage assemblages A total of 87morphotypeswere identified andproduced byDinophyta Ciliophora Rotifera andCrustacea In 22 cases the cyst belonged to a species absent from the plankton of the same periodThemost abundant resting stageswere those produced by Scrippsiella species (Dinophyta) Some calcareous cysts were identified as fossil species associated withPleistocene to Pliocene sediment although they were also found in surface sediments and some of them successfully germinatedthus proving their modern status Total abundance generally decreased with sediment depth at station 40 while station 45 showeddistinct maxima at 3 and 8 cm below the sediment surface The depth of peak abundance in the sediment varied with species Thispaper presents the first study of the plankton resting stages in the Bay of Vlore The study confirmed the utility of this type ofinvestigation for a more correct evaluation of species diversity In addition the varying distribution with sediment depth suggeststhat this field could be of some importance in determining the history of species assemblages

1 Introduction

Resting stages produced by plankton organisms in temper-ate seas accumulate in the bottom sediments of confinedcoastal areas [1] Their assemblages represent reservoirs ofbiodiversity which sustain the high resilience of planktoncommunities providing recruits of propagules at each returnof favourable conditions in accordance with the so-calledSupply Vertical Ecology model [2] The existence of benthicstages in the life cycles of holoplankton provides a new keyfor understanding the role of life cycles in the pelagic-benthicrelationship in coastal waters [3 4] Consequently assess-ments of biodiversity at marine sites should take accountof the unexpressed fraction of the plankton communitycontained in the bottom sediments by performing integratedsampling programs [5 6] Despite the proven importanceof resting stage banks in coastal marine ecology the issueof ldquoresting versus activerdquo plankters has commonly been

considered for single taxa and only rarely from the whole-community point of view This is probably due to the greatcomplexity (compositional functional and distributional) ofresting stage banks Indeed it has been demonstrated thatat any given moment the species assemblages in bottomsediments (as resting stages) are quite different from thespecies detectable in the water column (as active stages)[6 7] However the study of such marine ldquoseed banksrdquo (asunderstood by [3] analogous to terrestrial seed banks inforest soils) is complex on many levels Resting stages share acommonmorphological plan despite belonging to organismsfrom different kingdoms [8] Consequently resting stagemorphology differs sharply from that of active stages andin some cases their identification is highly problematicHowever it is also true that for some naked dinoflagellatesor for thecate ones with a similar thecal plate pattern cystsare quite different allowing correct identification withoutthe use of SEM or molecular techniques Cyst-producing

2 International Journal of Ecology

dinoflagellates differ in the length of their life cycle andorthe timing of cyst production and the rest capacity of restingstages also varies They are generally programmed to rest forthe duration of the adverse period but fractions of themcan also rest for longer periods allowing the population toreappear decades later ([9ndash11] for copepods [12 13] fordinoflagellates) Hairston et al [14] reported a rest of morethan 300 years for a calanoid resting egg albeit of a freshwaterspecies

The scarcity of literature on whole resting stage commu-nities encouraged us to describe situations in various parts ofthe Mediterranean in order to obtain a rich data set usefulfor building models and in experimental situations Herea detailed description of the structure of the marine ldquoseedbankrdquo produced by plankton in the Bay of Vlore is reported

The present study also focuses on an Albanian bay thathas not been extensively studied from themarine biodiversitypoint of view The data from the benthos are comparedwith analyses of the phytoplankton and microzooplankton[15] in the water column to assess with more precision thebiodiversity of the plankton in the Bay of Vlore

Moscatello et al [15] reported that the microzooplanktoncommunity of the Bay of Vlore was composed of more than200 taxa of which 97 were classified as ldquoseasonally absentrdquoThe aim of the present paper is to determine whether theseabsences in the water column correspond to resting stages inthe sediments

2 Materials and Methods

21 Study Site An oceanographic campaign was carried outin the Bay of Vlore from 17th to 23rd of January 2008 aboardthe oceanographic vessel ldquoUniversitatisrdquo This survey wasconducted as part of the PIC Interreg III Italy Albania Projectfor providing technical assistance for the management of anInternational Centre of Marine Sciences (CISM) in AlbaniaThe sampling period of the present study (January 2008)coincided with that of Moscatello et al [15] who investigatedactive plankton in the water column in the same area

In order to investigate the presence and distribution ofresting stages produced by plankton species in the area2 stations were chosen representing 2 different types ofenvironment a deep zone (station 40 depth 54m) withsediments of terrigenous mud dominated by Labidoplaxdigitata (Holothuroidea) and a shallower site (station 45depth 28m) with sediments of terrigenous mud dominatedby Turritella communis (Gastropoda) (Figure 1) (for theclassification of mud biocenosis in the Bay of Vlore see [16])

22 Sampling Procedure Samples of bottom sediments werecollected in three replicates (named 40 a b c and 45 a b c)using a Van Veen grab with upper windows that allowed thecollection of undisturbed sediment cores At each station 2different PVC corers (h 30 cm inner w 4 and 8 cm) wereused in order to obtain 2 different sets of samples Thesmaller core was processed to obtain cysts of protists thelarger core was processed to obtain resting eggs ofmetazoansThis differentiation was necessary because metazoan resting

N

Radhime

Vlore

Zvernec

Sazan isleNa

Orikum

45

40

NNNNNNaaaaaaaaaaaaaaaaaaaaaaaaaaNNNaaaaaaaaaaaaaaaNNaaaaaaaaaaNaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaa

Karaburun peninsula

40∘25

998400N

40∘20

998400N

19∘25

998400E19∘20

998400E

Figure 1 Map of study area showing location of two samplingstations (40 45) in Bay of Vlore (Albania)

stages are less abundant so a greater amount of sediment isrequired Moreover their walls are only organic allowing theadoption of a centrifugation method coupled with filtrationto obtain a ldquocleanrdquo sample from a relatively large quantity ofsediment In contrast protistan cysts are more abundant andhave different types of walls (calcareous siliceous organic)which complicates the procedure when the whole cyst bankis studied Thus the most fruitful method of separating cystsfrom sediment is filtration through meshes of different sizes

After extraction sediment cores were immediately sub-divided into 1 cm thick layers until the 15th cm from thesediment surface The thickness of 15 cm was chosen becausein previous studies we noted that abundances diminishedsignificantly at depths of more than 7ndash10 cm below thesediment surface [1 12] The outer edge of each layer wasdiscarded to avoid contamination from material from theoverlaying layer during the insertion of the corer into thesediments Once obtained the samples were stored in thedark at 5∘C until treatment in the laboratory

23 Protistan Cysts (20ndash125 120583m) In the laboratory the small-core samples were treated using a sieving technique consist-ing of the following steps

(i) The entire sample is homogenized and then sub-sampled obtaining 3ndash5mL of wet sediment which ispassed through a 20120583m mesh (Endecottrsquos LTD steelsieves ISO3310-1 London England) using naturalfiltered (045 120583m) seawater (Gulf of Taranto)

(ii) The retained fraction is ultrasonified for 1min andagain passed through a series of sieves (125 75 and20120583m mesh sizes) obtaining a fine-grained fraction(20ndash75120583m) containing most of the protistan cysts

International Journal of Ecology 3

and a 75ndash125120583m fraction with the larger ones (egLingulodinium spp) and the zooplankton restingeggs The material retained by the 125 120583m mesh wasnot considered

No chemicals were used to disaggregate sediment par-ticles in order to avoid the dissolution of calcareous andsiliceous cyst walls

Qualitative and quantitative analyses were carried outunder an inverted microscope (Zeiss Axiovert S100 equippedwith a Nikon Coolpix 990 digital camera) at 200 and 320magnifications Both full (ie probably viable) and empty(ie probably germinated) cysts were considered At least15 of the finer fraction and all of the gt75120583m fraction wereanalyzed

All the resting stage morphotypes were identified on thebasis of published descriptions ([17ndash19] for dinoflagellates[20 21] for ciliates and germination experiments)

Identification was performed to the lowest possible taxo-nomic level As a rule modern biological names were usedThe paleontological name is reported only for morphotypeswhose active stage was not known

A fixed aliquot (asymp5 g) of wet sediment from each samplewas oven-dried at 70∘C for 24 h to calculate the water contentand obtain quantitative data for each taxon as cysts gminus1 of drysediment

24 Metazoan Resting Eggs (45ndash200 120583m) For the analysisof the large-core samples the Onbe [22] method was usedslightlymodified by using 45 and 200120583mmesh sizes to obtaina size range typical of mesozooplankton resting eggs

For each sample a fixed quantity of wet sediment wastreated (asymp45 cm3)

Only full (ie probably viable) resting eggs were countedand quantitative data for each taxon are reported as restingeggs times 100 gminus1 of dry sediment

25 Germination Experiments To achieve germination allputative viable cysts of protists isolated from the sedimentwere individually positioned in Nunclon microwells (NalgeNunc International Roskilde Denmark) containing asymp1mLof natural sterilized seawater Cysts were incubated at 20∘C12 12 h LD cycle 100 120583E mminus2 secminus1 irradiance and examinedon a daily basis until germination up to a maximum of 30days The incubation conditions were chosen on the basis ofprevious studies [5 6 23] They have proved to be effectivefor a large number of species

26 Data Analysis For the 1st cm of the cores data on restingstage abundance from the 2 sampling stations were obtainedby merging the data from the 3 replicates of the 2 sets ofsamples (those for protistan cysts andmetazoan resting eggs)For samples below the first cm only the 45ndash200120583m fractionwas used in order to facilitate and accelerate the analysisFrom the abundance matrices (taxa versus stations and taxaversus station and cm respectively) of both surface and deepersediments the Bray Curtis similarity measure was calculated

after 4th root transformation in order to allow rare species tobecome more evident

The PRIMER ldquoDIVERSErdquo function (Primer-E Ltd Ply-mouth UK) was used to calculate the taxonomic richness (S)taxon abundance (N) Margalef index (d) Shannon-Wienerdiversity index (1198671015840) and Pieloursquos evenness index (1198691015840) for eachsample

The relationships between the samples collected at the2 stations were analyzed by means of nonmetric multidi-mensional scaling (nMDS) with superimposed hierarchicalclustering with a cutoff at 60 similarity (for surface sedi-ments) and 70 (for the sediment core as a whole) whilethe SIMPER routinewas used to identify relative dissimilarityand the taxa that contributed most to the differences

The statistical significance of the differences between the2 stations was calculated by means of a 2-way crossed anal-ysis of similarities (ANOSIM) on the Bray-Curtis similaritymatrix based on the stratigraphy

All univariate and multivariate analyses were performedusing PRIMER v6 (Primer-E Ltd Plymouth UK)

3 Results

31 Total Biodiversity Resting stages were found at all levelsof the 15 cm sediment core columns from the 2 investigatedsites in the Gulf of Vlore

Merging the data from the 2 sets of samples (20ndash125120583mand 45ndash200120583m) and considering both full (probably viable)and empty (probably germinated) forms from each station87 different resting stage morphotypes produced by planktonwere recognized (Table 1) Most of them (59 belonging to20 genera) were dinoflagellates 16 were ciliates (9 genera) 4rotifers (2 genera) and 5 crustaceans (4 genera) while 3 (1protistan cyst type and 2 resting eggs) remained unidentifiedStation 40 showed higher biodiversity with 79 morphotypes35 of them exclusive to the site At station 45 52morphotypeswere observed 8 of them being exclusive

Moreover analysis of the empty forms found among the20ndash125120583m fraction led to the recognition of 11 morphotypesall dinoflagellates

A total of 36 cyst types were identified as taxa missingfrom the plankton list of the same period (January 2008[15]) Partly due to nomenclature problems uncertaintyof identification and differences in examined periods itwas possible to ascertain the contemporaneous presence ofspecies in both pelagic and benthic compartments only in avery few cases

Identification was frequently impossible due to the pres-ence of previously unreported resting stage morphologies Insuch cases germination experiments allowed the cysts to beattributed to a high level taxon at least as with a Strombidium(Ciliophora) cyst whose morphology is reported here for thefirst time (see Figure 2)

32 Surface Sediments Theanalysis of surface sediments (the1st cm of the cores) that is those most affected by cystdeposition and resuspensiongermination revealed sharpdifferences between the 2 analysed stations In total 36


Table 1 List of resting stage (cyst) morphotypes recovered from sediments of Bay of Vlore (Albania)

Taxon St40 St45Dinoflagellates

Alexandrium minutumHalim e e I

Alexandrium tamarense (Lebour) Balech e

Alexandrium sp 1 e

Alexandrium sp 2 e

Bicarinellum tricarinelloides Versteegh e I e

Calcicarpinum perfectum Versteegh I

Calciodinellum albatrosianum (Kamptner) Janofske and Karwath e I e I

Calciodinellum operosum (Deflandre) Montresor e I I

Calciperidinium asymmetricum Versteegh I

Cochlodinium polykrikoidesMargalef type 1 e

Cochlodinium polykrikoidesMargalef type 2 I

Diplopelta parva (Abe) Matsuoka I

Diplopsalis lenticula Bergh e I

Follisdinellum splendidum Versteegh I

Gonyaulax group e I e I

Gymnodinium impudicum (Fraga and Bravo) G Hansen and Moestrup e

Gymnodinium nolleri Ellegaard and Moestrup e

Gymnodinium sp 1 e I e

Lingulodinium polyedrum (Stein) Dodge e I e I

Melodomuncula berlinensis Versteegh e I e

Nematodinium armatum (Dogiel) Kofoid and Swezy e I

Oblea rotunda (Lebour) Balech ex Sournia e e

Pentapharsodinium dalei Indelicato and Loeblich type 1 e I e

Pentapharsodinium dalei Indelicato and Loeblich type 2 e e

Pentapharsodinium tyrrhenicumMontresor Zingone and Marino type 1 e I e I

Pentapharsodinium tyrrhenicumMontresor Zingone and Marino type 2 I

Polykrikos kofoidii Chatton I

Polykrikos schwartzii Butschli I

Protoperidinium compressum (Abe) Balech I

Protoperidinium conicum (Gran) Balech e I

Protoperidinium oblongum (Aurivillius) Parke and Dodge e

Protoperidinium parthenopes Zingone and Montresor e

Protoperidinium steidingerae Balech e

Protoperidinium subinerme (Paulsen) Loeblich III I

Protoperidinium thorianum (Paulsen) Balech e I I

Protoperidinium sp 1 e I I

Protoperidinium sp 5 e I

Protoperidinium sp 6 e

Pyrophacus horologium Stein e e

Scrippsiella cf crystallina Lewis I

Scrippsiella lachrymosa Lewis e I e I

Scrippsiella ramoniiMontresor e I I

Scrippsiella trochoidea (Stein) Loeblich rough type e e

Scrippsiella trochoidea (Stein) Loeblich smooth type e e I

Scrippsiella trochoidea (Stein) Loeblich large type e I e


Table 1 Continued

Taxon St40 St45Scrippsiella trochoidea (Stein) Loeblich medium type e I e I

Scrippsiella trochoidea (Stein) Loeblich small type e I e

Scrippsiella sp 1 e I e I

Scrippsiella sp 4 e e



Scrippsiella sp 8 e I e

Thoracosphaera sp e e

Dinophyta sp 2 e e

Dinophyta sp 7 e e

Dinophyta sp 17 e

Dinophyta sp 26 e

Dinophyta sp 30 e

Dinophyta sp 33 e e

CiliatesCodonella aspera Kofoid and Campbell e

Codonella orthocerasHeackel e

Codonellopsis monacensis (Rampi) Balech e

Codonellopsis schabii (Brandt) Kofoid and Campbell e e

Epiplocylis undella (Ostenfeld and Schmidt) Jorgensen e e

Rabdonella spiralis (Fol) Brandt e

Stenosemella ventricosa (Claparede and Lachmann) Jorgensen e e

Strobilidium sp e e

Strombidium cf acutum (Leegaard) Kahl e e

Strombidium conicum (Lohman) Wulff I e

Tintinnopsis beroidea Stein e

Tintinnopsis butschlii Kofoid and Campbell e

Tintinnopsis campanula Ehrenberg e

Tintinnopsis cylindrica Daday e e

Tintinnopsis radix (Imhof) e

Undella claparedei (Entz) Daday e

RotifersBrachionus plicatilisMuller e

Synchaeta sp spiny type e I

Synchaeta sp rough type e

Synchaeta sp mucous type e

Crustaceans CladoceransPenilia avirostris Dana e e

Crustaceans CopepodsAcartia clausimargalefi e

Acartia sp 1 e I e I

Centropages sp e e I

Paracartia latisetosa (Krizcaguin) e I e

UnidentifiedCyst type 1 e

Resting Egg 1 e

Resting Egg 9 e

e cysts observed as full (ie probably viable) I cysts observed as germinated (ie empty)


(a)

(c)

(b)

Figure 2 Photographs of Ciliophora cyst with two oppositepapulae (a) Its empty shell (hatch occurs from one of two papulae)(b) Germinated active stage Strombidium ciliate (c)

different resting stagemorphotypeswere observed in this firstlayer (Table 2) 23 produced by dinoflagellates 6 by ciliates2 by rotifers 4 by crustaceans and 1 undetermined Evenconsidering the small amount of available data station 40showed higher biodiversity in terms of both number of taxaand diversity indexes (see Table 3) Total abundances werecomparable however with 389plusmn127 cysts gminus1 (average plusmn sd)at station 40 versus 329 plusmn 123 cysts gminus1 at station 45 SIMPERshowed 58 dissimilarity between the assemblages of the twosites (Table 4)

The most abundant cyst morphotypes in the surfacelayers were calcareous cysts produced by species of theCalciodinellaceae family (Dinophyta) At station 40 fivecyst morphotypes of this family accounted for 95 of totalabundance while at station 45 99was accounted for by justone cyst morphotype Scrippsiella trochoidea medium typeconfirming the lower evenness at this station

The nMDS ordination (Figure 3 stress = 0) with thehierarchical cluster superimposed with a cutoff at 60 simi-larity clearly reflects the separation between the samples fromstations 40 and 45 Among these due to its higher diversitysample 45b is farther from samples 45a and 45c than it is fromthe samples of station 40

33 Whole Sediment Cores At both the investigated stationsa general decrease in total abundances was observed withdepth along the sediment columns At station 40 higher totalabundance and diversity values than station 45 were regis-tered (Figure 4) with a sharp decline between the 6th and 7thcentimetres Beyond this depth total abundance remainedbelow 100 cysts 100 gminus1 In terms of species Codonellopsis

Transform fourth rootResemblance S17 Bray-Curtis similarity

40a

40b

40c

45a

45b

45c

Stress 0

Figure 3 nMDS plot of surface sediment samples collected atstations 40 and 45 in Bay of Vlore Hierarchical clustering super-imposed with cutoff at 60 similarity

schabii cysts and Synchaeta sp and Acartia clausimargalefiresting eggs were continuously observed along the wholesediment column at both stations The ciliate C schabii wasby far the most abundant taxon at station 40 (43 of totalabundance) with density highest in the 2nd cm (342 plusmn 192cysts 100 gminus1) as with total abundance a sharp decreasewas observed between the 6th and 7th centimetres Otherimportant species were the copepods Centropages sp (181 plusmn50 resting eggs 100 gminus1 at 4th cm) and Acartia spp (67 plusmn32 resting eggs 100 gminus1 at 1st cm) At station 45 the mostabundant type was Acartia spp (86 plusmn 57 resting eggs 100 gminus1at 1st cm) followed by C schabii (70 plusmn 60 cysts 100 gminus1 at 4thcm) and Synchaeta sp (41plusmn23 resting eggs 100 gminus1 at 5th cm)

In the nMDS ordination (Figure 5 stress = 012) withsuperimposition of the hierarchical cluster with a cutoffat 70 similarity all the samples from station 45 clustertogether while the samples from station 40 were widelydispersed a sign of greater variability at this site

The assemblage structure of the two stations differedsignificantly at all layers (ANOSIM 119877 = 0655 119875 = 0001)showing 59 dissimilarity (SIMPER Table 5)

34 Germination Experiments All putatively viable (ie full)protistan cyst types observed were isolated and incubatedunder controlled conditions to obtain germination Suc-cessful germination generally allowed us to confirm thecyst-based identification but in some cases it enabled usto go beyond this and discriminate between cysts sharingsimilar morphology For example Alexandrium minutumand Scrippsiella sp 1 both have a round cyst with a thin andsmooth wall withmucousmaterial attached Protoperidiniumthorianum and Protoperidinium sp 1 cysts are both round-brown and smooth andGymnodiniumnolleri and Scrippsiellasp 4 both produce round-brown cysts with a red spot insideThe germination of all these cyst types allowed us to correctlyidentify these species


Table 2 Abundance (cysts gminus1 dw) of probably viable resting stages (cysts) observed in surface sediments of two stations in Bay of Vlore(Albania) Values from three replicates are reported

40a 40b 40c 45a 45b 45c

Calciodinellum albatrosianum 201 183 351 00 00 00Calciodinellum operosum 00 00 117 00 00 00Gonyaulax group 201 00 00 00 00 596Gymnodinium sp 1 201 92 00 00 222 00Lingulodinium polyedrum 402 00 00 00 00 00Melodomuncula berlinensis 402 00 00 00 00 00Oblea rotunda 00 00 117 00 00 00Pentapharsodinium dalei type 1 201 00 00 00 111 00Pentapharsodinium tyrrhenicum type 1 402 183 234 00 111 00Protoperidinium sp 1 00 92 00 00 00 00Protoperidinium sp 5 00 00 117 00 111 00Scrippsiella ramonii 00 92 00 00 00 00Scrippsiella trochoidea rough type 402 183 468 00 00 00Scrippsiella trochoidea smooth type 00 92 117 00 111 00Scrippsiella trochoideamedium type 1810 733 1054 1731 1111 2384Scrippsiella trochoidea small type 805 642 585 2308 00 00Scrippsiella sp 1 201 00 117 00 111 00Scrippsiella sp 4 00 92 00 00 00 00Thoracosphaera sp 1 00 00 117 00 111 00Dinophyta sp 2 00 00 234 00 00 00Dinophyta sp 17 00 183 00 00 00 00Dinophyta sp 26 00 183 00 00 00 00Dinophyta sp 33 00 00 00 00 111 00Codonellopsis schabii 10 00 09 06 03 05Stenosemella ventricosa 01 00 00 00 00 00Strobilidium sp 01 00 01 00 00 00Strombidium acutum 00 00 00 00 111 00Tintinnopsis cylindrica 00 00 00 00 01 01Undella claparedei 01 00 01 00 00 00Brachionus plicatilis 02 00 01 03 00 01Synchaeta sp spiny type 03 02 00 02 00 01Penilia avirostris 00 00 01 00 00 00Acartia clausimargalefi 10 03 07 15 03 08Acartia sp 1 01 00 01 00 00 00Centropages sp 03 02 00 02 01 02Cyst type 1 00 00 00 577 00 00

Table 3 Abundance and diversity indices calculated for resting stages in surface sediments at two stations investigated in Bay of Vlore

Abundancecysts gminus1 dw

Total densitycysts gminus1 dw 119878 119889 119867

1015840

1198691015840

Station 40 389 plusmn 127 1167 18 plusmn 27 29 plusmn 03 22 plusmn 01 07 plusmn 01


Abundance averageplusmn standard deviation from three replicates Total density sum of cyst abundances observed in three replicates from each station 119878 numberof taxa identified (average plusmn standard deviation) 119889 Margalef diversity index1198671015840 Shannon diversity index 1198691015840 Pieloursquos evenness index


Table 4 Results of SIMPER analysis for resting stages from surface sediments at stations 40 and 45 in Bay of Vlore

Taxa Av Abund Av Sim SimSD Contrib CumStation 40

Average similarity 5681Scrippsiella trochoideamedium type 11992 2161 745 3805 3805Scrippsiella trochoidea small type 6773 1581 614 2783 6587Scrippsiella trochoidea rough type 3513 644 278 1134 7721Pentapharsodinium tyrrhenicum type 1 2733 518 896 913 8634Calciodinellum albatrosianum 2453 494 724 869 9503

Station 45Average similarity 4037

Scrippsiella trochoideamedium type 17421 4003 587 9916 9916Stations 40 and 45Average dissimilarity = 5820

Cysts ascribed to the paleontological taxa Bicarinellumtricarinelloides and Calciperidinium asymmetricum both ger-minated thus confirming that they belong to modern taxaThe active stages obtained were tentatively identified asscrippsielloid dinoflagellates

An unknown ciliate cyst with a papula at both extremi-ties produced an active stage identifiable as belonging to theStrombidium genus (Figure 2)

4 Discussion

The total number of resting stage morphotypes recognizedin the present study is particularly high compared withother studies in the Mediterranean None of these studiesgave a number higher than the one reported here despitebeing based on a larger geographical area (the whole NorthAdriatic in [24]) or a higher number of samples (157sediment samples in [5]) This richness could be due toour enhanced ability with the passage of time to identifycysts from different species but it could also depend on theconsideration of different depths in the sediments Indeedthe other mentioned studies only reported cysts from thesediment surface while in the present case the type listgrew by more than 60 when below-surface layers wereconsidered

As a consequence of its richness the reported list adds42 morphotypes to the Albanian list and 13 alternativemorphotypes to already known taxaThis fact clearly demon-strates that the description of cyst assemblages in coastalMediterranean areas is still far from being exhaustive

The discovery of differences in the benthic species assem-blage with respect to the plankton is partially due to the usein cyst studies of a terminology derived from paleontologicalstudies which has yet to be standardised with reference tomodern terminology However it is evident that the activestages in the water column assemblage of the Bay of Vlore[15] differ in number and quality from that of the bottomsediments reported in the present study By way of exampleand only considering the surface sediment layer (ie themostaffected by recent sinking andor re-suspension) 4 different

species of Scrippsiella (Dinophyta) were isolated as cysts butonly 2 were reported [15] as active stages in the water columnfor thewhole bayMoreover in this study 5 different cyst typesfor the single species S trochoideawere identified differing interms of size and wall This is evidence of great intraspecificdiversity but it could be also a sign of the presence of crypticspecies as discussed byMontresor et al [25] differing in cystmorphology but not in that of the swimming stage

The rotifer Synchaeta sp was not found in the watercolumn but its resting eggs were easily recognizable andabundant in the sediments

While the case of S trochoidea confirms that muchremains to be discovered about the morphological variabilityof cysts produced by the same species (see [26] forDinophytaor [27] forCalanoida) Synchaeta sp is a clear case of a speciesnot detected in the active plankton assemblage but waiting inthe sediments for a favourable moment to rejoin the watercolumn

Alsoworthy of attention is the observation of aCiliophoracyst with two papulae on opposite sides (Figure 2) which hasnever been reported before

A study of plankton composition was carried out in thesame site during the same scientific cruise (January 2008) asthe present study [15] In January 2008 the phytoplanktonand the microzooplankton included a total of 178 categoriesConsidering only the main cyst producers (dinoflagellatesand ciliates) examination of the water column at 16 stationsgave a total of 76 taxa (48 dinoflagellates 28 ciliates) Thepresent analysis of sediments from just 2 stations gave atotal of 75 taxa This striking similarity of values was nothowever reflected in the taxonomic composition of the 2compartments Indeed 36 cyst types were identified as taxanot present in the plankton list for the same period (January2008) This number would be even higher if we consideredonly plankton from stations close to the two used here for thesediments

It was not possible to correlate cyst abundance alongthe sediment column with age of deposition which wouldrequire dating of the sediment layers In any case our resultsshowed that the total abundance of cysts in the upper layers


0 100 200 300 400 500 600 700 800

123456789

10111213

Dep

th (c

m)

St40 Cysts100 g dw

(a)

Dep

th (c

m)

123456789

10111213

0 200 400 600 800

St45Cysts100 g dw

(b)

0 05 1 15 2 25 3123456789

10111213

Dep

th (c

m)

St40 H998400

(c)

Dep

th (c

m)

123456789

10111213

0 05 1 15 2 25 3

St45 H998400

(d)

Figure 4 Resting stage abundance (average plusmn standard deviations) and Shannonrsquos index (1198671015840) values recorded for each cm layer of sedimentcores collected at two investigated stations in Bay of Vlore (Albania)

was up to 10 times greater than in lower ones The sharpdecrease in abundance below the 5th cm of depth at least atstation 40 does however suggest that an event occurred at acertain moment in the history of the plankton in the Bay ofVlore a suggestion that clearly requires further study Indeeddue to its position station 40 is a candidate for studies of thehistory of cyst production (and their arrival in the sediment)Located in a depression on the seabed the depth of St 40(minus54m) probably favours the sedimentation of fine particlesand the depletion of oxygen content and the deposition andaccumulation of sinking resting stages can thus be consideredundisturbed In addition the observed fall in diversity fromlower to upper layers could be correlated with the growthof cultural eutrophication (ie urban development) as pro-posed for Tokyo Bay and Daja Bay [28]

This situation at St 45 (depth 28m) is not completelyidentical It is near the slope of a detritus conewherematerialsfrom river Vjosa accumulate andmarine currents possibly actat a different rate from those acting on St 40

Incubation of encysted forms under controlled condi-tions to obtain germination is a useful tool for confirmingthe identification made by observation of the cyst In some

cases different species produce very similar cysts especiallywhen the morphology is very simple that is sphericalwithout processes or wall structures In the present studywe observed many Dinophyta cysts with the same basicmorphology that is round body and smooth brownwall withno apparent signs of paratabulation or spines or processesTheir germination allowed us to classify this basic type intoat least 6 species Round brown cysts are typical of Pro-toperidinium species [29 30] but we also recognized Diplop-salis lenticula Gymnodinium nolleri and Oblea rotunda aswell as 3 additional Protoperidinium species In the sameway it was possible to distinguish between Alexandriumminutum and Scrippsiella sp1 whose cysts are very similarand whose distinctive features are recognizable only aftergermination

Conversely analysis of cysts may allow us to identifyspecies whose active stages are indistinguishable at least byopticalmicroscopeThis is the case in the present study for theScrippsiella group which produces active cells that are verydifficult to distinguish although their cysts differ in terms ofthe type of calcareous covering colour and the presence ofspines [31 32]


45 1

45 2

45 345 4

45 545 645 7

45 8

45 9

45 10

45 11

45 12

45 1340 1

40 2

40 3

40 4

40 5

40 6

40 740 8

40 940 1040 11

40 12

40 13

Stress 012


Station4540

Figure 5 nMDS plot of samples from each cm of sediment cores collected at stations 40 and 45 in Bay of Vlore Hierarchical clusteringsuperimposed with cutoff at 70 similarity

Table 5 Results of SIMPER analysis for resting stages in sediment cores collected at stations 40 and 45 in Bay of Vlore


Average similarity 4416Centropages sp 177 877 086 1986 1986Codonellopsis schabii 210 700 131 1586 3572Acartia clausimargalefi 156 621 122 1406 4978Synchaeta sp spiny type 147 531 110 1202 6181Penilia avirostris 114 447 098 1013 7193Brachionus plicatilis 096 290 081 656 7849Stenosemella ventricosa 078 147 055 332 8181Strobilidium sp 073 143 051 323 8504Scrippsiella spp 057 095 036 214 8718Gonyaulax spp 054 071 034 160 8879Strombidium conicum 044 069 033 157 9036


Acartia clausimargalefi 188 1213 208 2305 2305Synchaeta sp spiny type 173 1091 159 2074 4379Codonellopsis schabii 143 673 112 1280 5659Strobilidium sp 112 605 092 1151 6810Centropages sp 120 605 102 1150 7960Brachionus plicatilis 084 273 063 519 8479Acartia sp1 075 257 058 489 8967Lingulodinium polyedrum 074 239 059 454 9422Groups 40 and 45Average dissimilarity = 5863


Worthy of special attention here is the recovery during thepresent study of Dinophyta cysts whose active stages have yetto be identified As cysts they are still classified with a pale-ontological name in accordance with their description fromPleistocene to Pliocene sediment strata in the Mediterranean[33] Two of these cyst types (Bicarinellum tricarinelloidesand Calciperidinium asymmetricum) were successfully ger-minated producing motile forms recognisable as belongingto the Calciodinellaceae family In any case their frequentobservation in surface sediments in other Mediterraneanareas [23 34] and in sediment traps [35] is a clear sign thatthese species are present in the water column today and needto be better identified

Conflict of Interests

The authors declare that there is no financial interest orconflict of interests involved

Acknowledgments

Thepresent study was funded by CoNISMa in the frameworkof the INTERREG III Italy Albania Programme CISMProject (Technical Assistance for Establishing and Man-agement of an International Center for Marine Studies inAlbania) The authors thank the crew of the Research VesselUniversitatis (CoNISMa) for the valuable field assistanceProfessor Sami Souissi (Universite de Lille France) who tookcare of the paper editing and two anonymous referees whowere extremely helpful in the improvement of the paper

References

[1] G Belmonte P Castello M R Piccinni et al ldquoResting stages inmarine sediments off the Italian coastrdquo in Biology and Ecologyof Shallow Coastal Waters A Elefteriou C J Smith and A DAnsell Eds pp 53ndash58 Olsen ampOlsen Fredensborg Denmark1995

[2] N H Marcus and F Boero ldquoMinireview the importance ofbenthic-pelagic coupling and the forgotten role of life cycles incoastal aquatic systemsrdquo Limnology and Oceanography vol 43no 5 pp 763ndash768 1998

[3] A Giangrande S Geraci and G Belmonte ldquoLife-cycle and life-history diversity inmarine invertebrates and the implications incommunity dynamicsrdquo Oceanography and Marine Biology vol32 pp 305ndash333 1994

[4] F Boero G Belmonte G Fanelli S Piraino and F RubinoldquoThe continuity of living matter and the discontinuities of itsconstituents do plankton and benthos really existrdquo Trends inEcology and Evolution vol 11 no 4 pp 177ndash180 1996

[5] SMoscatello F RubinoOD SaracinoG Fanelli G Belmonteand F Boero ldquoPlankton biodiversity around the Salento Penin-sula (South East Italy) an integrated watersediment approachrdquoScientia Marina vol 68 no 1 pp 85ndash102 2004

[6] F Rubino O D Saracino S Moscatello and G Belmonte ldquoAnintegrated watersediment approach to study plankton (a casestudy in the southern Adriatic Sea)rdquo Journal of Marine Systemsvol 78 no 4 pp 536ndash546 2009

[7] F Rubino O D Saracino G Fanelli G Belmonte A Migliettaand F Boero ldquoLife cycles and pelago-benthos interactionsrdquoBiologia Marina Mediterranea vol 5 pp 253ndash259 1998

[8] G Belmonte A Miglietta F Rubino and F Boero ldquoMorpho-logical convergence of resting stages of planktonic organisms areviewrdquo Hydrobiologia vol 355 no 1ndash3 pp 159ndash165 1997

[9] N H Marcus R Lutz W Burnett and P Cable ldquoAge viabilityand vertical distribution of zooplankton resting eggs froman anoxic basin evidence of an egg bankrdquo Limnology andOceanography vol 39 no 1 pp 154ndash158 1994

[10] X Jiang G Wang and S Li ldquoAge distribution and abundanceof viable resting eggs ofAcartia pacifica (Copepoda Calanoida)in Xiamen Bay Chinardquo Journal of Experimental Marine Biologyand Ecology vol 312 no 1 pp 89ndash100 2004

[11] H U Dahms X Li G Zhang and P Y Qian ldquoResting stagesof Tortanus forcipatus (Crustacea Calanoida) in sediments ofVictoria Harbor Hong Kongrdquo Estuarine Coastal and ShelfScience vol 67 no 4 pp 562ndash568 2006

[12] G Belmonte P Pirandola S Degetto and F Boero ldquoAbbon-danza vitalita e distribuzione verticale di forme di resistenza neisedimenti del Nord Adriaticordquo Biologia Marina Mediterraneavol 6 pp 172ndash178 1999

[13] S Ribeiro T Berge N Lundholm T J Andersen F Abrantesand M Ellegaard ldquoPhytoplankton growth after a century ofdormancy illuminates past resilience to catastrophic darknessrdquoNature Communications vol 2 no 1 article 311 2011

[14] N G Hairston Jr R A Van Brunt C M Kearns and DR Engstrom ldquoAge and survivorship of diapausing eggs in asediment egg bankrdquo Ecology vol 76 no 6 pp 1706ndash1711 1995

[15] S Moscatello C Caroppo E Hajderi and G Belmonte ldquoSpacedistribution of phyto- and microzooplankton in the Vlora Bay(Southern Albania Mediterranean Sea)rdquo Journal of CoastalResearch no 58 pp 80ndash94 2011

[16] P Maiorano F Mastrototaro S Beqiraj et al ldquoBioecologicalstudy of the benthic communities on the soft bottom of theVlora Gulf (Albania)rdquo Journal of Coastal Research no 58 pp95ndash105 2011

[17] C J Bolch and GM Hallegraeff ldquoDinoflagellate cysts in recentmarine sediments from Tasmania Australiardquo Botanica Marinavol 33 pp 173ndash192 1990

[18] J A Sonneman and D R A Hill ldquoA taxonomic survey of cyst-producing dinoflagellates from recent sediments of Victoriancoastal waters Australiardquo Botanica Marina vol 40 no 3 pp149ndash177 1997

[19] A Rochon A De Vernal J L Turon J Matthiessen and MJ Head ldquoDistribution of recent dinoflagellate cysts in surfacesediments from the North Atlantic Ocean and adjacent seas inrelation to sea-surface parametersrdquo AASP Contribution Seriesvol 35 pp 1ndash152 1999

[20] P C Reid and A W G John ldquoTintinnid cystsrdquo Journal of theMarine Biological Association of the United Kingdom vol 58 pp551ndash557 1978

[21] P C Reid and A W G John ldquoResting cysts in the ciliateclass Polymenophorea phylogenetic implicationsrdquo Journal ofProtozoology vol 30 pp 710ndash712 1978

[22] T Onbe ldquoSugar flotation method for sorting the resting eggs ofmarine cladocerans and copepods fron sea bottom sedimentsrdquoBulletin of the Japanese Society for the Science of Fish vol 44 p1411 1978

[23] F Rubino M Belmonte C Caroppo and M GiacobbeldquoDinoflagellate cysts from surface sediments of Syracuse Bay


(Western Ionian Sea Mediterranean)rdquo Deep-Sea Research PartII vol 57 no 3-4 pp 243ndash247 2010

[24] F Rubino G Belmonte AMMiglietta S Geraci and F BoeroldquoResting stages of plankton in recent NorthAdriatic sedimentsrdquoMarine Ecology vol 21 no 3-4 pp 263ndash284 2000

[25] M Montresor S Sgrosso G Procaccini andW H C F Koois-tra ldquoIntraspecific diversity in Scrippsiella trochoidea (Dino-phyceae) evidence for cryptic speciesrdquo Phycologia vol 42 no1 pp 56ndash70 2003

[26] A Rochon J Lewis M Ellegaard and I C Harding ldquoTheGonyaulax spinifera (Dinophyceae) ldquocomplexrdquo perpetuatingthe paradoxrdquo Review of Palaeobotany and Palynology vol 155no 1-2 pp 52ndash60 2009

[27] G Belmonte ldquoDiapause egg production in Acartia (Paracar-tia) latisetosa (Crustacea Copepoda Calanoida)rdquo Bolletino diZoologia vol 59 pp 363ndash366 1992

[28] Z Wang K Matsuoka Y Qi J Chen and S Lu ldquoDinoflagellatecyst records in recent sediments from Daya Bay South ChinaSeardquo Phycological Research vol 52 no 4 pp 396ndash407 2004

[29] R Harland ldquoA review of recent and quaternary organic-walleddinoflagellate cysts of the genus Protoperidiniumrdquo Paleontologyvol 25 pp 369ndash397 1982

[30] J Lewis J D Dodge and P Tett ldquoCyst-theca relationship insome Protoperidinium species (Peridiniales) from Scottish sealochsrdquo Journal of Micropalaeontology vol 3 pp 25ndash34 1984

[31] M Gottschling R Knop J Plotner M Kirsch H Willemsand H Keupp ldquoA molecular phylogeny of Scrippsiella sensulato (Calciodinellaceae Dinophyta) with interpretations onmorphology and distributionrdquo European Journal of Phycologyvol 40 no 2 pp 207ndash220 2005

[32] H Gu J Sun W H C F Kooistra and R Zeng ldquoPhylogeneticposition and morphology of thecae and cysts of Scrippsiella(Dinophyceae) species in the East China Seardquo Journal ofPhycology vol 44 no 2 pp 478ndash494 2008

[33] G J M Versteegh ldquoNew Pliocene and Pleistocene calcareousdinoflagellate cysts from southern Italy and Creterdquo Review ofPalaeobotany and Palynology vol 78 no 3-4 pp 353ndash380 1993

[34] K J S Meier and H Willems ldquoCalcareous dinoflagellate cystsin surface sediments from the Mediterranean Sea distribu-tion patterns and influence of main environmental gradientsrdquoMarine Micropaleontology vol 48 no 3-4 pp 321ndash354 2003

[35] F Rubino S Moncheva M Belmonte N Slabakova andL Kamburska ldquoResting stages produced by plankton in theBlack Seamdashbiodiversity and ecological perspectiverdquo RapportCommission International pour lrsquoExploration Scientifique de laMer Mediterranee vol 39 p 399 2010

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

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EcosystemsJournal of


MeteorologyAdvances in

EcologyInternational Journal of


Marine BiologyJournal of


Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in


Environmental Chemistry

Atmospheric SciencesInternational Journal of



Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics


Geological ResearchJournal of

EarthquakesJournal of


BiodiversityInternational Journal of


ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of


The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014


ClimatologyJournal of


dinoflagellates differ in the length of their life cycle andorthe timing of cyst production and the rest capacity of restingstages also varies They are generally programmed to rest forthe duration of the adverse period but fractions of themcan also rest for longer periods allowing the population toreappear decades later ([9ndash11] for copepods [12 13] fordinoflagellates) Hairston et al [14] reported a rest of morethan 300 years for a calanoid resting egg albeit of a freshwaterspecies

The scarcity of literature on whole resting stage commu-nities encouraged us to describe situations in various parts ofthe Mediterranean in order to obtain a rich data set usefulfor building models and in experimental situations Herea detailed description of the structure of the marine ldquoseedbankrdquo produced by plankton in the Bay of Vlore is reported

The present study also focuses on an Albanian bay thathas not been extensively studied from themarine biodiversitypoint of view The data from the benthos are comparedwith analyses of the phytoplankton and microzooplankton[15] in the water column to assess with more precision thebiodiversity of the plankton in the Bay of Vlore

Moscatello et al [15] reported that the microzooplanktoncommunity of the Bay of Vlore was composed of more than200 taxa of which 97 were classified as ldquoseasonally absentrdquoThe aim of the present paper is to determine whether theseabsences in the water column correspond to resting stages inthe sediments

2 Materials and Methods

21 Study Site An oceanographic campaign was carried outin the Bay of Vlore from 17th to 23rd of January 2008 aboardthe oceanographic vessel ldquoUniversitatisrdquo This survey wasconducted as part of the PIC Interreg III Italy Albania Projectfor providing technical assistance for the management of anInternational Centre of Marine Sciences (CISM) in AlbaniaThe sampling period of the present study (January 2008)coincided with that of Moscatello et al [15] who investigatedactive plankton in the water column in the same area

In order to investigate the presence and distribution ofresting stages produced by plankton species in the area2 stations were chosen representing 2 different types ofenvironment a deep zone (station 40 depth 54m) withsediments of terrigenous mud dominated by Labidoplaxdigitata (Holothuroidea) and a shallower site (station 45depth 28m) with sediments of terrigenous mud dominatedby Turritella communis (Gastropoda) (Figure 1) (for theclassification of mud biocenosis in the Bay of Vlore see [16])

22 Sampling Procedure Samples of bottom sediments werecollected in three replicates (named 40 a b c and 45 a b c)using a Van Veen grab with upper windows that allowed thecollection of undisturbed sediment cores At each station 2different PVC corers (h 30 cm inner w 4 and 8 cm) wereused in order to obtain 2 different sets of samples Thesmaller core was processed to obtain cysts of protists thelarger core was processed to obtain resting eggs ofmetazoansThis differentiation was necessary because metazoan resting

N

Radhime

Vlore

Zvernec

Sazan isleNa

Orikum

45

40

NNNNNNaaaaaaaaaaaaaaaaaaaaaaaaaaNNNaaaaaaaaaaaaaaaNNaaaaaaaaaaNaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaa

Karaburun peninsula

40∘25

998400N

40∘20

998400N

19∘25

998400E19∘20

998400E

Figure 1 Map of study area showing location of two samplingstations (40 45) in Bay of Vlore (Albania)

stages are less abundant so a greater amount of sediment isrequired Moreover their walls are only organic allowing theadoption of a centrifugation method coupled with filtrationto obtain a ldquocleanrdquo sample from a relatively large quantity ofsediment In contrast protistan cysts are more abundant andhave different types of walls (calcareous siliceous organic)which complicates the procedure when the whole cyst bankis studied Thus the most fruitful method of separating cystsfrom sediment is filtration through meshes of different sizes

After extraction sediment cores were immediately sub-divided into 1 cm thick layers until the 15th cm from thesediment surface The thickness of 15 cm was chosen becausein previous studies we noted that abundances diminishedsignificantly at depths of more than 7ndash10 cm below thesediment surface [1 12] The outer edge of each layer wasdiscarded to avoid contamination from material from theoverlaying layer during the insertion of the corer into thesediments Once obtained the samples were stored in thedark at 5∘C until treatment in the laboratory

23 Protistan Cysts (20ndash125 120583m) In the laboratory the small-core samples were treated using a sieving technique consist-ing of the following steps

(i) The entire sample is homogenized and then sub-sampled obtaining 3ndash5mL of wet sediment which ispassed through a 20120583m mesh (Endecottrsquos LTD steelsieves ISO3310-1 London England) using naturalfiltered (045 120583m) seawater (Gulf of Taranto)

(ii) The retained fraction is ultrasonified for 1min andagain passed through a series of sieves (125 75 and20120583m mesh sizes) obtaining a fine-grained fraction(20ndash75120583m) containing most of the protistan cysts


















3 Results












Alexandrium sp 1 e

Alexandrium sp 2 e











































Table 1 Continued









Dinophyta sp 2 e e

Dinophyta sp 7 e e

Dinophyta sp 17 e

Dinophyta sp 26 e

Dinophyta sp 30 e

Dinophyta sp 33 e e








Strobilidium sp e e



















Resting Egg 1 e

Resting Egg 9 e



(a)

(c)

(b)







40a

40b

40c

45a

45b

45c

Stress 0








40a 40b 40c 45a 45b 45c





1015840

1198691015840












4 Discussion











0 100 200 300 400 500 600 700 800

123456789

10111213

Dep

th (c

m)

St40 Cysts100 g dw

(a)

Dep

th (c

m)

123456789

10111213

0 200 400 600 800

St45Cysts100 g dw

(b)

0 05 1 15 2 25 3123456789

10111213

Dep

th (c

m)

St40 H998400

(c)

Dep

th (c

m)

123456789

10111213

0 05 1 15 2 25 3

St45 H998400

(d)








45 1

45 2

45 345 4

45 545 645 7

45 8

45 9

45 10

45 11

45 12

45 1340 1

40 2

40 3

40 4

40 5

40 6

40 740 8

40 940 1040 11

40 12

40 13

Stress 012


Station4540











Acknowledgments


References










































Journal of












Volume 2014

Advances in









Geophysics































3 Results












Alexandrium sp 1 e

Alexandrium sp 2 e











































Table 1 Continued









Dinophyta sp 2 e e

Dinophyta sp 7 e e

Dinophyta sp 17 e

Dinophyta sp 26 e

Dinophyta sp 30 e

Dinophyta sp 33 e e








Strobilidium sp e e



















Resting Egg 1 e

Resting Egg 9 e



(a)

(c)

(b)







40a

40b

40c

45a

45b

45c

Stress 0








40a 40b 40c 45a 45b 45c





1015840

1198691015840












4 Discussion











0 100 200 300 400 500 600 700 800

123456789

10111213

Dep

th (c

m)

St40 Cysts100 g dw

(a)

Dep

th (c

m)

123456789

10111213

0 200 400 600 800

St45Cysts100 g dw

(b)

0 05 1 15 2 25 3123456789

10111213

Dep

th (c

m)

St40 H998400

(c)

Dep

th (c

m)

123456789

10111213

0 05 1 15 2 25 3

St45 H998400

(d)








45 1

45 2

45 345 4

45 545 645 7

45 8

45 9

45 10

45 11

45 12

45 1340 1

40 2

40 3

40 4

40 5

40 6

40 740 8

40 940 1040 11

40 12

40 13

Stress 012


Station4540











Acknowledgments


References










































Journal of












Volume 2014

Advances in









Geophysics



















Alexandrium sp 1 e

Alexandrium sp 2 e











































Table 1 Continued









Dinophyta sp 2 e e

Dinophyta sp 7 e e

Dinophyta sp 17 e

Dinophyta sp 26 e

Dinophyta sp 30 e

Dinophyta sp 33 e e








Strobilidium sp e e



















Resting Egg 1 e

Resting Egg 9 e



(a)

(c)

(b)







40a

40b

40c

45a

45b

45c

Stress 0








40a 40b 40c 45a 45b 45c





1015840

1198691015840












4 Discussion











0 100 200 300 400 500 600 700 800

123456789

10111213

Dep

th (c

m)

St40 Cysts100 g dw

(a)

Dep

th (c

m)

123456789

10111213

0 200 400 600 800

St45Cysts100 g dw

(b)

0 05 1 15 2 25 3123456789

10111213

Dep

th (c

m)

St40 H998400

(c)

Dep

th (c

m)

123456789

10111213

0 05 1 15 2 25 3

St45 H998400

(d)








45 1

45 2

45 345 4

45 545 645 7

45 8

45 9

45 10

45 11

45 12

45 1340 1

40 2

40 3

40 4

40 5

40 6

40 740 8

40 940 1040 11

40 12

40 13

Stress 012


Station4540











Acknowledgments


References










































Journal of












Volume 2014

Advances in









Geophysics















Table 1 Continued









Dinophyta sp 2 e e

Dinophyta sp 7 e e

Dinophyta sp 17 e

Dinophyta sp 26 e

Dinophyta sp 30 e

Dinophyta sp 33 e e








Strobilidium sp e e



















Resting Egg 1 e

Resting Egg 9 e



(a)

(c)

(b)







40a

40b

40c

45a

45b

45c

Stress 0








40a 40b 40c 45a 45b 45c





1015840

1198691015840












4 Discussion











0 100 200 300 400 500 600 700 800

123456789

10111213

Dep

th (c

m)

St40 Cysts100 g dw

(a)

Dep

th (c

m)

123456789

10111213

0 200 400 600 800

St45Cysts100 g dw

(b)

0 05 1 15 2 25 3123456789

10111213

Dep

th (c

m)

St40 H998400

(c)

Dep

th (c

m)

123456789

10111213

0 05 1 15 2 25 3

St45 H998400

(d)








45 1

45 2

45 345 4

45 545 645 7

45 8

45 9

45 10

45 11

45 12

45 1340 1

40 2

40 3

40 4

40 5

40 6

40 740 8

40 940 1040 11

40 12

40 13

Stress 012


Station4540











Acknowledgments


References










































Journal of












Volume 2014

Advances in









Geophysics















(a)

(c)

(b)







40a

40b

40c

45a

45b

45c

Stress 0








40a 40b 40c 45a 45b 45c





1015840

1198691015840












4 Discussion











0 100 200 300 400 500 600 700 800

123456789

10111213

Dep

th (c

m)

St40 Cysts100 g dw

(a)

Dep

th (c

m)

123456789

10111213

0 200 400 600 800

St45Cysts100 g dw

(b)

0 05 1 15 2 25 3123456789

10111213

Dep

th (c

m)

St40 H998400

(c)

Dep

th (c

m)

123456789

10111213

0 05 1 15 2 25 3

St45 H998400

(d)








45 1

45 2

45 345 4

45 545 645 7

45 8

45 9

45 10

45 11

45 12

45 1340 1

40 2

40 3

40 4

40 5

40 6

40 740 8

40 940 1040 11

40 12

40 13

Stress 012


Station4540











Acknowledgments


References










































Journal of












Volume 2014

Advances in









Geophysics
















40a 40b 40c 45a 45b 45c





1015840

1198691015840












4 Discussion











0 100 200 300 400 500 600 700 800

123456789

10111213

Dep

th (c

m)

St40 Cysts100 g dw

(a)

Dep

th (c

m)

123456789

10111213

0 200 400 600 800

St45Cysts100 g dw

(b)

0 05 1 15 2 25 3123456789

10111213

Dep

th (c

m)

St40 H998400

(c)

Dep

th (c

m)

123456789

10111213

0 05 1 15 2 25 3

St45 H998400

(d)








45 1

45 2

45 345 4

45 545 645 7

45 8

45 9

45 10

45 11

45 12

45 1340 1

40 2

40 3

40 4

40 5

40 6

40 740 8

40 940 1040 11

40 12

40 13

Stress 012


Station4540











Acknowledgments


References










































Journal of












Volume 2014

Advances in









Geophysics






















4 Discussion











0 100 200 300 400 500 600 700 800

123456789

10111213

Dep

th (c

m)

St40 Cysts100 g dw

(a)

Dep

th (c

m)

123456789

10111213

0 200 400 600 800

St45Cysts100 g dw

(b)

0 05 1 15 2 25 3123456789

10111213

Dep

th (c

m)

St40 H998400

(c)

Dep

th (c

m)

123456789

10111213

0 05 1 15 2 25 3

St45 H998400

(d)








45 1

45 2

45 345 4

45 545 645 7

45 8

45 9

45 10

45 11

45 12

45 1340 1

40 2

40 3

40 4

40 5

40 6

40 740 8

40 940 1040 11

40 12

40 13

Stress 012


Station4540











Acknowledgments


References










































Journal of












Volume 2014

Advances in









Geophysics















0 100 200 300 400 500 600 700 800

123456789

10111213

Dep

th (c

m)

St40 Cysts100 g dw

(a)

Dep

th (c

m)

123456789

10111213

0 200 400 600 800

St45Cysts100 g dw

(b)

0 05 1 15 2 25 3123456789

10111213

Dep

th (c

m)

St40 H998400

(c)

Dep

th (c

m)

123456789

10111213

0 05 1 15 2 25 3

St45 H998400

(d)








45 1

45 2

45 345 4

45 545 645 7

45 8

45 9

45 10

45 11

45 12

45 1340 1

40 2

40 3

40 4

40 5

40 6

40 740 8

40 940 1040 11

40 12

40 13

Stress 012


Station4540











Acknowledgments


References










































Journal of












Volume 2014

Advances in









Geophysics















45 1

45 2

45 345 4

45 545 645 7

45 8

45 9

45 10

45 11

45 12

45 1340 1

40 2

40 3

40 4

40 5

40 6

40 740 8

40 940 1040 11

40 12

40 13

Stress 012


Station4540











Acknowledgments


References










































Journal of












Volume 2014

Advances in









Geophysics


















Acknowledgments


References










































Journal of












Volume 2014

Advances in









Geophysics
































Journal of












Volume 2014

Advances in









Geophysics














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