www.cerf-jcr.org

Trophic Characterization of the Pelagic Ecosystem inVlora Bay (Albania)

Olga Mangoni{, Francesca Margiotta{, Maria Saggiomo{, Immacolata Santarpia{,Giorgio Budillon1, and Vincenzo Saggiomo*{

{Universita di Napoli Federico IIvia Mezzocannone 880134 Napoli, Italy

{Stazione Zoologica Anton DohrnVilla Comunale, 80121 Napoli, Italysaggiomo@szn.it

1Universita di Napoli ParthenopeCentro Direzionale, Isola C480143 Napoli, Italy

ABSTRACT

MANGONI, O.; MARGIOTTA, F.; SAGGIOMO, M.; SANTARPIA, I.; BUDILLON, G., and SAGGIOMO, V. 2011. Trophiccharacterization of the pelagic ecosystem in Vlora Bay (Albania). In: Tursi, A. and Corselli, C. (eds.), Coastal Research inAlbania: Vlora Gulf, Journal of Coastal Research, Special Issue No. 58, pp. 67–79. West Palm Beach (Florida), ISSN0749-0208.

Phytoplankton assemblages were studied to characterize the trophic status of the semienclosed Vlora Bay (Albania) andto evaluate the influence of terrestrial inputs on its pelagic ecosystem. The study was carried out as part of the EuropeanProject CISM (INTERREG IIIA Italy–Albania) and conducted during two oceanographic cruises (spring 2007, winter2008). The size-fractionated chlorophyll a concentrations, primary production rates, and the chemotaxonomiccomposition (high-performance liquid chromatography) of the phytoplankton assemblages were measured. The spatialvariability of primary production rates and chlorophyll a concentrations both showed a pronounced E-W gradient in thesurface layer, with the highest values along the eastern coast. In spring, a deep chlorophyll maximum was observed inthe central western part of the bay, whereas in winter a homogeneous vertical distribution was observed. Thephytoplankton assemblages were quite similar in both seasons and were dominated by the picophytoplankton fraction(<46% and 53% in spring and in winter, respectively). Haptophytes and pelagophytes were the major phytoplanktongroups, and accounted, respectively, for 50% and 15% in spring, and 40% and 25% in winter. The results showed thatVlora Bay was characterized by generally oligotrophic conditions and that the influence of the southern Adriatic openwaters was negligible. The trophic characteristics of the pelagic ecosystem of the bay were essentially driven byterrestrial inputs.

ADDITIONAL INDEX WORDS: Primary production, phytoplankton biomass size-fractions, HPLC pigment spectra.

INTRODUCTION

Knowledge of the structural and functional properties of

microalgal communities is essential for the evaluation of the

ecological consequences of human activities for the trophic

state of marine ecosystems. Many authors (Kiørboe, 1993;

Legendre and Le Fevre, 1991; Malone, 1980) have highlighted

the fact that the size structure of phytoplankton assemblages

is a crucial control factor in the functioning of pelagic food

webs, and consequently, it affects the rate of carbon export

from the upper ocean to deep layers. Strict relationships have

been observed between environmental conditions and phyto-

plankton communities; for example, phytoplankton commu-

nities respond to changes in the physical and chemical

properties of their environment by changing their taxonomic

composition and size structure (Platt et al., 2005).

In coastal areas, these relationships are even more evident

because of the extreme variability of physical and chemical

parameters, and the effects of human activities such as

urbanization and tourism. In areas like the coastal regions of

Albania, which are subject to drastic socioeconomic changes,

and consequently, to an increasing and uncontrolled exploi-

tation of aquatic ecosystems (Munari et al., 2010), the

assessment of the structure and productivity of phytoplank-

ton assemblages is a crucial issue. Such assessments,

however, regarding the Albanian marine coastal waters are

relatively scarce (Mangoni, Saggiomo and Santarpia, 2003;

Rubino et al., 2009; Saracino and Rubino, 2006).

Vlora Bay, Albania, is a good site to carry out these

assessments because it is a semienclosed bay with a densely

populated industrial city, Vlora (Cullaj, Lazo, and Baraj, 2004;

Cullaj et al., 2005). The bay is connected to the open southern

Adriatic Sea by a very shallow entrance (,40-m depth), and is

south of the mouth of the Vjosa River whose waters flow

southerly past the Narta Lagoon and into the bay (Pano et al.,

2006) (Figure 1). In addition, the bay is of paramount interest

to the Albanian fishing industry since it serves as a natural

nursery for many fish species of economic importance.

To our knowledge, there are no data available regarding

the phytoplankton assemblages and the productivity of Vlora

Bay. The present study was carried out as part of the

European Project CISM (INTERREG IIIA Italy–Albania),

which aims at producing a detailed characterization of the

Vlora Bay ecosystem. The aim of the present study was to

DOI:10.2112/SI_58_7 received and accepted in revision 12 April2010.

* Corresponding author.E Coastal Education & Research Foundation 2011

Journal of Coastal Research SI 58 67–79 West Palm Beach, Florida Winter 2011

evaluate the structure and productivity of the phytoplankton

assemblages in Vlora Bay to assess the trophic characteristics

of the bay on small temporal and spatial scales. In particular,

size-fractionated biomass, chemotaxonomic composition, and

size-fractionated primary production are discussed in relation

to the physical and chemical environmental conditions of the

bay.

MATERIALS AND METHODS

Two oceanographic cruises (CISM_1, CISM_2) were carried

out in the Vlora Bay in spring 2007 (May 26–31; CISM_1) and

in winter 2008 (January 19–22; CISM_2) on board the ship R/

V Universitatis. Eight transects (A–H) were performed on

each cruise (Figure 1): five transects (A, B, C, D, E) were

intercoastal between the Karaburun Peninsula and the

mainland; one transect (G) was between the Karaburun

Peninsula and Sazan Island; and two transects (F, H) were

between Sazan Island and the Narta Lagoon. Conductivity,

temperature, and depth (CTD) profiles were acquired at all 34

stations: vertical profiles of temperature, salinity, oxygen,

and fluorescence were acquired using a SBE 911 Plus CTD

probe equipped with a SBE oxygen sensor and a Chelsea

fluorometer. On CISM_1, 19 biological stations were sampled,

and on CISM_2, 13 biological stations were sampled. All

samples were collected using a SBE 32 Carousel equipped

with 12-L Niskin bottles having Teflon-coated springs. Each

sampling depth was chosen on the basis of fluorescence

profile and water column structure. At each biological station,

profiles of underwater Photosynthetically Available Radia-

tion (PAR) were obtained using a LI-COR quantum meter to

determine optical levels (model LI-192SA).

Samples for the determination of inorganic nutrient (NO2,

NO3, NH4, PO4, SiO4) concentrations were collected directly

from the Niskin bottles and immediately stored at 220uCuntil analysis. The analyses were performed using a FlowSys

Systea autoanalyzer, following the procedure described by

Hansen and Grassoff (1983). Five litres of seawater were then

drawn from each Niskin bottle and, after careful mixing,

subsamples were separated for size-fractionated chlorophyll a

(Chl a) and primary production, for pigment spectra (high-

performance liquid chromatography [HPLC]), for particulate

organic carbon (POC), and for total particulate nitrogen (PN)

determinations.

Phytoplankton biomass fractionation was performed fol-

lowing a protocol of serial filtration. One subsample was

collected on a Whatman GF/F filter (GF/F tot); two subsam-

ples were passed through a Nitex net (20 mm mesh size) or a

Nuclepore membrane (2 mm pore size) and then collected on

Whatman GF/F filters, having either GF/F , 20 mm, or GF/F

, 2 mm, respectively. Microphytoplankton Chl a concentra-

tion was obtained subtracting the GF/F , 20 mm from the GF/

F tot reading; nanophytoplankton concentration was obtained

by subtracting the GF/F , 2 mm from the GF/F , 20 mm

reading; and the picophytoplankton Chl a concentration

directly from the GF/F , 2 mm. Vacuum was , 0.2 atm for

all filtration procedures. Filters were stored in liquid nitrogen

until analysis. The analyses of size-fractionated Chl a and

phaeopigments (Phaeo) were carried out according to Jeffrey

and Humphrey (1975) using a SHIMADZU (mod. RF-5301PC)

spectrofluorometer.

The measurement of primary production was performed in

in situ-simulated conditions. For each sampling depth, a

sample was transferred to two light and one dark polycarbon-

ate 300-ml bottles, and then inoculated with 370 kBq (10 Ci) of

NaH14CO3 and incubated for 4 hours around midday. Surface

samples were incubated in running surface seawater, and

subsurface samples were incubated in circulated seawater

maintained at the same temperature recorded at the sampling

depth. Incubation light levels were obtained by means of

neutral light screens. After incubation, size fractions were

isolated by differential filtration of three 100-ml subsamples,

as those for Chl a. The filters were stored at 220uC until

analysis. In the laboratory, the filters were acidified with 200 ml

of 0.1 N HCL, and after adding 10 ml of Aquasol II scintillation

cocktail, were read with a Packard Tri-Carb (mod. 2100TR)

liquid scintillator. Daily production was estimated by multi-

plying the ratio between the whole-day irradiance and the

irradiance during the incubation period. The irradiance was

measured by means of a quantum meter LI-COR (model LI-

190SA) during the entire sampling period.

One or two liters of seawater were filtered on GF/F

Whatman filters (47-mm diameter) and stored in liquid

nitrogen for HPLC analyses. The analyses were performed

according to Vidussi et al. (1996) using a Hewlett Packard

HPLC (1100 Series). Calibration of the instrument was

carried out using external standard pigments provided by

the International Agency for 14C determination—VKI Water

Quality Institute. The following biomarker pigments were

used as chemotaxonomic descriptors: alloxanthin (crypto-

phytes), chlorophyll b (chlorophytes), prasinoxanthin (prasi-

Figure 1. Sampling stations in Vlora Bay (southern Adriatic Sea): square,

biological stations sampled during CISM_1 (spring 2007) and CISM_2

(winter 2008); circle, biological stations sampled during CISM_1 (spring

2007); pentagon, CTD profiles (see Materials and Methods).

68 Mangoni et al.

Journal of Coastal Research, Special Issue No. 58, 2011

nophytes), 199-butanoyloxyfucoxanthin (pelagophytes), fuco-

xanthin (diatoms), 199-hexanoyloxyfucoxanthin (hapto-

phytes), peridinin (dinophytes), zeaxanthin (cyanobacteria),

and divinyl Chl a (prochlorophytes). The contribution of the

main phytoplankton groups to the total Chl a was estimated

on the basis of the concentrations of biomarker pigments

using the chemical taxonomy software CHEMTAX (Mackey et

al., 1996).

Subsamples for the determination of POC and PN were

filtered on Whatman GF/F precombusted (450uC, 5 h) glass

fibre filters. The filters were immediately stored at 220uC.

The filters were exposed to HCl vapours to remove the

inorganic carbonate fraction, and then were analysed with a

Thermo Electron CHN elemental analyzer (FlashEA 1112

Series) (Hedges and Stern, 1984). Cyclohexanone-2,4-dinitro-

phenyl hydrazone was used as standard.

Phytoplankton composition from CHEMTAX was analyzed

using the Primer5 v 5.2.9 (Plymouth Marine Laboratory,

U.K.) software. A nonlinear multidimensional scaling (MDS)

analysis, on the basis of the Bray–Curtis similarity matrix,

was performed to determine the presence of a pattern in the

phytoplankton assemblages. Principal component analyses

(PCA) based on a correlation matrix were used to investigate

the relationship between in situ physical and chemical

parameters (salinity and nutrients) and biological features

(Chl a, size classes, total primary production, and particulate

N and C). All analyses were performed with STATISTICA 6.0

software.

RESULTS

During the spring cruise (CISM_1), weather conditions

were mainly characterized by the wind blowing from the

southeast, and quite variable cloud cover. The incident light

varied from 25.8 (on May 27) to 46.9 mol photons d21 (on May

30). During the winter cruise (CISM_2), the first sampling

days were characterized by good weather conditions, and on

the last day the sky was quite cloudy. The incident light was

19.5 mol photons d21 on January 20, 18.0 mol photons d21 on

January 21, and decreased to 12.4 mol photons d21 on

January 22.

Physicochemical Parameters

The vertical profiles of temperature and salinity are

reported in Figure 2. Higher variations of temperature and

salinity were observed in spring (temperature: 22.96–

14.99uC; salinity: 36.92 and 38.47) (Figures 2a and b), as

compared with winter (temperature: 15.05–13.80uC; salinity:

38.01–38.43) (Figures 2c and d). The spatial distributions of

temperature and salinity in spring and winter for the surface

and bottom layers are reported in Figure 3. An E-W gradient

of temperature and salinity was very evident during both

seasons. More specifically, during the spring the E-W surface

gradient was characterized by low salinity and warm water in

the eastern and central areas, and by high salinity and cold

water in the western area (Figures 3a and c). The distribution

of these variables in the bottom layer was strictly related to

bathymetry, i.e., the presence of open-sea waters was evident

only in the deepest part of the bay (Figures 3b and d). During

the winter, the presence of open-sea waters was evident only

at the surface of the western area. The gradients were less

pronounced, and the eastern area was occupied by colder

waters (Figures 3e and g).

During both seasons, the concentrations of NO3 and PO4

were low and, at times, near or below the detection limits,

especially in spring (Table 1). In spring the vertical distribu-

tion of NO3 showed high variability (,0.01 to 0.42 mmol dm23),

with the highest values in the bottom layer. In contrast, NH4,

SiO4, and PO4 did not show any vertical gradient. During

winter, the vertical distribution of all inorganic nutrients was

quite homogeneous. NO3 showed higher concentrations than

in spring, and varied from 0.07 to 0.65 mmol dm23. The PO4

concentrations were similar to those observed in spring (avg.

5 0.03 mmol dm23). The SiO4 concentrations were relatively

low (range 4.36–0.97 mmol dm23) and similar in both seasons.

The NH4 concentrations were quite high in spring, as high as

0.87 mmol dm23, whereas in winter the mean concentration

was only half of that measured in spring.

Biological Parameters

During spring, the mean Chl a value was 0.25 mg m23

(60.16), and the vertical profiles showed the presence of a

deep chlorophyll maximum (DCM) in the deepest part of the

Figure 2. Vertical profiles of temperature (uC) (a,c) and salinity (b,d) in

spring and in winter, respectively.

Trophic Characterization of Vlora Bay 69

Journal of Coastal Research, Special Issue No. 58, 2011

Fig

ure

3.

Sp

ati

al

dis

trib

uti

onat

surf

ace

an

din

the

bot

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layer

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mp

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(a,

b)

an

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(c,

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insp

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inte

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70 Mangoni et al.

Journal of Coastal Research, Special Issue No. 58, 2011

bay. During winter, the vertical distributions of phytoplank-

ton biomass were quite uniform (avg. 5 0.35 6 0.06 mg m23)

(Table 1; Figure 4). In spring, the surface spatial distribution

of Chl a showed high concentrations along the eastern coast of

the bay. In the bottom layer, the higher concentrations (max.:

0.84 mg m23, station C1, 248 m) were recorded in the deepest

part of the bay along the Karaburn Peninsula (Figures 5a and

b). In winter, the highest values of Chl a were recorded in the

eastern and central areas of the bay (Figures 5c and d). The

mean integrated values of Chl a were 11 and 13 mg m22 in

spring and in winter respectively.

The percentage contribution of different size classes to

phytoplankton biomass was quite similar in spring and

winter. There was an evident predominance of the picophy-

toplankton fraction of about 46% and 53% in spring and

winter, respectively. The mean contribution of the micro-

phytoplankton fraction was 12% (Table 1). During spring, an

anomalous high contribution (80%) of microphytoplankton

was observed in the bottom layer (248 m) of station C1. In

spring, the total phytoplankton biomass showed a good

correlation with the three size fractions (Figure 6a). Total

Chl a increase was mainly due to the increase of the

picofraction (slope 5 0.51; R 5 0.95, p , 0.001, n 5 58) and

the nanofraction (slope 5 0.33; R 5 0.89, p , 0.001, n 5 58),

and, to a lesser extent, to the increase of the microfraction

(slope 5 0.16; R 5 0.79, p , 0.001, n 5 58). In winter, the

nanofraction drove the biomass increase (slope 5 0.79; R 5

0.66, p , 0.001, n 5 31). No significant correlation was found

for the microphytoplankton (Figure 6b).

The results of CHEMTAX analyses showed that the

haptophytes were the major contributors to the biomass;

they accounted for 50% in spring and 38% in winter. The

results of the MDS analysis showed the presence of three

main groups. The winter samples were all very similar,

whereas the spring samples divided into two parts, separated

in the upper and deeper water layers, that is, above and below

the seasonal thermocline (Figure 7). The samples above the

thermocline showed a higher contribution of cyanobacteria

and diatoms (20% and 8%, respectively) and a lower

contribution of haptophytes (48%) and pelagophytes (12%)Table

1.

Ma

xim

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aver

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icro

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na

no

(20–2

mm),

an

dp

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(,2

mm),

an

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ary

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as

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ISM

_1in

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ISM

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win

ter)

.

NH

4

(mm

old

m2

3)

NO

2

(mm

old

m2

3)

NO

3

(mm

old

m2

3)

PO

4

(mm

old

m2

3)

SiO

4

(mm

old

m2

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TIN

(mm

old

m2

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Ch

la

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T

(mg

m2

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Ch

la

mic

ro(%

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Ch

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PP

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T

(mg

Cm

23

h2

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PP

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(%)

CIS

M_1

(sp

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Max

0.8

70.1

80.4

20.1

54.3

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480

75

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733

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CIS

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11

8Figure 4. Vertical profiles of mean chlorophyll a and standard deviation

(a) in spring and (b) in winter in all stations.

Trophic Characterization of Vlora Bay 71

Journal of Coastal Research, Special Issue No. 58, 2011

as compared with those collected below the thermocline

(Figures 8a and b). The bottom layer (248 m) of station C1

showed peculiar features: a noticeable presence of diatoms

that accounted for up to 32% of the total biomass. The winter

samples were characterized by a higher contribution of

pelagophytes (avg. 24%) and prochlorophytes (avg. 6%) than

the spring samples (Figure 8c).

During the spring the primary production values ranged

from 0.43 to 3.07 mg C m23 h21, and had a mean value of

1.14 mgC m23 h21. The mean contributions of micro-, nano-,

Figure 5. Spatial distribution of chlorophyll a (mg m23) at surface and in the bottom layer in spring (a, b) and in winter (c, d).

72 Mangoni et al.

Journal of Coastal Research, Special Issue No. 58, 2011

and picophytoplankton were 10%, 26%, and 64%, respectively

(Table 1). The daily mean integrated values of primary

production varied from 6.28 mg C m23 d21 (station C1, in

the western central area) to 20.14 mg C m23 d21 (station

D5, off the city of Vlora) (Figure 9a). The primary produc-

tion rates in winter were low and varied from 0.07 to

2.0 mg C m23 h21, and the percentage contribution of

picophytoplankton was up to 74% (Table 1). The mean

integrated values varied from 1.34 mg C m23 d21 ( station

B2, in the SW area) to 9.23 mg C m23 d21 (station D5, near the

city of Vlora) (Figure 9b). The mean values of daily integrated

primary production for the entire bay were 389 and

134 mg C m22 d21 in spring and in winter, respectively.

In spring, the production/biomass (P/B) ratio varied from

0.88 to 9.06 mg C m23 h21 (mg m23 Chl a)21 (avg. 5.1 6 1.9).

The highest P/B values (.6 mg C m23 h21 [mg m23 Chl a]21)

were recorded at stratified surface layer. Below the thermo-

cline (average available light ,50 mmol photons m22 s21) the

photosynthetic capacity showed a slight decrease (avg.

3 mg C m23 h21 [mg m23 Chl a]21). In winter, the P/B values

were lower than in spring, ranging between 0.25 and

4.90 mg C m23 h21 (mg m23 Chl a)21 (avg. 2.2 6 1.2). The

POC and PN values differed in spring and in winter. During

spring, a considerable spatial variability in the surface

distributions of particulate C (coefficient of variation [CV] 5

49%) and N (CV 5 57%) was observed. The highest values

were recorded in the northern part of the bay (transects D, E,

F, and G), reaching 196 mg m23 of POC at station F3 and

36.6 mg m23 of PN at station G3; the average concentrations

of POC and PN were 136.9 mg m23 and 20.9 mg m23,

respectively. Lower concentrations of POC and PN (avg. 59.6

and 7.6 mg m23, respectively) were observed at the southern-

most stations of the bay (transects A, B, and C). The C/Chl a

ratio showed the same spatial distribution as the one

observed for POC concentrations: higher values (avg. 747)

were found in the northern area as compared with the

southern (avg. 316). During winter, particulate matter had a

homogeneous distribution: the coefficients of variability were

half of those encountered in spring (CV for POC 5 29% and

for PN 5 25%). The mean concentrations were 46.3 mg m23of

POC and 7.5 mg m23 of PN. The C/Chl a were considerably

lower in winter (avg. 5 138) as compared with those observed

in spring.

DISCUSSION

The Adriatic Sea is composed of a wide variety of

ecosystems, from the eutrophic conditions in the northwest

to oligotrophic conditions in the southeast. The dynamics of

these ecosystems are driven by the interactions between the

sea hydrodynamics and the discharge of nutrient-rich waters

from several rivers entering the sea. The river inputs strongly

influence both the circulation and the biogeochemical pro-

cesses of the entire Adriatic Sea (Degobbis and Gilmartin,

1990; Polimene et al., 2006). In addition, the Vlora Bay,

because of its position in the southeastern Adriatic Sea, is

also influenced by the waters coming from the eastern

Mediterranean, one of the most oligotrophic areas of the

world’s oceans (Allen, Blackford and Radford, 1998; Rele-

vante and Gilmartin, 1995).

The highly variable temperatures and salinity values

observed during the spring highlighted the complexity of

the bay’s hydrology that is due to the morphology of the

bottom and to the influence of land runoff. The shallow depths

in the channels connecting the open Adriatic sea to the bay

reduce the exchange of subsurface waters (,40 m) with the

southern Adriatic Sea. This factor has a major impact on the

ecology of the coastal ecosystem of the bay. The open South

Adriatic waters were primarily important in the surface layer

of the western part of the bay, whereas the influence of land

runoff was important in the eastern part. As a consequence,

an E-W salinity gradient was observed in both seasons. In

winter it occurred despite the vertical mixing of the water

column.

During the spring, the phytoplankton biomass showed a

mean value of 0.25 mg m23 (a range that is typical of the

oligotrophic areas; e.g., Li et al., 1983; Yacobi et al., 1995), and

a DCM at the bottom of the deepest stations (.40 m). The

surface spatial distribution of the phytoplankton biomass and

the primary production showed a clear E-W gradient, with

the highest concentrations along the eastern coast, thus

emphasizing the role of terrestrial input from the city of Vlora

and from the Narta Lagoon. These distributions were

Figure 6. Correlation between total Chl a and micro-, nano-, and pico- Chl

a concentrations (a) in spring and (b) in winter, for all sampling depths.

Trophic Characterization of Vlora Bay 73

Journal of Coastal Research, Special Issue No. 58, 2011

consistent with the temperature and salinity gradients. In

addition, the low PO4 and NO3 concentrations, which were

often near or below the detection limit, indicated a condition

of nutrient depletion. This nutrient depletion could suggest

that our spring cruise took place after an algal bloom. This

hypothesis is partially confirmed by the relatively high

phaeopigment and NH4 concentrations that are indices of

senescence and of grazing activity. However, it cannot be

excluded that the NH4 concentrations were due, at least in

part, to terrestrial input, as suggested by the relatively high

SiO4 concentrations.

In winter, the vertical distribution of Chl a was mainly due

to the water column dynamics. The phytoplankton biomasses

were uniformly distributed along the water column because of

the column’s isopycnal characteristics. This type of distribu-

tion is typical of winter phytoplankton distribution in the

open sea at temperate latitudes. It is interesting to notice that

the primary production rate was lower in winter than in

spring even though the chlorophyll concentration was higher

in winter. It should be excluded that these low primary

production rates were due to nutrient limitation, since (a) the

mean NO3 concentration was higher in winter than in spring,

and (b) the mean concentrations of PO4 and SiO4 were the

same in both seasons. It could be hypothesized that the low

winter primary production rates were due to the shorter

winter days and to the low irradiance availability. In fact, in

winter, the average light available during the incubations

was 300 mmol photons m22 s21 at the surface, and decreased

rapidly in the deep layers (at 15 m of depth it had already

decreased to ,50 mmol photons m22 s21).

To our knowledge, the data of the present study are the

first data available regarding primary production rates in the

Vlora Bay. To have some terms of comparison our data are

discussed in relation to the data available from two previous

studies of primary production. The first was conducted at a

semienclosed bay, located in the central Adriatic Sea, similar

to Vlora Bay, namely, the Kastela Bay (Croatia). In addition,

Kastela Bay has an ecological context similar to Vlora Bay in

that it is characterized by nearby intensive industrialization

and urbanization and low exchange with open sea waters

(Marasovic et al., 2005; Sestanovic, Solic, and Krstulovic,

2009; Vukadin and Stojanoski, 2004). The second was

conducted in the open waters of the southern Adriatic Sea

(Civitarese and Gacic, 2001). To better compare our data with

those available for Kastela Bay and for the open waters of

central and southern Adriatic Sea we considered only the

Figure 7. MDS analysis performed on a matrix of similarity between samples in terms of phytoplankton groups as derived from CHEMTAX (spring samples

above [black circle] and below [grey circle] the thermocline; [white circle] winter samples).

74 Mangoni et al.

Journal of Coastal Research, Special Issue No. 58, 2011

primary production rates of the deeper stations, in which the

whole euphotic zone (1% of incident light) was covered.

The mean daily primary production rates in the euphotic

zone of the Vlora Bay in January and in May (186 and

508 mg C m22 d21, respectively) were sensibly lower than

those reported for Kastela Bay for the same months (550 and

850 mg C m22 d21, respectively). These Vlora Bay rates,

however, were similar to those measured in the open waters

outside of Kastela Bay, the central Adriatic Sea (200 and

400 mg C m22 d21, respectively) (Marasovic et al., 2005).

Civitarese and Gacic (2001) analysed several data sets and

calculated the new winter primary production derived from

nitrate depletion in the euphotic layer in the open waters of

the southern Adriatic Sea for the years 1987–1999. The

primary production ranged from 29 g C m22 in 1988 and 1989

to 10 g C m22 in 1998. The highest rates of new primary

production were in winter (February–March), when convec-

tive mixing transfers nutrients from the deep reservoir to the

surface. The authors hypothesized that the rates of new

production depend upon the year-to-year variability of local

climatic conditions. These conditions, in fact, determine the

magnitude of convective mixing, and consequently, the

amount of nutrients available for primary producers. As a

result, low values of primary production were recorded during

mild winters when the vertical mixing was negligible. Winter

2007 was also mild according to Bensi, Cardin, and Civitare

(2009), and they reported the absence of the vertical mixing in

the southern Adriatic Sea. Following the same line of

reasoning regarding our spring cruise of the same year

(CISM_1; May 26–31, 2007), we hypothesize that the offshore

waters of the southern Adriatic Sea did not play any role in

driving primary production in Vlora Bay. On the basis of our

observations, we assume vertical mixing was negligible

during winter 2007, and thus nutrient enrichment of the

euphotic layer was relatively scarce. The winter cruise

(CISM_2; January 19–22, 2008) was carried out in the

preconditioning phase of vertical mixing (Civitarese and

Gagic, 2001). Without new nutrient enrichment of the

euphotic layer, the role of open waters in the trophism of

the Vlora Bay was, again, negligible.

Similar to the study by Civitarese and Gacic (2001), the

study of Marasovic et al. (2005) also hypothesized that the

influence of the local climatic conditions, which are probably

related to global change, play an important role in determin-

ing primary production rates. Our data strongly suggest that

this hypothesize may also apply to the Vlora Bay. Pico- and

nanophytoplankton fractions, essentially haptophytes, were

dominant in both seasons; however, some differences were

observed. In spring, moving along the water column, there

was a slight shift in the prokaryote community: the

prochlorophytes, almost completely absent in the surface

layer, accounted for the 4% of phytoplankton biomass below

the seasonal thermocline, and the contribution of cyanobac-

teria decreased. A similar pattern of occurrence has been

Figure 8. Average contribution of different microalgal groups to phyto-

plankton assemblages as identified by the MDS analysis; (a) above and (b)

below the thermocline, in spring; (c) in winter.

Figure 9. Spatial distributions of mean integrated primary production

(mg C m23 d21), (a) in spring and (b) in winter.

Trophic Characterization of Vlora Bay 75

Journal of Coastal Research, Special Issue No. 58, 2011

reported in the Gulf of Naples (Casotti et al., 2000) as well as

in other ecological contexts (Ting et al., 2002; Worden, Nolan,

and Palenik, 2004). This distribution is partially explained by

the higher sensitivity of prochlorophytes to ultraviolet

radiation, as Sommaruga et al. (2005) demonstrated in a

series of experiments on picoplankton populations in Medi-

terranean coastal waters. The occurrence of prochlorophytes

in the winter assemblage seems to be a recurrent feature in

the distribution of this group in the Mediterranean Sea

(Marty et al., 2002; Vaulot et al., 1990). It is interesting to

note the peculiar feature of the bottom layer at station C1

(248m), where the microphytoplankton fraction accounted

for 79.5% and diatoms contributed more than 35% to the total

biomass. We hypothesize that the deep accumulation of

phytoplankton biomass is due, in part, to the formation of a

DCM constituted by haptophytes, and to low hydrodynamics

in the area that favour the sedimentation of upper-layer

microplanktonic diatoms.

The chemical and biological properties of the water column

were strongly influenced by water column dynamics: in

Figure 10. Results of PCA applied to physical, chemical, and biological parameters (a) above and (b) below the thermocline, in spring. See text for

abbreviations of the parameters included in the analysis.

76 Mangoni et al.

Journal of Coastal Research, Special Issue No. 58, 2011

spring the thermal stratification separated the surface waters

from the bottom layer, whereas in winter a quite uniform

vertical distribution was observed. To assess the relationships

between physical, chemical, and biological parameters under

various water column conditions, we performed three multi-

variate analyses (PCA) applied to salinity, nutrients (SiO4,

NO3, NH4, PO4), Chl a (total, micro-, nano-, picophytoplank-

ton fractions), particulate matter (POC, PN), and primary

production rate. In the first PCA we analyzed the spring

samples above the thermocline (Figure 10a). We found that

(a) salinity and silicate were opposed on the first axis; (b) low-

salinity stations were characterized by high primary produc-

tion and high concentrations of NO3, SiO4, and Chl a; and (c)

the northernmost stations (transects G, F, D) presented a W-

E gradient characterized by a decrease in particulate matter

and salinity toward the east. In the second PCA we analyzed

the spring samples below the thermocline (Figure 10b). We

found that: (a) the salinity and silicate were strongly

correlated to the first axis, which separated the stations in

function of depth (. or ,40 m); (b) depth characterized also

the second axis with higher biological activity and biomass

abundance of small phytoplankton (nano- and picofractions);

(c) the sample collected at 248m depth of station C1 is

separated from all the other samples because of high

concentrations of large phytoplankton as reported above.

The third PCA was applied to all the winter samples

(Figure 11). In this season salinity was opposed on the first

axis to the chemical (NO3, SiO4, PO4) and biological

properties (Chl a, primary production rates, POC, PN,

nanophytoplankton).

In synthesis, the mechanisms operating during the spring

that drive the primary production processes are different in

the surface waters and in the bottom layers. In the surface

waters, the terrestrial inputs play a key role in modulating

phytoplankton growth. The eastern part of the bay, charac-

terized by lower salinity and higher nutrient concentrations,

showed the higher rates of primary production and biomass.

In the bottom layers, a reverse scenario was found: the higher

salinities were associated with higher nutrient concentra-

tions, relatively high primary production rates occurred in

the high-salinity waters, and these rates increased with

depth. In particular in the deeper stations the formation and

maintenance of the DCM during spring and summer were

typical of temperate areas. We hypothesize that the higher

nutrient concentrations are a kind of nutricline generated by

in situ recycling or resuspension of nutrients from the

seafloor sediments. If this is the case, then the incident light,

rather than the nutrients, may limit the microalgal produc-

tion. In winter the gradients along the water column were

less pronounced, the higher production rates occurred at low

salinity and high nutrient levels, and terrestrial inputs in the

eastern area were observed in the surface waters, as they

were also observed to be in spring.

During spring, the distribution patterns of particulate

matter (C and N) appeared completely uncoupled from the

other biological features in the surface layer; the N-S gradient

was very pronounced compared with the E-W gradient

observed for the other chemical and biological parameters.

The considerable POC and PN concentrations and the high C/

Chl a ratios in the northern area of the bay suggest the

presence of terrestrial inputs probably related to discharge

from the city of Vlora or from the Narta Lagoon. In contrast,

in winter and in the bottom layer in spring, characterized by

low C/Chl a ratios, it can be hypothesized that the biological

properties were coupled and the predominant fraction of POC

was due to phytoplankton.

Figure 11. Results of PCA applied to physical, chemical, and biological parameters in winter. See Figure 10.

Trophic Characterization of Vlora Bay 77

Journal of Coastal Research, Special Issue No. 58, 2011

CONCLUSIONS

N In spring 2007 and in winter 2008, Vlora Bay was

characterized by generally oligotrophic conditions and

highly variable primary production processes.

N The influence of the open southern Adriatic waters on the

trophism of the bay was negligible, whereas the influence

of terrestrial inputs was very pronounced. The distribution

of biomass at surface clearly showed the role of terrestrial

discharges from the eastern coast in driving primary

production processes. The bay was divided in two sections

along a SE-NW direction: the lowest values of both

phytoplankton biomass and production were recorded in

the western area.

N The trophic state was driven by local hydrodynamic

conditions, terrestrial nutrient inputs, and biogeochemical

cycles that were all mainly confined within the bay.

ACKNOWLEDGMENTS

We express our gratitude to Prof. A. Tursi for having

invited us to join this project. We also thank Augusto

Passarelli and Ciro Chiaese for their technical and logistical

support.

We are grateful to C. Brunet and M. Modigh for con-

structive criticism regarding the manuscript.

LITERATURE CITED

Allen, J.; Blackford, J., and Radford, P., 1998. A 1-D verticallyresolved modelling study of the ecosystem dynamics of the Middleand Southern Adriatic Sea. Journal of Marine Systems, 18, 265–286.

Bensi, M.; Cardin, V., and Civitare, G., 2009. Seasonal variability ofhydrological properties in the southern Adriatic sea during theVECTOR project (cruises 2006–2008). II Workshop Vector, Rome,11p.

Casotti, R.; Brunet, C.; Arnone, B., and Ribera d’Alcala, M., 2000.Mesoscale features of phytoplankton and planktonic bacteria in acoastal areas induced by external water masses. Marine EcologyProgress Series, 195, 15–27.

Civitarese, G. and Gacic, M., 2001. Had the Eastern MediterraneanTransient an impact on the new production in the southernAdriatic? Geophysical Research Letters, 28(8), 1627–1630.

Cullaj, A.; Hasko, A.; Miho, A.; Schanz, F.; Brandl, H., and Bachofen,R., 2005. The quality of Albanian natural waters and the humanimpact. Environmental International, 31, 133–146.

Cullaj, A.; Lazo, P., and Baraj, B., 2004. Investigation of mercurycontamination in Vlora Bay (Albania). Materials and Geoenviron-ment, 51(1), 58–62.

Degobbis, D. and Gilmartin, M., 1990. Nitrogen, phosphorus andsilicon budgets for the Northern Adriatic Sea. Oceanologica Acta,13, 31–45.

Hansen, H.P. and Grasshoff, K., 1983. Automated chemical analysis.In: Grasshoff, K.; Ehrardt, M., and Kremlin, K. (eds.), Methods ofSeawater Analysis. Weinheim: Chemie, pp. 347–379.

Hedges, J.I. and Stern, J.H., 1984. Carbon and nitrogen determina-tion of carbonate-containing solids. Limnology and Oceanography29, 657–663.

Jeffrey, S.W. and Humphrey, G.F., 1975. New spectrophotometricequations for determining chlorophylls a, b, c1 and c2 in higherplants, algae and natural phytoplankton. Biochemie und Physiolo-gie der Pflanzen, 167, 191–194.

Kiørboe, T., 1993. Turbulence, phytoplankton cell size, and thestructure of pelagic food webs. Marine Biology, 29, 1–72.

Legendre, L. and Le Fevre, J., 1991. From individual plankton cells topelagic ecosystems and to global biogeochemical cycles. In: Demers,S. (ed.), Particle Analysis in Oceanography. Berlin: Springer-Verlag, pp. 261–300.

Li, W.K.W.; Subba Rao, D.V.; Harrison, W.G.; Smith, J.C.; Cullen,J.J.; Irwin, B., and Platt T., 1983. Autotrophic picoplankton in thetropical ocean. Science, 219, 292–295.

Mackey, M.D.; Mackey, D.J.; Higgins, H.W., and Wright, S.W., 1996.CHEMTAX—a program for estimating class abundances fromchemical markers—application to HPLC measurements of phyto-plankton. Marine Ecology Progress Series, 144, 265–283.

Malone, T.C., 1980. Algal size. In: Morris, I. (ed.), The PhysiologicalEcology of Phytoplankton. Oxford: Blackwell Scientific Publica-tions, pp. 433–463.

Mangoni, O.; Saggiomo, M., and Santarpia I., 2003. Il trofismodell’Adriatico meridionale: distribuzione quali-quantitativa deipopolamenti fitoplanctonici lungo le coste pugliesi ed albanesi.Biologi Italiani, Anno XXXIII 1, 46–51 [in Italian].

Marasovic, I.; Nincevic, Z.; Kuspilic, G.; Marinovic, S., and Marinov,S., 2005. Long-term changes of basic biological and chemicalparameters at two stations in the middle Adriatic. Journal of SeaResearch, 54, 3–14.

Marty, J.C.; Chiaverini, J.; Pizay, M.D., and Avril, B., 2002. Seasonaland interannual dynamics of nutrients and phytoplankton pig-ments in the western Mediterranean Sea at the DYFAMED time-series station (1991–1999). Deep Sea Research II, 49, 1965–1985.

Munari, C.; Tessari, U.; Rossi, R., and Mistri, M., 2010. The ecologicalstatus of Karavasta Lagoon (Albania): closing the stable door beforethe horse has bolted? Marine Environmental Research, 69, 10–17.

Pano, N.; Frasheri, A.; Simeoni, U., and Frasheri, N., 2006. Outlookon seawaters dynamics and geological setting factors for theAlbanian Adriatic coastline developments. Albanian Journal ofNatural and Technical Sciences, 19/20, 152–166.

Platt, T.; Bouman, H.A.; Devred, E.; Fuentes-Yaco, C., and Sathyn-dranatah, S., 2005. Physical forcing and phytoplankton distribu-tions. Scientia Marina, 69, 55–73.

Polimene, L.; Pinardi, N.; Zavatarelli, M., and Colella, S., 2006. TheAdriatic Sea ecosystem seasonal cycle: validation of a three-dimensional numerical model. Journal of Geophysical Research,111, C03S19, doi:10.1029/2005JC003260.

Revelante, N. and Gilmartin, M., 1995. The relative increase of largerphytoplankton in a subsurface chlorophyll maximum of thenorthern Adriatic Sea. Journal of Plankton Research, 17, 1535–1562.

Rubino, F.; Saracino, O.D.; Moscatello, S., and Belmonte, G., 2009. Anintegrated water/sediment approach to study plankton (a casestudy in southern Adriatic Sea). Journal of Marine Systems, 78(4),536–546.

Saracino, O.D. and Rubino, F., 2006. Phytoplankton composition anddistribution along the Albanian coast, South Adriatic Sea. NovaHedwigia, 83(1–2), 253–266.

Sestanovic, S.; Solic, M., and Krstulovic, N., 2009. The influence oforganic matter and phytoplankton pigments on the distribution ofbacteria in sediments of Kastela Bay (Adriatic Sea). ScientiaMarina, 73(1), 83–94.

Sommaruga, R.; Hofer, J.S.; Alonso-Saez, L., and Gasol, J.M., 2005.Differential sunlight sensitivity of picophytoplankton from surfaceMediterranean coastal waters. Applied and Environmental Micro-biology, 71(4), 2154–2157.

Ting, C.S.; Rocap, G.; King, J., and Chisholm, S.W., 2002. Cyano-bacterial photosynthesis in the oceans: the origins and significanceof divergent light-harvesting strategies. Trends in Microbiology,10(3), 134–142.

Vaulot, D.; Partenski, F.; Neveux, J.; Mantoura, R.F.C., andLlewellyn, C.A., 1990. Winter presence of prochlorophytes insurface waters of the northern western Mediterranean Sea.Limnology and Oceanography, 35, 1156–1164.

Vidussi, F.; Claustre, H.; Bustillos-Guzman, J.; Cailliau, C., andMarty, J.C., 1996. Determination of chlorophylls and carotenoids ofmarine phytoplankton: separation of chlorophyll a from divinyl-chlorophyll a and zeaxanthin from lutein. Journal of PlanktonResearch, 18, 2377–2382.

78 Mangoni et al.

Journal of Coastal Research, Special Issue No. 58, 2011

Vukadin, I. and Stojanoski, L., 2004. Present water quality of KastelaBay (Adriatic Sea) and some proposals for its protection andimprovement. In: Briand, F. (ed.), Rapport du 37e Congres de laCommission Internationale pour l’Exploration Scientifique de lamer Mediterranee, Monaco: CIESM, 253p.

Worden, A.Z.; Nolan, J.K., and Palenik, B., 2004. Assessing thedynamics and ecology of marine picophytoplankton: the importance

of the eukaryotic component. Limnology and Oceanography. 49(1),168–179.

Yacobi, Y.Z.; Zohary, T.; Kress, N.; Hecht, A.; Robarts, R.D.; Waiser,M.; Wood, A.M., and Li, W.K.W., 1995. Chlorophyll distributionthroughout the southeastern Mediterranean in relation to thephysical structure of the water mass. Journal of Marine Systems, 6,179–189.

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