Spreading and autoecology of the invasive species Gracilaria vermiculophylla (Gracilariales, Rhodophyta) in the lagoons of the north-western Adriatic Sea (Mediterranean Sea, Italy)

Estuarine, Coastal and Shelf Science 114 (2012) 192e198

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Spreading and autoecology of the invasive species Gracilaria vermiculophylla (Gracilariales, Rhodophyta) in the lagoons of the north-western Adriatic Sea (Mediterranean Sea, Italy) A. Sfriso a, *, M.A. Wolf b, S. Maistro b, K. Sciuto b, I. Moro b a b

Department of Environmental Sciences, Informatics & Statistics, University of Venice, Calle Larga, Santa Marta 2137, 30123 Venice, Italy Department of Biology, University of Padua, Via Ugo Bassi 58b, I-35131 Padua, Italy

a r t i c l e i n f o

a b s t r a c t

Article history: Received 4 April 2012 Accepted 25 July 2012 Available online 3 September 2012

Gracilaria vermiculophylla (Ohmi) Papenfuss, an invasive Rhodophyta recently recorded in the Po Delta lagoons (May 2008), was also found in the Venice lagoon in March 2009 and successively in Pialassa della Baiona (EmiliaeRomagna Region) in May 2009. The species has colonized the eutrophic and confined areas of Venice by pleustophytic tangled populations (5e15 kg fwt m
2), replacing the allochthonous species whereas it is absent in the areas characterized by low nutrient availability and high water exchange. In contrast, in the Po Delta lagoons and in Pialassa della Baiona it is present everywhere, also with high water renewal, because of the eutrophication caused by the Po river and the industrial area of Ravenna. This study presents the autoecology and distribution of G. vermiculophylla in the above environments, according to their different eutrophication status, showing its relationship with physicochemical parameters and nutrient concentrations in water column, pore-water, surface sediments and particulate matter collected by traps in a station of the Venice lagoon (Teneri) sampled monthly during one year. Furthermore, we give new information on its morphology and the high dimorphism between female and male gametophytes and tetrasporophytes. Ó 2012 Elsevier Ltd. All rights reserved.

Keywords: introduced species macroalgae Gracilaria vermiculophylla Venice lagoon eutrophication autoecology

1. Introduction The Venice lagoon is one of the Mediterranean transitional environments considered to be a prime area for the introduction of alien species, especially macrophytes (Verlaque,1994; Boudouresque and Verlaque, 2002; Occhipinti-Ambrogi, 2002; Sfriso and Curiel, 2007). A revision of the allochthonous species, updated December 2010 (Zenetos et al., 2010), shows that there are 33 non-indigenous species (NIS) of macroalgae recorded in the Venice lagoon, ca. 80% of the number (49 taxa) recorded in the Adriatic Sea and 39% of those (125 taxa) found in the whole Mediterranean Sea. Among them some are considered invasive or potentially invasive: i.e. Codium fragile subsp. fragile (Suringar) Hariot (Sfriso, 1987), Sargassum muticum (Yendo) Fensholt (Gargiulo et al., 1992), Grateloupia turuturu Yamada (Tolomio, 1993, as Grateloupia doryphora (Montagne) M.A. Howe), Undaria pinnatifida (Harvey) Suringar (Rismondo et al., 1993), Heterosiphonia japonica Yendo (Sfriso et al., 2002) and Gracilaria vermiculophylla (Ohmi) Papenfuss (Sfriso et al., 2010a) due to their worldwide spread, but some of them have spread largely only in the * Corresponding author. E-mail address: [email protected] (A. Sfriso). 0272-7714/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ecss.2012.07.024

lagoons of the North Adriatic and particularly in the Venice lagoon: i.e. Sargassum muticum, U. pinnatifida and G. vermiculophylla. Other NIS, such as Agardhiella subulata (C. Agardh) Kraft & M.J. Wynne and Solieria filiformis (Kützing) P.W. Gabrielson are highly invasive, but only in our lagoons. Gracilaria vermiculophylla, a species native from Japan and Korea, is the most recent introduced species (Sfriso et al., 2010a). It was firstly recorded in the northern coasts of the Atlantic Sea in 2002 (Rueness, 2005; Thomsen et al., 2007) and has rapidly colonized many European coasts and the transitional systems of the Adriatic Sea. The first record in the Venice lagoon was in March 2009, but in the following months many populations were recorded both in the central and southern basins (Sfriso et al., 2011). In May 2009, high biomasses (5e15 kg fwt m
2) of this species were also found at Pialassa della Baiona (Ravenna), where G. vermiculophylla covered a large part of the southern basin. This paper maps the presence of this species (Venice lagoon, transitional systems of the Po Delta and Pialassa della Baiona) and analyses the different morphology of non-reproductive and reproductive thalli and their correlation with some physico-chemical parameters and nutrient concentrations in water column, porewater, surface sediments and particulate matter collected by traps.

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2. Materials and methods 2.1. Sampling areas Samples were collected during national and regional programmes carried out in order to monitor the ecological status of the Italian transitional environments according to the requirements of the European Water Framework Directive (2000/60/EC) for the “Macrophytes” biological element (macroalgae and aquatic angiosperms). The Po Delta lagoons were monitored in 2008, 2009, 2010 in late spring and autumn of each year (Sfriso, 2010, 2011; Sfriso et al., 2011 and references therein). Pialassa della Baiona was sampled in the same seasons in 2009 whereas macrophytes have been recorded in Venice lagoon also in other periods, within both the European WFD and the study of alien species since 2008. Gracilaria vermiculophylla was collected monthly in one locality of the Venice lagoon (Teneri) during one year (March 2010e February, 2011) in order to assess the seasonal changes affecting biomass and cover percentage and the relationships with the main environmental parameters. Fig. 1 shows the lagoon sites where G. vermiculophylla was recorded. 2.1.1. Venice lagoon The Venice lagoon (45 340 e45120 N; 12 090 e12 360 E) is the largest transitional system of the Mediterranean Sea. It is subdivided into 4 basins connected to the sea by three large (400e 900 m) and deep (10e20 up to 50 m) port-entrances (Lido, Malamocco and Chioggia). The total surface is of ca. 549 km2, of which ca. 432 km2 are exposed to the tidal ranges. On average the mean depth is ca. 1 m, but deep canals (>5 m) occupy ca. 5% of its surface. Water exchange with the sea is high and ca. 60% of the water is renewed on any tidal cycle (12 h). The lagoon presents a range of morphological and physico-chemical characteristics that favour the growth of a rich flora (Sfriso and Curiel, 2007) composed of wide meadows of aquatic angiosperms and beds of macroalgae (Sfriso and Facca, 2007). 2.1.2. Po Delta lagoons The Delta of the Po river (45 080 e44 480 N; 12160 e12 340 E) is composed of many small basins covering a surface of ca. 200 km2,

193

out of them ca. 100 km2 are open to the tidal ranges. The mean depth of some of the basins ranges between 0.5 and 1 m: Barbamarco, Caleri, Canarin, Marinetta, Vallona and 2e3 m: Goro and Scardovari. The last two exhibit a high water exchange because of their large sea inlet. The others show both confined and highly renewed areas. All exhibit high trophic levels and turbidity. No aquatic angiosperms are present, the flora is scarce and dominated by opportunistic species, especially Gracilariaceae, Solieriaceae and Ulvaceae. 2.1.3. Pialassa della Baiona Pialassa della Baiona (44 310 e44 280 N; 12140 e12160 E) is a small shallow basin located to the South of the Po Delta near the port of Ravenna in the EmiliaeRomagna Region. Its surface is only ca. 10 km2 and its depth ranges between 0.6 and 1.4 m. In the southern part of the lagoon water exchange with the sea is high because of the presence of many small (10e20 m wide) artificial canals which are ca. 3e6 m deep, whereas in the north it is more reduced. Nutrients are relatively high but their concentration is strongly influenced by the seasonal production of high biomasses of Gracilariaceae and Ulvaceae that hamper sediment resuspension thus producing clear waters. Because it lacks artificial hard substrata, such as the ones that characterize the Venice lagoon, marine algae are rare and mostly present under a pleustophytic form, similarly to the ones in the Po Delta. 2.2. Sampling procedures The presence/absence of Gracilaria vermiculophylla during the spring and autumn macroalgal sampling was determined by testing the bottom surface with a rake (20 sub-samples at each sampling site). This procedure also allows the coverage of each species to be determined with an accuracy of >95%. The population was monthly sampled in 2009e2010 at Teneri (Venice lagoon) by means of an aluminium box of 71  71 cm (0.5 m2) repeatedly plunged in an area of 15  15 m, according to the procedure set up by Sfriso et al. (1991) to determine the algal pleustophytic biomass on soft substrata in transitional systems. The biomass weight was the mean of 3e6 subsamples according to the algal abundance in order to obtain a measurement accuracy of 95%. Samples were preserved in 4% formaldehyde neutralized with hexamethylenetetramine up to

Fig. 1. Maps of the lagoon of Venice, Pialassa della Baiona and Po Delta transitional systems with indication of the Gracilaria vermiculophylla presence.

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laboratory identification by means of a stereo zoom microscope E1654ZT45 (Euromex microscopes, Holland) and a light microscope353Ph (Optika microscopes, Italy). 2.3. Environmental parameters During the biomass sampling the standard physico-chemical parameters (temperature, salinity, pH, redox-potential, underwater light transmission, dissolved oxygen, suspended particulate matter, sediment grain-size, sediment density and nutrient concentrations in water column, pore-water and surface sediments) were also recorded. Sampling methodologies are reported in Sfriso and Marcomini (1997) and Sfriso et al. (2003). 3. Results 3.1. Morphology Thalli of Gracilaria vermiculophylla are blackish to dark-red and for this reason they could be easily recognized. In Venice this species is called the “black Gracilaria” (Fig. 2A, B). Axes, arising from a small basal disk, are cylindrical to slightly compressed, irregularly and densely branched (Fig. 2C), wrinkled and very long: <0.5e1.0 (2.0) m high, especially female gametophytes. Usually axes are larger in the central region where they can reach 1.5e3 mm in diameter and show long longitudinal grooves. The diameter of ultimate branches decreases suddenly and they become very thin,

almost capillary-like. Female and male gametophytes and tetrasporophytes show different morphological features. Female gametophytes are poorly branched, strongly wrinkled and very thick in the lower portion; axes up to 2e3 (4) mm in diameter. In contrast, male gametophytes, like tetrasporophytes, have a dense branching pattern. Fertile male gametophytes exhibit a pale colour due to the presence of numerous conceptacles visible as pale elliptical spots on the thallus surface. In cross-section, axes are hollow except for the upper branches (Fig. 2E) and this gives them an elastic consistency. An outer layer of pigmented cortical cells, radially elongated of (3) 4e7  8e12 (15) mm (Fig. 2F), covers 1e2 layers of irregular rounded weakly pigmented cells, the diameter of which increases towards the inside. In the thinner branches some layers of large and colourless medullary cells follow the pigmented cells and show a bigger diameter. In contrast, thicker filaments are hollow. Medullary cells have a characteristic colourless wall, 10e20 mm thick (Fig. 2G, H), with numerous secondary pit-connections (Fig. 2I). Cells have small spherical green rhodoplasts, 2e3 mm in diameter. The life cycle is that of the genus Gracilaria: diplohaplontic and isomorphic with alternance of a tetrasporophyte and gametophytes. In the male gametophyte, spermatangia are produced in “verrucosa-type” conceptacles, 40e100 (125) mm long in surface view and 60e75 mm broad and up to 100e135 mm deep in cross-section (Fig. 3A, B, C). Female gametophytes have been found only in the Po Delta. Cystocarps are hemispherical without basal constriction, 0.7e 0.9 mm high and 0.8e1.3 mm in diameter, and are irregularly

Fig. 2. Thalli of Gracilaria vermiculophylla. A) Tangled population in turbid and eutrophic waters. B) Comparison of the black colour of this species with the red thalli of Gracilariopsis longissima; scale bar e 5 cm. C) Morphology of a non-reproductive thallus; scale bar e 5 cm. D) Cross-section of the apical region of a thallus filled of medullary cells; scale bar e 100 mm. E) Cross-section of the hollow median region of a thallus with highlight on the deep longitudinal grooves; scale bar e 500 mm. F) Cross-section of a thallus with highlight on cortical cells; scale bar e 10 mm. G, H) Detail of the medullary cells and the thick colourless walls; scale bar e 50 mm. I) Detail of a secondary pit-connection between two medullary cells; scale bar 25 mm.

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Fig. 3. Reproductive structures of G. vermiculophylla. A, B) Male conceptacles in surface view and in cross-section: scale bar e 150 mm. C) “Verrucosa-type” male conceptacles immersed in the cortical layer; scale bar e 30 mm. B) Female gametophyte with many cystocarps; scale bar e 1 cm. E) Detail of cystocarps; scale bar e 2 mm. F) Cross-section of a cystocarp. Highlight on the apparent absence of traversing nutritive cells; scale bar e 100 mm. G) Tetrasporangia immersed in the cortical layer; scale bar e 30 mm.

arranged all around the filaments (Fig. 3D, E). Traversing nutritive cells between the gonimoblast and the pericarp, which is one of the distinctive characters of the genus Gracilaria, were not observed in our samples (Fig. 3F). The rarity of such cells was already mentioned by Thomsen et al. (2005) for this species. Carposporangia are clavate to elongated-ovoid, 20e25 mm in diameter. Tetrasporophytes are morphologically similar to male gametophytes. Tetrasporangia, 20e30 mm in diameter, 20e40 (50) mm long and cruciately divided, are scattered in the cortex all around the filaments (Fig. 3G, H, I). 3.2. Species distribution The first record of this species in the Mediterranean Sea was in the Po Delta lagoons in May 2008 (Sfriso et al., 2010b). Later Gracilaria vermiculophylla was also recorded in Venice lagoon (March 2009) and in some transitional systems of the EmiliaeRomagna Region: Sacca di Goro and Pialassa della Baiona (May 2009). 3.2.1. EmiliaeRomagna Region Gracilaria vermiculophylla, recorded almost everywhere at Sacca di Goro and Pialassa della Baiona (Fig. 1), forms dense and continuous pleustophytic populations reaching up to 15 kg fwt m
2 that overcome and replace all the other species, including Ulvaceae and other Gracilariaceae. No fertile female gametophytes were found in those lagoons. Until 2004 no sample of G. vermiculophylla was found in Sacca di Goro. In fact, at the time, among the 9 recorded

taxa the dominant ones were Gracilaria gracilis (Stackhouse) Steentoft, Irvine et Farnham and some laminar and filamentous Chlorophyta: Ulva rigida C. Agardh, Chaetomorpha ligustica (Kützing) Kützing and Ulva flexuosa Wulfen subsp. pilifera (Kützing) Wynne (Sfriso, 2010). 3.2.2. Venice lagoon Sampling campaigns, carried out at ca. 150 stations spread over the whole Venice lagoon between 2009 and 2011, showed that Gracilaria vermiculophylla has colonized only eutrophic and confined areas, particularly in the southern and central basins, whereas it lacks where water renewal is high (Fig. 1). The highest biomasses have been recorded in the tidal lands of the central lagoon where that species is absolutely dominant, reaching up to 12 kg fwt m
2, and growing associated to Ulva rigida, Gracilaria gracilis or Gracilariopsis longissima (S.G. Gmelin) Steentoft et al. In these areas, the environmental conditions are similar to those recorded in Pialassa della Baiona and in the lagoons of the Po Delta (Sfriso et al., 2010b): the grain-size of the surface sediment is fine and nutrient concentrations are high both in waters and surface sediments. The biomass and coverage of Gracilaria vermiculophylla, monitored with a monthly frequency during March 2010eFebruary 2011 together with some environmental parameters at Teneri in the confined area of the Venice lagoon (Fig. 1, Table 1) can supply information on the environmental requirements of the species. Some populations of Gracilaria vermiculophylla have also been recorded in the watershed of Lido Island with biomasses up to

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Table 1 Annual mean, standard deviation (Std), maximum (Max) and minimum (Min) values of biomass and percentage cover of G. vermiculophylla, and of environmental parameters at Teneri (Venice lagoon) during 2009. Water column Twater  C

G. vermiculophylla
2

Biomass kg fwt m

Coverage %

pH Water

Eh Sed.

Water

DO %

Salinity psu

Light at bottom %

FPM g L
1

150 44 205 78

24.2 2.6 27.3 17.6

40 8 57 22

32.3 10.4 54.2 20.6

Sed.

Mv Mean Std Max Min

2.27 2.13 6.53 0.30

72 24 100 23

16.4 9.0 28.1 4.10

8.31 0.22 8.66 8.00

7.56 0.27 7.95 7.10

248 42 322 189


194 59
49
254

Water column Chl-a

Pore-water (5 cm top layer)

Phaeo-a mg L
1

Tot

NO
2

NO
3

NHþ 4

DIN

RP

Si

mM Mean Std Max Min

1.90 1.70 5.81 0.60

1.03 1.00 3.44 0.01

2.93 2.44 9.25 0.84

1.91 1.30 5.77 0.92

NHþ 4

NOx

DIN

RP

4433 2432 8316 1276

141 65 278 67

mM dm3 of sediment 15.1 8.01 34.1 2.42

13.4 4.80 19.1 3.20

30.5 8.92 49.0 19.2

0.71 0.25 1.15 0.40

11.5 8.29 29.8 1.92

4351 2430 8252 1183

82 47 173 13

Surface sediment (5 cm top layer) Fine <63 mm %

Dry density g dwt cm3

Carbon Total

Inorg mg g

Mean Std Max Min

96 3 99 89

0.61 0.03 0.65 0.57

80.9 4.36 90.3 76.3

Org

Nitrogen

Phosphorus

Total mg g
1

Total


1

68.5 8.81 76.5 52.2

Inorg

Org

Porg/ptot %

0.34 0.03 0.37 0.28

0.23 0.04 0.30 0.15

40 5 51 31


1

mg g 12.4 9.33 34.2 2.98

3.41 0.52 4.02 2.60

0.57 0.03 0.60 0.50

3e5 kg fwt m
2. Finally, occasional thalli have been sampled in two sites of the northern lagoon (Fig. 1), however in those areas the biomass was negligible. No samples have been recorded in the watershed of Pellestrina island and in the distal region of the northern lagoon. 3.3. Relationship with environmental parameters in Teneri station At Teneri Gracilaria vermiculophylla was present during the whole year (Fig. 4). The mean biomass was 2.27  2.13 kg fwt m
2, ranging from 0.3 kg fwt m
2 in February to 6.53 kg fwt m
2 in June. The highest biomass recorded in June was followed by a rapid biomass collapse to 0.5 kg fwt m
2 in July during a hypoxic period, then in August it increased again in the presence of improved environmental conditions. That confined area is characterized by high fluctuations of physico-chemical parameters and high concentrations of nutrients, especially in pore-water and surface sediments (Table 1). Interesting annual changes were observed for pH and Eh values both in the water column and surface sediment; the %DO saturation was strongly linked to those parameters since the range was between 78 and 20%. Salinity ranged from 17.6 to 27.3 psu showing the typical values observed in the confined areas of this lagoon. Water turbidity was relatively high and suspended particulate fluctuated between 20.6 and 54.2 g L
1 whereas total Chl-a showed a mean of 2.93  2.44 mg L
1 peaking in July with 9.25 mg L
1. Nutrient concentrations were relatively high. The mean

dissolved inorganic nitrogen (DIN ¼ NHþ 4 , NO2 , NO3 ) exceeded the imperative value of the RonchieCosta Decree (Italian Ministerial Decree “RonchieCosta Decree”, April 1998; Italian Ministerial Decree, July 1999) for pollutant concentrations in the waters of the Venice lagoon (25 mM), reaching 49 mM in June. Reactive phosphorus (RP) showed an annual mean slightly lower than the imperative RonchieCosta value (0.8 mM) from February to August but exceeded that value from September to January (the maximum was 1.15 mM).

Fig. 4. Annual changes of the Gracilaria vermiculophylla biomass (a) and coverage (b) percentage at Teneri in Venice lagoon during 2009. Bars are the standard errors.

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Nutrient concentrations in pore-water of surface sediments (5 cm top layer) were high: DIN ranged from 1276 to 8316 mM dm3 of sediment and RP from 67 to 278 mM dm3. Sediment was prevalently fine (fraction <63 mm: 96  3%) and dry density was 0.61  0.03 g dwt cm3. The concentrations of organic carbon (Corg), total nitrogen (Ntot) and organic phosphorus (Porg) in surface sediment were on average 12.4  9.33, 3.41  0.52 and 0.23  0.036 mg g
1, respectively. In particular, Porg was 40% of the total phosphorus (Ptot) ranging from 31 to 51%. The Pearson correlation analysis shows only significant coefficients (p < 0.05) between the biomass and Si, NO
2 in the water
column, and NOx ðNO
2 þ NO3 Þ concentrations in pore-water (Table 2). On the contrary the PCA analysis shows a high variance of many variables significantly linked to the Gracilaria vermiculophylla biomass. On the whole, 4 eigenvalues explain 72.5% of the total variance (Table 3), among them 44.7% is due to the first two components. The significant variables (loading <0.7, Fig. 5a) in the 1st component are: pH, %DO and RP in water, Eh in pore-water, Corg, inorganic carbon (Cinorg) and Ntot in surface sediments. In the 2nd component the significant values are due to water temperature (T  C), filtered particulate matter (FPM) and Chl-a. Some significant variables have also been recorded in the 3rd (light irradiance at bottom and Porg) and the 4th component (salinity and NO
2 , Fig. 5b).

197

Table 3 PCA extraction at Teneri station. Eigenvalue

1 2 3 4

Loading

%Variance

Single

Total

Single

Total

7.2 4.8 4.2 3.3

7.2 12.1 16.3 19.6

26.8 17.9 15.5 12.3

26.8 44.7 60.2 72.5

lagoon, and it is one of the most abundant invasive species of the confined areas. Usually it is associated with Ulvaceae, such as Ulva rigida C. Agardh, other Gracilariaceae, especially Gracilaria gracilis and Gracilariopsis longissima, and two other allochthonous species: Agardhiella subulata and Solieria filiformis which have recently arrived in our lagoons and also spread invasively (Sfriso and Curiel, 2007). G. vermiculophylla forms dense tangled populations in

4. Discussion and conclusions Gracilaria vermiculophylla is one of the most recently introduced allochthonous species in the lagoons of the Northern Adriatic Sea after its recording on the coast of North Europe in the 2002 (Rueness, 2005; Thomsen et al., 2007). The species has rapidly colonized these transitional systems, except the MaranoeGrado

Table 2 Correlation coefficients between Gracilaria vermiculophylla and some environmental variables (in bold significant values).

Water

Pore-water

Surface sediment

p < 0.05 per r >j0.58j.

Parameters

Biomass

Coverage

T pH Eh %DO Salinity Bottom irradiance FPM Chl-a Phaeo-a Chl-a tot NO
2 NO
3 NHþ 4 DIN RP Si NHþ 4 NOx DIN RP pH Eh Fine Dry density Ctot Cinorg Corg Ntot Ptot Pinorg Porg Porg/Ptot


0.11
0.39
0.39
0.20
0.48
0.07 0.01
0.06 0.09 0.00 0.60 0.17 0.14 0.32
0.11 0.82
0.26 0.59
0.25
0.01
0.18
0.32
0.14
0.06 0.36
0.20 0.35 0.36
0.12 0.32
0.33
0.34


0.54
0.11 0.07
0.20
0.44
0.47 0.42 0.26 0.34 0.32 0.47
0.06 0.26 0.15 0.18 0.44
0.40
0.04
0.40 0.10 0.16 0.00
0.24 0.19
0.15
0.33 0.24 0.01 0.11 0.39
0.20
0.30

Fig. 5. Principal components analysis of Gracilaria vermiculophylla biomass and percentage cover and some environmental parameters at Teneri in Venice lagoon during 2009. Captions: Twater ¼ temperature in the water column; %DO ¼ percentage of dissolved oxygen; pHwater ¼ pH in the water column; Ehsed ¼ redox potential in surface sediments; FPM ¼ filtered particulate matter; Chl-a ¼ chlorophyll-a; RP ¼ reactive phosphorus; Corg ¼ organic carbon; Cinorg ¼ inorganic carbon; Ntot ¼ total nitrogen; Porg ¼ organic phosphorus; NO
2 ¼ nitrite concentration.

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shallow areas growing associated with mollusc shells, tunicates and calcareous tube worms but never found associated with aquatic angiosperms. In fact, in our environments G. vermiculophylla grows in the presence of turbid waters and high nutrient concentrations in the water column, pore-water and surface sediments. Its spreading is mainly due to vegetative fragmentation, especially because of grazing as observed from Thomsen et al. (2007). Introduction vectors in the North European coasts were probably oyster farms (Rueness, 2005), which imported these bivalves from the Korea and Japan where G. vermiculophylla is abundant. Similarly, in the Adriatic Sea the most probable introduction vectors were clamfarms, which imported the Manila clam Ruditapes philippinarum Adams & Reeve. The same happened with reference to other allochthonous invasive species (Sfriso and Curiel, 2007), but the local spreading in the North Adriatic Sea is due to other vectors such as boats, anchors, nets and other fishing tools. Gracilaria vermiculophylla rapidly colonises eutrophic and low hydrodynamic environments and overcomes the indigenous vegetation, as already observed (Rueness, 2005; Thomsen et al., 2005, 2007; Sfriso et al., 2010b). It has a predilection for shallow environments characterized by muddy sediments that are usually rich in nutrients but it can be also present on sandy sediments with high nutrient availability. This is the case of the lagoon mouth of Sacca di Goro that is strongly affected by the “Po di Volano” inflow and by other branches of the river such as “Po di Maistra” and “Po di Goro” that flow into the Adriatic Sea. The river waters are conveyed by the North Adriatic circulation in front of Sacca di Goro and the environment is strongly eutrophic also along the sea-side. While in 2004 this area was covered by a mixed population of Ulva rigida and Gracilaria gracilis, only a pleustophytic population of G. vermiculophylla was present in 2009. In contrast, Gracilaria vermiculophylla was never found near the inlets of the Venice lagoon because of the low nutrient availability and the high hydrodynamics. It was never found in confined areas where nutrient concentrations are low, except close to some small river inflows (Fig. 1) where the trophic level was high and the salinity ranged between 10 and 30 psu. In conclusion, the most relevant parameters for the establishment and spreading of this species in our transitional systems seem to be high nutrient concentrations and a moderate salinity whereas the other parameters are less significant. Acknowledgements We thanks the anonimous referees for the suggestions and the English revision and ARPA Veneto and ARPA Emilia-Romagna for logistical support during the sampling.

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