www.elsevier.com/locate/scitotenv

Science of the Total Environm

Phytoplankton size-distribution and community structure in relation

to mucilage occurrence in the northern Adriatic Sea

Cecilia Totti a,*, Monica Cangini b, Carla Ferrari c, Romina Kraus d, Marinella Pompei b,

Alessandra Pugnetti e, Tiziana Romagnoli a, Silvana Vanucci f, Giorgio Socal e

a Dipartimento di Scienze del mare, Universita Politecnica delle Marche, Via Brecce Bianche, 60131, Ancona, Italyb Centro Ricerche Marine, Viale Vespucci 2, I-47042 Cesenatico, Italy

c Struttura Oceanografica Daphne, ARPAER, Viale Vespucci 2, I-47042 Cesenatico, Italyd Center for Marine Research, Rudjer Boskovic Institute, G. Paliaga 5, 52210 Rovinj, Croatia

e Istituto di Scienze Marine (ISMAR), CNR, Castello 1364, I-30122 Venezia, Italyf Dipartimento di Biologia Animale ed Ecologia Marina, Universita di Messina, Messina, Italy

Available online 4 October 2005

Abstract

The spatial and temporal variations of pico-, nano- and microphytoplankton abundance and composition were investigated over

a 37 month period, focusing on the ecological role of different size classes of phytoplankton, and on the changes of the community

structure that might occur during periods when large mucilage macroaggregates appear. Samples were collected monthly from June

1999 to July 2002 at 11 stations, along three transects covering the northern Adriatic basin. Highest abundances were observed in

late-winter/spring for microphytoplankton (mainly diatoms), in spring–summer for nanophytoplankton, and in summer for

picophytoplankton. The autotrophic component was more abundant in the summers of 2000 and 2002 (when large mucilage

aggregates occurred) than in the summers of 1999 and 2001 (when a massive phenomenon was not observed). This increase was

statistically significant for pico-, nano- and, among microphytoplankton, only for dinoflagellates. Blooms of picophytoplankton

were often observed at the bottom layer during mucilage summers. The microphytoplankton community during mucilage

phenomena was characterized by a species composition (Chaetoceros spp., Cerataulina pelagica, Pseudo-nitzschia delicatissima,

P. pseudodelicatissima, Cylindrotheca closterium, Dactyliosolen fragilissimus) comparable to that observed in summers without

extensive mucilage occurrence. However, some species appeared with significantly higher densities in the summers of 2000 and

2002: Ceratium furca, C. closterium, Oxytoxum spp., Hemiaulus hauckii and Gonyaulax fragilis. Microscopic observation of

aggregates revealed that the microphytoplankton species composition inside the aggregates was comparable to that observed in the

water column, with an enrichment of opportunistic species such as C. closterium and P. delicatissima. The presence of mucilage

aggregates affects the phytoplankton populations in the water column, even when aggregates are at early stages. It seems that there

is a mutual relationship between phytoplankton and aggregates, i.e., several diatom and dinoflagellate species may contribute to the

aggregate formation and enlargement, but mucilage aggregates themselves may also affect the phytoplankton populations, allowing

the development of a rich diatom community and in general enhancing nanophytoplankton growth.

D 2005 Elsevier B.V. All rights reserved.

Keywords: Mucilage aggregates; Microphytoplankton; Nanophytoplankton; Picophytoplankton; Northern Adriatic Sea

0048-9697/$ - s

doi:10.1016/j.sc

* Correspondin

E-mail addre

ent 353 (2005) 204–217

ee front matter D 2005 Elsevier B.V. All rights reserved.

itotenv.2005.09.028

g author. Tel.: +39 071 220 4647; fax: +39 071 220 4650.

ss: c.totti@univpm.it (C. Totti).

C. Totti et al. / Science of the Total Environment 353 (2005) 204–217 205

1. Introduction

Large mucilage aggregates (the ddirty seaT phenom-

enon) have been reported in the Adriatic Sea since

17th century, when several episodes where reported

and the first hypotheses were formulated (Fonda-

Umani et al., 1989 and references therein). Recent

episodes of large mucilage macroaggregate formation

in the northern Adriatic Sea occurred in 1988, 1989,

1991, 1997, 2000 and 2002. Nevertheless, the phe-

nomenon has been observed at its early stages (marine

snow and microflocs occurrence) almost every year.

This phenomenon starts in late-spring/early-summer,

when the stratification of the water column strength-

ens, and the water mass exchange between the north-

ern and middle sub-basin slows down (Degobbis et

al., 1999).

There is a general agreement that large mucilaginous

macroaggregates represent the last stage of aggregation

of organic matter (i.e. DOM), mainly formed by gelat-

inous polysaccharides. The origin of this organic matter

has been historically attributed to the phytoplankton

exudates (Alldredge et al., 1993; Myklestad, 1995;

Alldredge, 1999), as well as to bacterial activity

(Azam et al., 1999; Azam and Long, 2001; Simon et

al., 2002). Indeed, mucilage formation is a very com-

plex phenomenon involving several biological and hy-

drological interactions. Single phases of the problem

have been addressed and explained by the scientific

community, i.e. the production of organic matter, its

aggregation into larger formations, the role of biologi-

cal communities inhabiting the aggregates, the scarce

degradability of aggregates, the meteo-oceanographic

conditions, the climatic factors etc. Although many

steps of this phenomenon have been clarified, and

several models have been proposed, this dpuzzleT in

its completeness has still not been solved, and many

questions, such as the relative role of phytoplankton

and bacteria, or the relative importance of the extracel-

lular production of diatoms and dinoflagellates, are still

open.

The environmental conditions that seem to be

propitious to mucilage formation involve (i) a general

P limitation, which affects both the amount of phy-

toplankton exudation (Obernosterer and Herndl, 1995)

and the bacterial activity (Danovaro, 1998), and (ii)

the meteo-oceanographic conditions and the pattern

of currents: i.e. years of mucilage appearance were

characterized by a reduced circulation in the northern

Adriatic sub-basin during late spring–summer, due to

a strong decrease of the western Adriatic coastal

current (Russo et al., 2005–this volume). Moreover,

the Istrian counter-current and the related offshore

anticyclone can also play a significant role in retain-

ing freshwater in the northern Adriatic (Supic et al.,

2000).

It is well known that micro- and macroaggregates

represent a suitable microhabitat for a rich community

of microorganisms (cyanobacteria, eukaryotic phyto-

plankton, heterotrophic bacteria, microzooplankton,

etc.), which often reach densities 1–2 orders of magni-

tude higher than those observed in the surrounding

water (Pistocchi et al., 2005–this volume). Furthermore,

the biological activity of aggregate inhabitants can

contribute to aggregate enlargement. This role was

evidenced for some diatoms (e.g. Cylindrotheca clos-

terium), for bacteria which are able to produce large

amounts of highly refractory capsular material (Stoder-

egger and Herndl, 1998), and for cyanobacteria, it has

been suggested play a significant role in the secondary

enlargement of macroaggregates (Kaltenbock and

Herndl, 1992).

The composition of phytoplankton assemblages in

the aggregates and in the surrounding water has aroused

much interest since the occurrence of the first episodes

of mucilage appearance, due to their possible involve-

ment in the genesis of the phenomenon, at least in its

early stages (Fonda-Umani et al., 1989). In past epi-

sodes, species prevailing in the aggregates such as

Cylindrotheca closterium were indicated as responsible

for their production, because (i) they were often very

abundant in the aggregates of different areas (Revelante

and Gilmartin, 1991; Pettine et al., 1993) and (ii) under

experimental conditions they were able to produce large

amounts of polysaccharides, which seem to be refrac-

tory to decomposition (Monti et al., 1995; Alldredge,

1999; Alcoverro et al., 2000). Actually, phytoplankton

communities associated with mucilage aggregates have

been shown to vary, with different dominating species,

depending on sampling area and period (Marchetti et

al., 1989; Honsell and Cabrini, 1990; Revelante and

Gilmartin, 1991; Cabrini et al., 1992; Pettine et al.,

1993; Totti et al., 1993).

During the MAT (Processi di formazione delle

Mucillagini nell’Adriatico e nel Tirreno) programme,

the entire sub-basin of the northern Adriatic Sea was

sampled with monthly frequency, from the Italian to the

Croatian coast, during both the occurrence and absence

of large aggregates.

In this paper, we describe the spatial and temporal

variations of phytoplankton abundance and composi-

tion over a 37 month period (1999–2002), focusing (i)

on the ecological role of pico-, nano- and microphyto-

plankton and (ii) on the microphytoplankton communi-

C. Totti et al. / Science of the Total Environment 353 (2005) 204–217206

ty structure in summer periods, during the appearance

of large macroaggregates.

2. Materials and methods

2.1. Sampling

Sampling was carried out, on monthly basis from

June 1999 to July 2002, along three transects (A, B,

C) from the Italian to the Croatian coast, covering the

entire northern Adriatic basin. Several stations were

selected along the three transects, in order to repre-

sent the western, central and eastern areas of each

transect (Fig. 1): transect A (stations A3, A7, A11), B

(stations B3, B6, B10, B13, B15), and C (stations

C1, C4, C7, C12, C14). Water samples were collected

using a Rosette Multisampler coupled with Niskin

bottles, at selected depths (2 to 4 for each stations):

at the surface, near the bottom and 1–2 intermediate

depths, depending on the water column structure and

on the fluorescence profile (in stratification condi-

tions, base of mixed layer and maximum fluorescence

depth).

2.2. Pico- and nanophytoplankton

After collection, samples (500 ml) were preserved

by adding glutaraldehyde (0.5% final concentrations),

and stored in the dark at +4 8C until the slides were

prepared (within a few days from sampling). For nano-

phytoplankton, sub-samples (35–40 ml) were stained

with DAPI (4V,6V-diamidino-2-phenylindole) and fil-

tered at low pressure (b50 mm Hg) onto 2.0 Am pore

size (25 mm diameter) Nuclepore filters. For picophy-

toplankton, sub-samples (10–30 ml) were filtered (b50

mm Hg) onto 0.2 Am pore size (25 mm diameter)

Nuclepore filters. Filters (both for nanophytoplankton

and picophytoplankton) were then washed with 0.2 Amprefiltered seawater, and mounted on glass slides

(Kemp et al., 1993). Duplicate slides were prepared

for each sample. Slides were stored at �20 8C in the

dark until microscopic examination (within a few days).

Slides for nanophytoplankton enumeration were exam-

ined for DAPI (set filter: G365/FT395/LP420) and

chlorophyll fluorescence (set filter: BP450-490/

FT510/LP520) at �1000 using a Zeiss Axioplan epi-

fluorescence microscope. A minimum of 100–150 cells

per filter were counted. Nanophototrophs were distin-

guished from heterotrophs by their chlorophyll auto-

fluorescence, and their cell shape and flagella were

visualised by DAPI staining fluorescence (Sherr and

Sherr, 1993). Slides for picophytoplankton were ob-

served at �1000 using the same epifluorescence micro-

scope (set filter: BP450-490/FT510/LP520). Counting

for picophytoplankton was carried out on 20–30 ran-

domly chosen fields.

2.3. Microphytoplankton

Samples from transect B and C were preserved with

0.8% formaldehyde, prefiltered and neutralized with

hexamethylene-tetramine (Throndsen, 1978), and

stored in dark glass bottles. Samples from transect A

were preserved with Lugol’s solution buffered with

sodium acetate and stored in dark plastic bottles. Micro-

phytoplankton analysis was carried out at the inverted

microscope following the Utermohl method (Hasle,

1978). Counting was carried out at �400 magnification

along transects or in random fields of vision (Cordella

and Cavolo, 1988) to count a minimum of 200 cells.

This counting was then integrated with the count on the

whole sedimentation chamber with �200 magnifica-

tion, to have a more correct estimation of taxa, less

abundant, but having greater volume. During counting,

only autotrophic microphytoplanktonic fraction was

considered (i.e. cells which, at least in one dimension,

were greater than 20 Am), including nanoplanktonic

colonial species. Microphytoplankton taxa were finally

grouped into major classes, diatoms, dinoflagellates,

others; the latter group includes flagellates (mostly

euglenophyceans), coccolithophorids, and incertae

sedis having size N20 Am.

2.4. Mucilage aggregate sampling

During mucilage appearance, aggregates were also

sampled by scuba divers, using syringes or pump

(Giani et al., 2005–this volume). Samples for micro-

scopic observation were preserved by adding 1.6%

prefiltered neutralized formaldehyde. Mucilage samples

were then examined for a qualitative analysis of their

phytoplankton composition. In several samples, a rough

estimate of cell density within mucilage aggregates was

also carried out: a small volume of mucilage was

poured into a sedimentation chamber using a micropi-

pette and the cells were counted.

2.5. Statistical analysis

Statistical analyses were performed using Statistica

by Statsoft. Differences in the pico-, nano- and micro-

phytoplankton abundances were established among sea-

sons, years, summers with and without mucilage,

transects, western and eastern areas and depths, using

Fig. 1. The study area.

C. Totti et al. / Science of the Total Environment 353 (2005) 204–217 207

multivariate analysis-of-variance (MANOVA) tech-

nique. When a significant difference for the main effect

was observed (P b0.05), a Tukey’s pairwise compari-

son test was also performed.

Principal component analysis (PCA) was carried

out to analyze the whole data set, after log-transfor-

mation of biological data to meet assumptions of

normality.

Table

1

Meanvalues

andstandarddeviationsofmainenvironmentalparam

etersandphytoplanktonabundances(cellsl�

1)in

each

samplingstationduringtheentire

studyperiod:salinity(S),totalinorganic

nitrogen

(DIN

),orthophosphate(PO4),silicate

(SiO4),picophytoplankton(Pico),nanophytoplankton(N

ano),diatoms(D

iato),dinoflagellates(D

ino),other

microphytoplanktongroups(O

th)and

Totalmicrophytoplankton(Totalmicrophyto),n.a.(notavailable)

Stat

S(PSU)

DIN

(AM)

PO4(AM)

SiO4(AM)

Pico

Nano

Diato

Dino

Oth

Totalmicrophyto

Avg.

Std.

Avg.

Std.

Avg.

Std.

Avg.

Std.

Avg.

Std.

Avg.

Std.

Avg.

Std.

Avg.

Std.

Avg.

Std.

Avg.

Std.

A3

36.83

1.96

3.09

4.58

0.09

0.11

5.20

6.22

4.59EF07

5.97EF07

2.22EF06

2.73EF06

358,393

597,760

3203

6531

701

1844

362,297

600,691

A7

37.29

1.28

2.09

2.28

0.06

0.07

4.20

4.93

3.75EF07

3.68EF07

1.66EF06

1.45EF06

251,739

418,725

3114

6457

985

4754

255,838

423,701

A11

37.62

0.87

1.16

0.91

0.02

0.02

2.64

2.15

3.10EF07

2.49EF07

1.51EF06

1.55EF06

56,523

127,254

1612

2965

449

872

58,583

129,798

B3

35.67

3.47

4.14

5.96

0.08

0.06

4.95

6.49

3.19EF07

5.35EF07

1.52EF06

1.20EF06

851,739

2,350,004

2531

6591

––

854,270

2,354,258

B6

36.93

3.07

1.92

2.78

0.07

0.06

3.06

3.17

2.05EF07

2.07EF07

1.06EF06

8.97EF05

257,208

776,923

1668

3696

––

258,877

779,580

B10

37.90

0.86

0.87

0.83

0.05

0.03

1.66

1.21

1.97EF07

1.76EF07

7.39EF05

3.69EF05

67,914

347,581

909

1276

––

68,823

347,622

B13

37.91

0.69

0.69

0.57

0.05

0.02

1.68

1.11

1.98EF07

1.58EF07

7.32EF05

3.75EF05

25,692

39,347

1306

5454

––

26,997

39,893

B15

37.84

0.54

0.88

0.73

0.05

0.03

1.78

0.91

2.15EF07

1.64EF07

6.78EF05

3.03EF05

13,518

16,673

584

597

––

14,101

16,769

C1

35.07

3.10

6.16

7.37

0.08

0.07

n.a.

n.a.

n.a.

n.a.

n.a.

n.a.

1,216,258

2,073,804

17,500

18,344

11,030

2303

1,244,788

2,072,685

C4

37.85

0.92

1.18

1.20

0.07

0.04

2.42

2.43

1.62EF07

1.72EF07

1.39EF06

8.54EF05

85,207

161,058

4187

5396

3735

12,850

93,128

165,587

C7

38.29

0.49

0.80

0.94

0.06

0.03

1.71

1.20

1.29EF07

1.36EF07

1.13EF06

5.60EF05

38,155

83,549

3437

4339

1326

2165

42,918

85,125

C12

38.36

0.33

0.67

0.61

0.06

0.03

1.48

0.96

1.29EF07

1.44EF07

1.04EF06

4.83EF05

29,409

38,468

3065

3010

1038

1750

33,512

38,966

C14

38.40

0.32

0.68

0.94

0.05

0.02

1.32

0.81

n.a.

n.a.

n.a.

n.a.

35,426

46,091

3074

2980

1286

1769

39,786

46,036

C. Totti et al. / Science of the Total Environment 353 (2005) 204–217208

3. Results

3.1. Environmental parameters

A complete description of the physical and trophic

characteristics of the study area is reported in Russo et

al. (2005–this volume) and Degobbis et al. (2005–this

volume) while a synthetic characterisation of the sta-

tions is reported in Table 1. A strong trophic gradient,

decreasing from northwest to southeast, is evident. We

defined stations A3, B3, B6 and C1 as bwesternQ,stations A11, B15 and C14 as beasternQ and the remain-

ing ones as bcentralQ. The separation between the cen-

tral and western stations was made considering the

hydrological and trophic characteristics.

The phytoplankton community appears predictably

related with some environmental parameters, i.e. the

abundance of pico-, nanophytoplankton, dinoflagellates

and bothersQ was positively correlated with temperature

(P b0.01), while diatoms and dinoflagellates displayed

an inverse correlation with salinity (P b0.01).

Principal component analysis (PCA) was applied to

the whole data set (Fig. 2). The first component (PC1:

25% of total variance) gives evidence of the phyto-

plankton seasonal variability, related to the temperature,

indicating that all groups (diatoms excluded) reach their

maximum abundances in summer. The second compo-

nent (PC2: 20% of total variance) mainly represents the

effect of the riverine inputs, showing phytoplankton

abundance and nutrients opposed to salinity, and indi-

cating the effect of the western coastal front, which

separates high-nutrient/low-salinity coastal water

masses (with high phytoplankton abundances) from

high-salinity nutrient-poor offshore waters.

3.2. Picophytoplankton

Picophytoplankton abundances during study periods

ranged from 8.3�104 to 4.3�108 cells l�1, respective-

ly, at st. C7 (bottom) in November 2001, and st. A3

(surface) in September 2000, with a mean value of

2.6�107F3.4�107 cells l�1. Prokaryotic picophyto-

plankton (mainly represented by chroococcoid cyano-

bacteria, Synechococcus like) were 2 orders of

magnitude more abundant than eukaryotic picophyto-

plankton. Comparing the average picophytoplankton

abundance in different seasons, the highest abundances

were observed in the summer (P b0.0001), and the

lowest in winter (Fig. 3). In the summer of 2000,

which was a period of large mucilage aggregate ap-

pearance, picophytoplankton abundances were higher

than in any other periods (Table 3).

0.00E+00

1.00E+07

2.00E+07

3.00E+07

4.00E+07

5.00E+07

6.00E+07

7.00E+07

cells

l-1ce

lls l-1

pico

0.00E+00

5.00E+05

1.00E+06

1.50E+06

2.00E+06

2.50E+06

3.00E+06

Spr Sum Aut Win

Spr Sum Aut Win

nano

Western Central Eastern

Fig. 3. Seasonal distribution (cells l�1) of picophytoplankton (pico

and nanophytoplankton (nano) over the entire study period at the

western, central and eastern stations (meanFSE). Note the differen

scales in the y axis.

Factor 1 (25%)

Fac

tor

2 (2

0%)

TEMP

SAL

DIN

PO4SIO4

PICONANO

DIATO DINOOTH

-0.8

-0.6

-0.4

-0.2

0.0

0.2

0.4

0.6

0.8

-0.8 -0.6 -0.4 -0.2 0.0 0.2 0.4 0.6 0.8

Fig. 2. Loadings of environmental and biological variables of the first

two extracted components (PCA). TEMP: temperature; SAL: salinity;

DIN: Dissolved inorganic nitrogen; PO4: phosphate; SIO4: silicate;

PICO: picophytoplankton; NANO: nanophytoplankton; DIATO: dia-

toms; DINO: dinoflagellates; OTH: other microphytoplankton groups.

C. Totti et al. / Science of the Total Environment 353 (2005) 204–217 209

Spatial distribution of picophytoplankton showed a

marked north–south gradient (Table 1), with signifi-

cantly lower abundances in the southernmost transect

C than in transects B (P b0.01) and A (P b0.0001).

The west–east gradient was less marked (Table 1):

western stations showed significantly higher densities

than the other stations of the transects (P b0.0001). On

average, in transects A and B, central stations showed

the lowest values, while an increase was again observed

toward the eastern stations.

Considering the vertical distribution, on average,

picophytoplankton abundances at surface layer (3.05F4.67�107) were significantly higher than those at inter-

mediate layer (2.44F2.69�107, P b0.05) and bottom

(2.26F2.25�107, P b0.005). However, in transect B

and C, during June–July of 2000 and 2002, blooms of

picophytoplankton densities were often observed at the

bottom layer (Table 2).

3.3. Nanophytoplankton

Phototrophic nanoplankton ranged from 1.8�104 to

1.5�107 cells l�1, respectively, at st. A3 (bottom) in

July 1999 and st. A3 (surface) in June 2000, with a

mean value of 1.3�106F1.5�106 cells l�1. As a

general role, in all transects, nanophytoplankton assem-

blages were dominated by very small cells (e.g. 2–3 Amin size), followed by larger cells (e.g. 3–5 Am in size),

and by nanophytoplankton 5–20 Am in size. Although

nanophytoplankton could not be taxonomically deter-

mined using epifluorescence microscopy, some details

(such as cell shape, dimensions, chloroplast shape/num-

ber and flagella) indicate that the smallest cells were

mainly represented by prasinophytes, whereas, among

cells 3–5 Am in size prymnesiophytes were abundant;

moreover, larger nanophytoplankton (i.e. N5 Am) were

represented mainly by cryptophytes, small diatoms, and

dinoflagellates. Nevertheless, most of the cells were

taxonomically unclassified.

Significantly higher nanophytoplankton abundances

were observed in spring and summer (Fig. 3), while

lower values were observed in autumn (P b0.0001). On

average, nanophytoplankton densities observed during

year 2000 were higher than those observed in other

years, the lowest being observed in 2001 (P b0.01).

Spatial distribution of nanophytoplankton densities

(Table 1) showed, on average, significantly higher

abundances at transect A (P b0.0001). Considering

the west–east gradient, significantly higher values

were observed at western stations (P b0.0001), while

at the central stations minimum values were generally

observed. The vertical distribution (Table 2) revealed

that, on average, a decreasing gradient between the

surface (mean value 1.79F1.96�106 cells l�1) and

bottom (9.04F7.03�105 cells l�1) was present

(P b0.0001).

3.4. Microphytoplankton

The total microphytoplankton abundances ranged

from 0.4�103 to 14.4�106 cells l- 1, respectively at

st. B15 (surface) in August 2000 and B3 (surface) in

January 2001, with mean values of 2.2F8.5�105 cells

)

t

Table 2

Mean vertical distribution of pico-, nano- and microphytoplankton abundances (cells l�1FSE), in transects A, B, and C and at different seasons:

Sur (surface layer), Int (intermediate quotes); Bot (bottom)

Winter Spring Summer Autumn

AVG SE AVG SE AVG SE AVG SE

Transect A

Picophytoplankton

Sur 1.56EF07 1.33EF06 4.19EF07 7.27EF06 8.34EF07 9.55EF06 3.03EF07 7.57EF06

Int 1.66EF07 1.81EF06 3.56EF07 4.88EF06 5.49EF07 5.63EF06 2.52EF07 5.27EF06

Bot 1.57EF07 2.70EF06 1.86EF07 1.70EF06 3.97EF07 3.53EF06 1.27EF07 2.35EF06

Nanophytoplankton

Sur 2.32EF06 4.53EF05 3.50EF06 5.74EF05 3.47EF06 4.15EF05 1.38EF06 2.72EF05

Int 1.18EF06 2.55EF05 2.41EF06 4.37EF05 2.12EF06 2.44EF05 8.45EF05 1.70EF05

Bot 7.88EF05 1.16EF05 9.75EF06 1.89EF05 1.27EF06 1.59EF05 7.14EF05 1.36EF05

Microphytoplankton

Sur 314,808 104,829 254,236 101,606 458,090 106,732 374,575 147,412

Int 227,342 85,042 161,875 73,589 152,546 32,596 225,750 62,982

Bot 197,125 71,731 110,460 63,696 86,467 23,250 26,001 5253

Transect B

Picophytoplankton

Sur 1.32EF07 1.76EF06 1.09EF07 1.80EF06 2.72EF07 3.88EF06 2.75EF07 1.27EF07

Int 1.78EF07 2.70EF06 1.17EF07 1.21EF06 2.01EF07 1.65EF06 1.55EF07 2.40EF06

Bot 2.10EF07 3.07EF06 1.87EF07 2.68EF06 3.71EF07 2.93EF06 1.07EF07 2.10EF06

Nanophytoplankton

Sur 9.67EF05 1.11EF05 1.46EF06 2.52EF05 1.18EF06 1.26EF05 8.45EF05 8.04EF04

Int 7.81EF05 9.37EF04 8.59EF05 1.65EF05 8.11EF05 5.65EF04 548EF05 4.98EF04

Bot 7.76EF05 1.00EF05 9.03EF05 1.02EF05 1.03EF06 8.53EF04 3.83EF05 3.51EF04

Microphytoplankton

Sur 950,275 398,811 245,226 113,441 110,949 31,908 906,917 513,882

Int 136,733 83,666 25,359 8921 53,227 15,516 33,583 12,507

Bot 146,784 69,741 52,649 21,396 54,746 16,112 91,045 64,020

Transect C

Picophytoplankton

Sur 1.01EF07 1.85EF06 1.00EF07 2.10EF06 1.74EF07 2.01EF06 1.44EF07 2.64EF06

Int 1.17EF07 2.06EF06 1.17EF07 2.51EF06 1.68EF07 1.72EF06 1.28EF07 2.31EF06

Bot 1.20EF07 2.71EF06 7.38EF06 1.56EF06 2.19EF07 4.40EF06 3.58EF06 7.62EF05

Nanophytoplankton

Sur 1.19EF06 1.36EF05 1.89EF06 1.90EF05 1.59EF0 1.07EF05 1.34EF06 1.59EF05

Int 1.14EF06 1.06EF05 1.38EF06 1.08EF05 1.20EF06 1.06EF05 1.04EF06 1.49EF05

Bot 8.90EF05 1.00EF05 1.18EF06 1.93EF05 9.74EF05 7.93EF04 5.61EF05 7.08EF04

Microphytoplankton

Sur 697,878 305,095 29,839 184,231 124,403 49,603 570,031 291,413

Int 30,733 5361 82,056 32,176 28,980 5167 59,807 10,861

Bot 513,300 245,472 240,466 121,452 84,974 16,047 173,368 82,730

C. Totti et al. / Science of the Total Environment 353 (2005) 204–217210

l�1. Microphytoplankton abundance did not show any

significant differences among the sampling years

(MANOVA, ns). Mean abundances were significantly

higher in winter than in other seasons (P b0.0001),

with minimum values observed in summer.

However, the temporal trend differed markedly

among transects, as well as between western and east-

ern stations (Fig. 4). At the western stations, microphy-

toplankton maxima were always observed in winter

periods, while other peaks occurred in spring and au-

tumn. The latter showed height highly variable,

depending on the extension of diluted waters. At the

central and eastern stations, higher phytoplankton peaks

were observed in spring and autumn respectively. In the

eastern stations, summer peaks appeared, with higher

abundances in 2000 and 2001 than in 1999 and 2002.

Spatial distribution of microphytoplankton showed a

decreasing west-east gradient, with the highest densities

in the western stations of all three transects (Table 1;

P b0.0001). On average, microphytoplankton densities

did not exhibit a north–south gradient (MANOVA, ns),

as was observed for pico- and nanophytoplankton.

0.00E+00

5.00E+05

1.00E+06

1.50E+06 western

0.00E+00

5.00E+04

1.00E+05

1.50E+05central

0.00E+00

2.00E+04

4.00E+04

6.00E+04

8.00E+04eastern

Diato Dino Oth

cells

l-1ce

lls l-1

cells

l-1

Spr Sum Aut Win

Spr Sum Aut Win

Spr Sum Aut Win

Fig. 4. Seasonal distribution (cells l�1) of microphytoplankton over

the entire study period at the western, central and eastern stations

(meanFSE): Diato: diatoms, Dino: dinoflagellates, Oth: other micro-

phytoplankton groups. Note the different scales in the y axis.

C. Totti et al. / Science of the Total Environment 353 (2005) 204–217 211

Considering the vertical distribution, on average micro-

phytoplankton was significantly more abundant

(4.07F13.2�105 cells l�1) at surface layer (0–5 m)

than at other depths (P b0.01) (Table 2).

Microphytoplankton communities were dominated

by diatoms, while dinoflagellate abundance was 1–2

orders of magnitude lower. Peaks of the group bOthersQ

Table 3

Mean abundances and standard deviations (cells l�1) of phytoplankton size

study year, in all stations and depths: Pico: picophytoplankton; Nano: na

microphytoplankton groups; Total microphyto: total microphytoplankton

Year Pico Nano Diato

Avg. Std. Avg. Std. Avg.

1999 2.43EF07 1.83EF07 1.37EF06 6.44EF05 134,252

2000 4.59EF07 5.14EF07 2.22EF06 2.54EF06 136,917

2001 3.86EF07 4.22EF07 1.10EF06 8.66EF05 71,803

2002 3.75EF07 4.54EF07 1.24EF06 1.46EF06 100,829

appeared mainly in late summer and, to a lesser extent,

in spring. Abundances were significantly higher in the

transect C than in A and B (P b0.0001). The most

important species were Euglena sp., Syracosphaera

pulchra and Calciosolenia murrayi. Winter periods

were characterised by diatom blooms, mainly in the

western stations of all transects (generally with densi-

ties N106 cells l�1), regularly sustained by Skeletonema

marinoi (formerly S. costatum), which showed the

highest values between the end of January and Febru-

ary. Moreover, in winter 2002 we also observed a

diatom bloom due to Asterionellopsis glacialis, which

started in December and reached its maximum in Jan-

uary. Autumn peaks were generally observed at all

stations: dominating diatoms were Chaetoceros socialis

and other Chaetoceros species. Spring maxima were

generally due to Chaetoceros and Pseudo�nitzschia

species. Dinoflagellate increase was also observed in

autumn.

3.5. Summer phytoplankton communities

Comparing phytoplankton abundances in the sum-

mers of 2000 and 2002, when large mucilage aggre-

gates occurred, to those observed in the summers of

1999 and 2001, in which only early stages were ob-

served in the northern Adriatic Sea (marine snow,

macroflocs), higher values of autotrophic phytoplank-

ton were observed in 2000 and 2002 (Table 3), although

this increase was significant only for pico- (P b0.01)

and nanophytoplankton (P b0.0001). Among micro-

phytoplankton, only dinoflagellates exhibited signifi-

cantly higher abundances in dmucilageT summers than

in dnon mucilageT ones (P b0.001). In particular, sig-

nificantly lower dinoflagellate abundances were ob-

served in the summer 1999 than in other years. In

summer periods, all autotrophic components showed a

significantly decreasing north–south gradient, except

for microplanktonic dinoflagellates, which exhibited

the highest abundances along the transect C. Consider-

ing the vertical distribution during the summer period,

classes referred to summer periods (from June to September) of each

nophytoplankton; Diato: diatoms; Dino: dinoflagellates; Oth: other

Dino Oth Total microphyto

Std. Avg. Std. Avg. Std. Avg. Std.

375,149 1852 2099 986 3578 137,090 376,862

417,967 4273 8314 1349 5492 142,539 419,586

144,765 3033 5176 2455 11,004 77,291 147,753

232,237 4210 6874 661 2313 105,700 235,247

C. Totti et al. / Science of the Total Environment 353 (2005) 204–217212

significantly higher densities of picophytoplankton

were observed at the bottom, in transect B and C, in

comparison to the intermediate layer (transect B,

P b0.001) and to the surface and intermediate layers

(transect C, P b0.01). On the contrary, in transect A the

highest abundances were observed at surface.

The microphytoplankton composition during sum-

mer was characterized by a rich community of diatoms,

quite similar for all three transects, mainly represented

by Chaetoceros spp., Cerataulina pelagica, Pseudo-

Table 4

Result of 1-way MANOVA ( F-test and P) on microphytoplankton

species abundances (expressed as log cell density+1), between the

summers with (2000, 2002) and without (1999, 2001) the presence of

large aggregates

Taxa 1999, 2001 2000, 2002 F P

Asterionellopsis glacialis 2.83 4.29 0.92 N.S.

Bacteriastrum spp. 2.70 3.10 1.46 N.S.

Ceratium spp. 4.62 4.71 0.20 N.S.

Ceratium furca 1.44 2.27 6.72 *

Ceratium fusus 2.15 1.97 0.77 N.S.

Chaetoceros affinis 3.27 3.68 0.50 N.S.

Chaetoceros anastomosans 0.49 3.32 3.86 N.S.

Chaetoceros compressus 3.52 2.90 0.64 N.S.

Chaetoceros curvisetus 3.74 3.30 0.45 N.S.

Chaetoceros decipiens 3.01 3.02 0.00 N.S.

Chaetoceros insignis 2.16 3.11 3.04 N.S.

Chaetoceros lorenzianus 1.95 2.56 2.10 N.S.

Chaetoceros spp. 4.50 4.55 0.02 N.S.

Chaetoceros wighamii 0.00 3.37 1.77 N.S.

Cyclotella glomerata 0.00 3.10 2.00 N.S.

Cylindrotheca closterium 3.40 4.41 4.20 *

Dactyliosolen fragilissimus 4.00 3.96 0.02 N.S.

Dactyliosolen phuketensis 3.22 0.06 1.03 N.S.

Euglena spp. 1.57 2.22 2.42 N.S.

Gonyaulax fragilis 1.84 2.64 7.19 **

Guinardia flaccida 2.16 2.39 2.31 N.S.

Guinardia striata 3.25 2.33 6.92 **

Hemiaulus hauckii 2.16 2.54 8.70 **

Leptocylindrus danicus 3.06 3.51 1.08 N.S.

Leptocylindrus minimus 3.67 2.48 1.91 N.S.

Lioloma pacificum 1.68 0.00 2.93 N.S.

Oxytoxum spp. 2.31 2.97 5.83 *

Pleurosigma spp. 2.28 2.45 0.30 N.S.

Proboscia alata 3.16 3.08 0.43 N.S.

Prorocentrum compressum 1.42 2.05 0.93 N.S.

Prorocentrum micans 2.70 2.89 1.76 N.S.

Prorocentrum triestinum 2.16 1.93 0.57 N.S.

Pseudo-nitzschia dseriatacomplexT

0.42 2.87 3.87 N.S.

Pseudo-nitzschia

ddelicatissima complexT4.83 4.51 3.76 N.S.

Skeletonema marinoi 3.43 3.99 0.91 N.S.

Syracosphaera pulchra 3.03 2.56 4.92 *

Thalassionema frauenfeldii 2.59 2.72 0.13 N.S.

Thalassionema nitzschioides 3.60 3.48 0.19 N.S.

*P b0.05; **P b0.01. N.S., not significant.

nitzschia delicatissima, P. pseudodelicatissima, Cylin-

drotheca closterium and Dactyliosolen fragilissimus. In

this period, microplanktonic dinoflagellates reached

their annual maximum. Peaks were generally observed

in June, dominated by Prorocentrum micans and sev-

eral Oxytoxum spp., which were accompanied by other

species (at transect A Ceratium spp. and Dinophysis

spp., at transect B, Katodinium rotundatum and Toro-

dinium teredo, at transect C Dinophysis caudata).

No differences, in terms of species composition of

microphytoplankton, were observed among years with

mucilage occurrence and years without it. However,

some species displayed significantly higher abundances

in 2000 and 2002 (Table 4), and appeared to be char-

acteristic of mucilage periods (i.e. Cylindrotheca clos-

terium, Ceratium furca, Hemiaulus hauckii, Oxytoxum

spp. and Gonyaulax fragilis). On the contrary, the

coccolithophorid Syracophaera pulchra was signifi-

cantly less abundant in mucilage summers.

The microscopic examination of the aggregates

revealed a species composition comparable to that ob-

served in the water column samples, with a strong

enrichment of selected taxa, such as Cylindrotheca

closterium, Pseudo-nitzschia delicatissima, Gonyaulax

fragilis, Cyclotella sp., Cerataulina pelagica, Dacty-

liosolen fragilissimus. The relative importance of such

species showed some variations in relation to the station

where the aggregates were collected.

4. Discussion

The northern Adriatic basin is a highly complex

system, in which the spatial distribution and the sea-

sonal variability of phytoplankton are mainly driven by

the Po river discharge, coupled with the stratification/

mixing regime (Revelante and Gilmartin, 1976). Plank-

ton biomass typically shows a decreasing north–south/

west–east gradient (Fonda-Umani, 1996; Totti et al.,

1999), and the relative importance of the different

size classes varies according to the trophic gradient:

nano- and microphytoplankton tend to become domi-

nant in the coastal area, while nano- and picoplankton

dominate in the central part of the basin (Revelante and

Gilmartin, 1995; Heilmann and Richardson, 1999;

Vadrucci et al., 2002).

The subdivision of phytoplankton in the different

size classes (i.e. pico-, nano- and microphytoplankton)

is indeed an important tool which allows the interpre-

tation and explanation of many ecological responses,

such as the adaptability of phytoplankton to low or high

nutrient concentration, or the community structure in

different water column regimes (i.e. stratification or

C. Totti et al. / Science of the Total Environment 353 (2005) 204–217 213

mixing). However, this methodological approach may

be too simplistic and may hide other important infor-

mation such as the composition of the phytoplankton

assemblages, unless accompanied by taxonomical

observations. In fact, each size-class is extremely het-

erogeneous, which means that not only the size, but

also the taxonomic position contributes to significant

differences in abundances, as observed among the years

in the present study. On this point, there are several

other analyses which may be done, besides Utermohl

counting, to obtain additional information about size

class subdivision of phytoplankton (e.g. size-fraction-

ated HPLC chlorophyll analyses).

Autotrophic pico- and nanoplankton abundances

observed in this study fall within a range of values

previously reported for the northern Adriatic Sea

(Revelante and Gilmartin, 1988; Vanucci et al.,

1994; Del Negro et al., 1996; Fonda Umani et al.,

1999). Picophytoplankton abundance showed a

marked seasonality, with the highest abundances typ-

ically observed in summer, confirming previous obser-

vations (Kaltenbock and Herndl, 1992; Del Negro et

al., 1996; Vanucci et al., 1994). The high densities of

picoplankton observed in summer have been related to

their small dimensions, which influence the efficiency

of nutrient uptake in an oligotrophic environment.

Moreover, a seasonal response of cyanobacteria to

higher temperatures has also been reported (Whitton

and Potts, 1982).

Nanophytoplankton abundances were, on average,

almost one order of magnitude higher than those of

microphytoplankton, and the highest values were

recorded in spring–summer; moreover, nanophyto-

plankton assemblages were mainly represented by flag-

ellate forms (i.e. N80%). These findings are in

accordance with previous data on nanophytoplankton

(mostly derived from Utermohl counting) recorded in

the northern Adriatic Sea that show the nanoplankton

fraction as the most abundant of the phytoplankton

community all year around, with phytoflagellates repre-

senting the most important contributors to this fraction,

reaching higher densities in summer (Zoppini et al.,

1995; Totti et al., 2002a).

In the annual cycle of microphytoplankton, differ-

ent patterns have been recognized, depending on the

area. Winter bloom characterized the stations located

within the western coastal front of the northern Adria-

tic Sea, due to Skeletonema marinoi (formerly S.

costatum), a small colonial centric diatom with a

marked seasonal behaviour (Totti et al., 2002a; Ber-

nardi-Aubry et al., 2004). In January 2002, we ob-

served a delayed bloom of Asterionellopsis glacialis,

a seasonal diatom species which, since the early

1990s, has occurred typically in autumn after a period

of apparent disappearance from the plankton of the

northern Adriatic (Marzocchi et al., 1989; Totti et al.,

2002a). On the contrary, in the oligotrophic central

and eastern stations, the microphytoplankton followed

the seasonal trend generally observed in the open

middle Adriatic basin (Totti et al., 2000) and in the

Mediterranean Sea (Cushing, 1989), with two peaks

in spring and autumn. The occurrence of summer

peaks characterized mainly the eastern stations.

The autotrophic communities of the northern Adria-

tic Sea displayed significant differences, in terms of

abundances, between summer periods in which large

mucilage aggregates appeared and those in which the

phenomenon was observed only in its early phases (i.e.

occurrence of marine snow and macroflocs). Pico- and

nanophytoplankton, together with microplanktonic

dinoflagellates, had significantly higher densities in

dmucilageT summers, although a general increase in

density was observed even for diatoms. Summer

blooms of cyanobacteria have already been reported

during other mucilage episodes (Kaltenbock and

Herndl, 1992), and in the periods without the phenom-

enon (Vanucci et al., 1994). During the years of muci-

lage appearance, blooms of cyanobacteria were

observed under the pycnocline, at the bottom layer,

especially in transects B and C. The significantly higher

densities of picophytoplankton in ambient water during

dmucilageT summers would indicate that cyanobacteria

may enhance their growth rates in the presence of

mucus aggregates, beside fueling the mucoid matrix,

and thus supporting further aggregation of marine snow

(Kaltenbock and Herndl, 1992). The significantly

higher densities of nanophytoplankton found in

dmucilageT compared to dnon mucilageT summers are

likely to be associated with the increase in the avail-

ability of dissolved organic matter in the periods pre-

ceding mucilage appearance (Danovaro et al., 2005–

this volume). Mixotrophy, that is the capability of

autotrophic phytoplankton to exploit organic matter,

both via osmotrophic uptake and via phagocytosis, is

widespread in phytoplankton classes (Jones, 1994;

Raven, 1997). According to this criterion, most of the

nanophyplankton reported in this study can be consid-

ered mixotrophs, and an opportunistic behaviour of

nanoplanktonic assemblages able to acquire organic

nutrients during changes in the trophic conditions of

the system can be hypothesized (Lovejoy et al., 2000).

This hypothesis is further supported by results obtained

in a synoptic study, referred to the same campaign, but

limited to transect C and the years 1999 and 2000,

C. Totti et al. / Science of the Total Environment 353 (2005) 204–217214

where, besides nanophytoplankton, heterotrophic nano-

plankton and pico-eukaryotes were also investigated in

water samples (Vanucci, 2003). Nanophytoplankton

abundance exceeded that of heterotrophic nanoplankton

in both years and all year around (on average, by almost

one order of magnitude). The structure of these nano-

plankton assemblages was different from those reported

in other Mediterranean areas (e.g. in the oligotrophic

eastern Mediterranean Sea, Christaki et al., 1999; and in

the Aegean Sea, Mihalatou and Moustaka-Gouni,

2002). However, in addition to the significant increase

of nanophytoplankton, significant increases of both

heterotrophic nanoplankton and heterotrophic pico-

eukaryotes were found in the summer of 2000 with

respect to the summer of 1999. Moreover, the relative

increase observed in summer 2000 was higher for

heterotrophic than for autotrophic nanoplankton

(Vanucci, 2003). All these changes reflect modified

trophic pathways, which are able to optimise the ex-

ploitation of the available nutrient sources (Legendre

and Rassoulzadegan, 1995; Mousseau et al., 1996).

Simon et al. (2002), reviewing on microbial ecology

of organic aggregates in aquatic ecosystems, pointed

out that not only the aggregates but also their surround-

ings are sites and hot-spots of microbial processes, with

the plume of solutes leaking out of aggregates. There-

fore, it is likely that the increased enzymatic activity

during mucilage summers (Danovaro et al., 2005–this

volume) may enhance organic and inorganic matter

mobilization, which is successfully taken by phyto-

plankton capable of mixotrophy, thus contributing to

the growth of free-living microbial components.

Despite the higher densities observed in the sum-

mers of 2000 and 2002, the microphytoplankton popu-

lation in the water column, during mucilage

phenomena, was characterized by a species composi-

tion more or less comparable to that observed in sum-

mers when only early stages of the phenomenon

appeared. There are several recurrent taxa, which are

characteristic of the summer assemblages of the north-

ern Adriatic Sea, in the last 15 years, such as Ceratau-

lina pelagica, Chaetoceros spp., Pseudo-nitzschia

pseudodelicatissima, P. delicatissima, Dactyliosolen

fragilissimus, Prorocentrum micans and Cylindrotheca

closterium (Totti et al., 2002a; Bernardi-Aubry et al.,

2004). A few species appeared in the phytoplankton

community, with significantly higher densities in the

years 2000 and 2002, such as Hemiaulus hauckii, C.

closterium, Ceratium furca, Oxytoxum spp. and

Gonyaulax fragilis. The latter was observed with high

abundances in the water column only in the late spring–

summer periods of 2000 and 2002, and again with low

density in May–June 2001, otherwise it was never

observed during the study period. The possible involve-

ment of G. fragilis in mucus production has been

hypothesized by Pistocchi et al. (2005–this volume),

due to its very high concentrations in mucus aggregates,

and to the fact that this species may release high

amounts of extracellular polysaccharides under experi-

mental conditions (Pompei et al., 2003).

The phytoplankton assemblage in the mucilage

aggregates was comparable, in terms of species com-

position, to that observed in the surrounding water

column. Opportunistic species such as Cylindrotheca

closterium and Pseudo-nitzschia delicatissima reached

very high densities in the aggregates, probably benefit-

ing from the highly favourable microenvironment.

However, when comparing microbial assemblages of

aggregates with those of surrounding water, it should

be taken into account that a clear physical separation

between these two components, as they would be dis-

tinct compartments, is sometimes forced. In fact, when

water ambient is sampled using Niskin bottles, small

aggregates, microflocs, etc., which may be derived from

a partial break-up of mucilage aggregates, are sampled

with the surrounding water, affecting its analysis.

Phytoplankton assemblages associated to mucilage

aggregates differed in terms of the relative importance

of the species in all the reported episodes, and among

different areas as well. Pucher-Petkovic and Marasovic

(1987) reported several benthic diatoms as dominating

species in the aggregates during the episodes of 1983.

During phenomena of summer 1988, Honsell and Cab-

rini (1990) observed a rich diatom assemblage dominat-

ed by Pseudo-nitzschia spp. and Skeletonema costatum

and reported high amounts of Gonyaulax hyalina, a

species closely related to G. fragilis. In the very intense

episodes of 1989, dominating species in front of Seni-

gallia were Cerataulina pelagica, Leptocylindrus dani-

cus, Pseudo-nitzschia delicatissima, Cylindrotheca

closterium and G. fragilis (Totti et al., 1993), while in

the Gulf of Trieste Cabrini et al. (1992) reported Tha-

lassiosira sp., Pseudo-nitzschia sp., C. pelagica and L.

danicus. In the same period, Revelante and Gilmartin

(1991) observed high densities of Nitzschia longissima

and C. closterium in the aggregates in front of the Po

River delta. In the episodes of 1991, an almost mono-

specific population of C. closterium was observed in

aggregates originating from different areas of the Adria-

tic Sea (Pettine et al., 1993; Monti et al., 1993). Finally,

during the 1997 summer, Fornasiero (1998) found C.

pelagica, Dactyliosolen fragilissimus, Cyclotella sp.

and also benthic diatoms such as Nitzschia sigma,

Navicula spp. and Pleurosigma sp.

C. Totti et al. / Science of the Total Environment 353 (2005) 204–217 215

All these observations would indicate that the phy-

toplankton assemblages inhabiting the aggregates dis-

play high variability, as does any plankton population

in general, and have their own story and evolution as

do the phytoplankton of the surrounding water. Cylin-

drotheca closterium for example has been recognized

as a recurrent species appearing especially in aged

aggregates, often forming very dense and almost

monospecific populations. The aggregates represent a

microenvironment very suitable for the development

of a rich community of microorganisms (Simon et al.,

2002), which is separated from the surrounding water,

but which may interchange with it in terms of species

composition. A secondary development of diatoms in

the aggregates was already proposed by the bpioneerQscientists in the field (Steuer, 1903; Cori, 1905). The

presence of mucilage aggregates affects the composi-

tion of phytoplankton populations in the water col-

umn, even when aggregates are at early stages, and

there is a mutual connection between phytoplankton

and aggregates, i.e., several diatom and dinoflagellate

species may contribute to aggregate formation and

enlargement through the exudation process (Alldredge,

1999; Myklestad, 1995; MacKenzie et al., 2002), but

mucilage aggregates themselves may affect the phyto-

plankton populations, allowing the development of a

rich diatom community, as some phytoplankton spe-

cies take advantage of such peculiar and favourable

environment.

The composition of summer phytoplankton com-

munities observed during this study falls within a

more general change, which has occurred in the north-

ern Adriatic Sea since 1988. Historical data of phyto-

plankton time series of the northern Adriatic Sea (Totti

et al., 2002a) indicate a shift in the summer phyto-

plankton community from the decade 1978–1987, in

which dinoflagellate red tides were very common

(Regione Emilia Romagna, 1978-2003; Boni, 1983;

Boni et al., 1983; Artegiani et al., 1985; Pompei et

al., 1998; Totti et al., 1999) to the period 1988–2002

in which mucilage phenomena appeared, characterized

by a strong dominance of diatoms in summer, al-

though never reaching the level of blooms. This de-

cadal change also has a climatic match, as the

atmospheric pressure values in the January–March of

1988–2002 period were significantly higher than those

observed in the previous decade (Totti et al., 2002b),

and high pressure in winter has been significantly

correlated to mucilage occurrence and has been de-

scribed as one of the conditions necessary for the

mucilage phenomena (Crisciani et al., 1990), due to

its effect on water mass circulation.

Acknowledgements

The study was performed in the frame of the MAT

Project (Mucilages in the Adriatic and Tyrrhenian seas)

coordinated by Istituto Centrale per la Ricerca scienti-

fica e tecnologica Applicata al Mare (ICRAM) and

financed by the Italian Ministry of Environment.

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