Macrophyte production in a shallow coastal lagoon. Part II: Coupling with sediment, SPM and tissue carbon, nitrogen and phosphorus concentrations

Marine Environmental Research 47 (1999) 285±309

Macrophyte production in a shallow coastal lagoon. Part II: Coupling with sediment, SPM and tissue carbon, nitrogen and phosphorus concentrations Adriano Sfriso*, Antonio Marcomini Department of Environmental Sciences, University of Venice, Calle Larga S. Marta 2137, 30123 Venice, Italy Received 12 May 1997; received in revised form 20 August 1998; accepted 28 August 1998

Abstract The spring-summer concentrations of total nitrogen (TN) and total phosphorus (TP) in the top 0±5 cm of sediment in two areas of the Venice lagoon covered by seagrasses and seaweeds, respectively, showed opposite trends. During biomass build up and decomposition, the sediment TN concentration increased by ca. 45% in an area covered by Ulva, whereas, after an early spring increase, TN progressively decreased to a concentration close to the winter values in an area populated by Zostera. A similar trend was recorded for TP, increasing by ca. 18% in the area Ulva-dominated and decreasing by ca. 14% in that populated by Zostera. The concentration of organic carbon (OC), over the same period, increased in the surface sediments of both areas, more in that populated by Zostera (ca. 100%) than in that covered by Ulva (ca. 30%). Winter values were then re-established after October. A similar trend was found at 10±15 cm sediment depth although lower nutrient concentrations were present. The mean concentrations of TN and TP in the particulate matter collected by sediment traps were ca. 3±6 times higher than in the surface sediments in both areas but showed less marked seasonal changes. The spring-summer concentrations of TN and TP in both Ulva and Zostera tissues decreased by a factor of 2±4, with nitrogen possibly acting as a limiting factor. Based on the gross primary production and the tissue nutrient content, the estimated amounts of C, N, P annually recycled by rhizophyte in the lagoon are 200,000±300,000; 11,700±17,500 and 1150±1730 tonnes, respectively. In contrast, the actual nutrient recycling by Ulva is at least one order of magnitude lower. These amounts are much higher than the nutrient availability via point or di€use sources as well as by surface sediment ¯uxes; thus the sea is thought to be

* Corresponding author. Tel.: 0039 415298529; fax: 0039 415298584 0141-1136/99/$Ðsee front matter # 1999 Elsevier Science Ltd. All rights reserved. PII: S014 1-1136(98)0012 2-6

286

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

a major nutrient supplier for macrophyte growth in the lagoon of Venice. # 1999 Elsevier Science Ltd. All rights reserved.

1. Introduction After the recent changes in climatic (lower water temperatures in spring) and environmental conditions (lower nutrient availability, increased sediment disturbance during harvesting of bivalves, increased grazing pressure, etc.) recorded in the Venice lagoon (Sfriso, 1996; Sfriso and Marcomini, 1996a), macrophyte populations include some macroalgal species (especially: Ulva rigida, Chaetomorpha linum, Gracilaria sp.pl.) and rooted macrophytes (Zostera noltii, Z. marina and Cymodocea nodosa), and these are competing for the same space. Of the three natural basins of the Venice lagoon, the southern one is rhizophyte-dominated, whereas the central and northern ones are predominantly populated by macroalgae, with Ulva rigida as the main species (Sfriso, 1987). The spatial distributions of seagrasses (Caniglia et al., 1990, 1992; Scarton et al., 1995; Curiel et al., 1996) and macroalgae (Sfriso et al., 1989, 1992, 1993, 1994; Sfriso and Marcomini, 1994, 1996a,b,c) as well as their production (Sfriso et al., 1988, 1989, 1993, 1994; Sfriso and Marcomini, 1994, 1996b,c; Sfriso and Pavoni, 1994) have been extensively described. It has been shown that macroalgae interfere markedly with nutrient and pollutant recycling (Sfriso et al., 1989, 1995a,b; Pavoni et al., 1990; Maroli et al., 1993; Marcomini et al., 1993, 1997) and an evaluation of the gross primary production (Sfriso and Marcomini, 1994) allowed the estimation of the mass balance for the total amounts of carbon, nitrogen and phosphorus in the central lagoon. The present investigation was undertaken in order to quantify the C, N and P concentrations in the sediments, the settled particulate matter (SPM) and macrophyte tissues of the lagoon, as well as to update the estimation of the nutrient balance in the central basin after the dramatic decline of Ulva since 1990 (Sfriso, 1996; Sfriso and Marcomini, 1996a). The nutrient mass-balance was also extended to areas populated by rhizophytes. Accordingly, we compared the nutrient behaviour in two areas: Lido station, located in the central lagoon and dominated by Ulva rigida C. Ag., and Petta di BoÁ which is in the southern lagoon and is dominated by Zostera marina L. The results of this investigation, coupled with the available results on primary production and nutrient concentrations in the water column and porewater of the same areas (Sfriso and Marcomini, 1997), expands the knowledge on the role played by di€erent macrophytes in the trophic cycles of shallow coastal lagoons. 2. Materials and methods 2.1. Biomass and primary production of Ulva and Zostera The determination of macrophyte biomass was obtained by averaging 6±8 sub-samples (0.5 m2 for Ulva and 0.05 m2 for Zostera) within permanent and homogeneous

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

287

areas of 15  15 m. This sampling procedure assures an accuracy >95% (Sfriso et al., 1991). Sampling frequency was two to four times a month for Ulva and monthly for Zostera. The net primary production (NPP) of Ulva was measured by the biomass variation method by summing the signi®cant (ANOVA, p < 0.01) biomass increases over the sampling period: February 1994±February 1995. The NPP of Zostera (shoots + rhizomes-roots) was obtained twice a month by marking the shoot and rhizome meristem of 10 di€erent plants and calculating the biomass increases per square meter taking into account shoot and leaf density. The gross primary production (GPP) of Ulva was estimated by a mass balance of phosphorus in sediment, settled particulate matter (SPM) and Ulva tissues according to a procedure set up by Sfriso and Marcomini (1994). The GPP of Zostera was obtained by GPP/NPP ratios found in literature. Further details of these procedures are reported in Part I of this research work (Sfriso and Marcomini, 1997). 2.2. Carbon, nitrogen and phosphorus concentrations in sediment and SPM Two sediment layers, 0±5 cm and 10±15 cm deep, respectively, were obtained by homogenizing 5±6 core fractions, collected by using a plexiglas corer (i.d. 10 cm), on a monthly basis, from February 1994 until January 1995. Sediment samples were frozen, lyophilised and analyzed for their nutrient content. Total nitrogen (TN) and total carbon (TC) were determined using a CNS Analyser (Carlo Erba NA 1500). Organic carbon (OC) was obtained with the same procedure used for TC, after acidi®cation with 1N HCl to remove carbonates. Inorganic carbon (IC) was calculated as the di€erence between TC and OC. Inorganic and total phosphorus (IP and TP) were determined by shaking the ®nely powdered samples (200 mg) in 1N HCl (50 ml) for 16 h, before and after combustion at 550 C, according to the procedure used by Aspila (1976) and the colorimetric methods reported by Strickland and Parsons (1972). The di€erence between TP and IP gives the organic phosphorus (OP). Data of chemical analyses are the mean of duplicate or, when it was necessary, triplicate measurements to attain a precision >95%. Particulate samples were obtained by homogenizing the settled particulate matter (SPM) collected twice a month on the bottom by three sediment traps (bottom: 20  20 cm, surface: 15  15 cm, height: 10 cm) covered by a 1-cm nylon net to minimize the introduction and spawning of ®sh and benthic fauna. Traps had been speci®cally designed for shallow water areas with strong tidal excursions (Sfriso et al., 1991) and successfully used to estimate the seasonal and annual integrated ¯uxes of SPM, nutrients and pollutants (Sfriso et al., 1992, 1995b) as well as the gross production of Ulva rigida (Sfriso and Marcomini, 1994). Nutrient concentrations were determined in volumetric sub-samples of 250 ml after lyophilization, and applying the same analytical procedures used for the sediment. 2.3. Carbon, nitrogen and phosphorus concentrations in Ulva and Zostera tissues Freeze-dried aliquots of shoots, roots-rhizomes and dead parts of shoots and rhizomes mixed together, were ®nely powdered and analyzed in duplicate or triplicate

288

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

for carbon, nitrogen and phosphorus content. Carbon and nitrogen were obtained by using the CNS Elemental Analyser. The precision of measures was >97%. Phosphorus was determined colorimetrically after te¯on bomb digestion by a HNO3±HClO4 mixture, according to Kornfeldt (1982). The colorimetric quanti®cation was performed in agreement with the procedures reported by Strickland and Parsons (1972). The precision of phosphorus determination was >95%. The accuracy of these analytical procedures was tested by an intercalibration exercise carried out by ten European Laboratories on the framework of the European Programmes: ``Benthic Eutrophication Studies'' (BEST) and ``Eutrophication and Macrophytes'' (EUMAC). 2.4. Statistical procedures Tests of signi®cance between variables were obtained by ANOVA and the most signi®cant relationships between variables were investigated by a Pearson correlation matrix between the whole set of variables considered in Part I, and the parameters studied in this paper. Finally all data, grouped in such a way as to obtain an average sample per month, were analysed by the Principal Component Analysis of the Statistica (StatSoft, USA, 1994) software package, release 4.5.

3. Results 3.1. Biomass of Ulva and Zostera Biomass trends of Ulva rigida C.Ag. and Zostera marina L. are presented in Fig. 1. Both species exhibited biomass peaks in June, but Ulva reached a maximum standing crop about twice that of Zostera. Ulva ¯uctuated around 5±6 kg mÿ2 (wet wt.) until May, then increased up to 11.2 kg mÿ2, wet wt. During the summer, the frequent occurrence of hypoxic conditions reduced the biomass to 2±4 kg mÿ2, wet wt. The minimum standing crop was monitored in September (ca. 1 kg mÿ2, wet wt.), and the pre-spring biomass (ca. 5 kg mÿ2, wet wt.) was re-stored over the successive cold season. Zostera started to increase in April from a winter biomass of ca. 1.7 kg mÿ2, wet wt. This species reached the highest standing crop in June (ca. 6.3 kg mÿ2, wet wt.) and progressively decreased down ca. 2.0 kg mÿ2, wet wt. in December. Between Zostera meadows occasional patches of macroalgae (especially Ulva rigida and Chaetomorpha linum) were found and an additional biomass, accounting for 20± 30% that of Zostera, must be taken into consideration. Further information on trends and productions of these species in relation to physico-chemical parameters and nutrient dynamics in waters and pore-waters of the studied areas were presented in Part I of this research (Sfriso and Marcomini, 1997).

Fig. 1. Macrophyte biomass trends at the Ulva (Lido) and Zostera (Petta di BoÁ) stations. The accuracy of biomass measurements was higher than 95%.

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309 289

Settled particulate material (SPM)

Deeper sediment layer (10±15 cm)

Surface sediment layer (0±5 cm)

C

N P

C

N P

C

Total inorg.

Total inorg. org. Total Total inorg. org.

Total inorg. org. Total Total inorg. org.

64 41

75 66 6.8 0.8 0.42 0.32 0.07

79 68 8.2 1.2 0.35 0.25 0.07

89 65

82 74 11.2 1.2 0.52 0.40 0.18

82 73 12.2 1.9 0.4 0.33 0.11

76 ‹ 8 53 ‹ 7

78 ‹ 1.8 69 ‹ 2.7 8.9 ‹ 1.4 1.1 ‹ 0.1 0.48 ‹ 0.03 0.36 ‹ 0.03 0.12 ‹ 0.03

80 ‹ 1.1 71 ‹ 1.4 9.4 ‹ 1.1 1.4 ‹ 0.2 0.38 ‹ 0.02 0.28 ‹ 0.02 0.09 ‹ 0.01

69 34

49 44 2.8 0.4 0.46 0.30 0.13

51 44 5.2 0.5 0.42 0.37 0.02

100 48

60 55 7.9 1.2 0.58 0.36 0.22

62 52 12.0 1.3 0.49 0.42 0.10

Max

76 ‹ 9 41 ‹ 4

54 ‹ 3.2 49 ‹ 2.7 5.1 ‹ 1.2 0.7 ‹ 0.2 0.51 ‹ 0.04 0.33 ‹ 0.02 0.18 ‹ 0.03

56 ‹ 2.7 49 ‹ 2.6 7.3 ‹ 2.4 0.8 ‹ 0.2 0.45 ‹ 0.02 0.40 ‹ 0.02 0.05 ‹ 0.02

Mean

Min

Mean

Min

Max

Petta di BoÁ area (Zostera marina)

Lido area (Ulva rigida)

Table 1 Nutrient concentrations (mg/g, dwt) in sediments, settled particulate material (SPM) and macrophyte tissues

ns <0.0001

<0.0001 <0.0001 <0.0001 <0.0001 <0.03 <0.02 <0.0001

<0.0001 <0.0001 <0.02 <0.0001 <0.0001 <0.0001 <0.0001

ANOVA

290 A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

C N P

Total Total Total

org. Total Total inorg. org. 245 19 0.5

16 2.4 0.59 0.14 0.44 285 ‹ 24 27 ‹ 5 0.9 ‹ 0.3

23 ‹ 5 4.3 ‹ 1.2 0.73 ‹ 0.12 0.21 ‹ 0.06 0.53 ‹ 0.08

C N P Roots-r- C hizomes N P Dead C parts N P

Shoots

322 33 1.5

33 6.7 0.92 0.32 0.65

408 29 3.8 370 17 1.5 383 21 1.8

Total 9 Total 0.6 Total 209 Total 11 Total 0.6

289 32 2.1

53 6.5 0.81 0.34 0.51

354 17 1.3 207

Total Total Total Total

241 11 0.5

24 1.5 0.53 0.16 0.38

14 ‹ 3 1.1 ‹ 0.4

12 ‹ 3 1.0 ‹ 0.2 326 ‹ 44

376 ‹ 16 23 ‹ 4 2.3 ‹ 0.8 320 ‹ 44

265 ‹ 15 21 ‹ 7 1.1 ‹ 0.6

35 ‹ 9 3.7 ‹ 1.4 0.67 ‹ 0.09 0.22 ‹ 0.07 0.45 ‹ 0.04 <0.02 <0.05 ns

<0.001 ns ns ns <0.01

(Values refer to 12 monthly samples. Anova compares the signi®cativity of the di€erences between the two areas at p < 0.05; ns=not signi®cant).

Zostera tissues

Ulva tissues

N P

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309 291

292

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

Fig. 2. Nutrient concentrations in the surface sediment (0±5 cm) of the sampling areas. Precision was higher than 95%.

3.2. Carbon, nitrogen and phosphorus concentrations in the surface sediment The studied areas di€er quite markedly in terms of concentrations and trends of nutrients, both in the surface (0±5 cm) and deeper (10±15 cm) sediment (Table 1, Fig. 2). On an annual basis, mean values of N and C compounds were signi®cantly lower at the Zostera than at the Ulva area. Organic carbon accounted for ca. 9±13% of TC. Phosphorus, except the organic fraction, displayed opposite concentration trends, i.e. it was 10±20% higher at the Zostera than at the Lido area (Fig. 2), mostly in the surface sediment (ANOVA, p < 0.0001) rather than in the deeper layer (ANOVA, p < 0.03) (Table 1). The organic fraction of phosphorus was ca. 23±24%

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

293

Table 2 Mean C:N:P atomic ratios in sediment and SPM of the sampling areas Ulva area

Sediment SPM

0±5 cm 10±15 cm

Zostera area

C:P

C:N

N:P

C:N:P

C:P

C:N

N:P

C:N:P

549 428 273

66 85 22

8.3 5.1 13

549:8:1 428:5:1 273:13:1

324 276 297

84 103 27

4.0 2.8 12

324:4:1 276:3:1 297:12:1

of the TP at both depths at the Zostera area, whereas it accounted for ca. 12%, in the surface and ca. 35% in the deeper layer at the Ulva station. The concentration of TN and TP, in the area dominated by Ulva rigida, in summer exceeded by ca. 45% and 18% the mean winter values, which were re-established the successive autumn (Fig. 2). Vice versa, in the area mainly populated by Zostera marina the TN and TP concentrations, after an initial increase in spring due to nutrient availability in the water column, rapidly decreased to minima values in late summer, when concentrations were similar to or lower than to those recorded in winter (Fig. 2). The concentrations of organic carbon (OC) were found to increase in both areas, especially in that populated by Zostera where OC doubled from April to June. The mean C:N:P atomic ratios in the surface and deeper sediment layers at the Ulva station were 549:8:1 and 528:5:1, respectively, while at the Zostera station the same ratios were 324:4:1 and 276:3:1 (Table 2). Particularly low were the mean N:P values found in the Zostera area suggesting a possible nitrogen limitation. 3.3. Carbon, nitrogen and phosphorus concentrations in the settled particulate matter (SPM) The annual trends of nutrients in SPM were similar but their concentrations (Table 1, Fig. 3) were signi®cantly higher (ANOVA, p < 0.001) than those recorded in surface sediments. On average, ca. 67±72% of TP and 30±46% of TC in SPM were represented by the organic fractions, which were ca. 6±8 and 2.5±5 times higher than the amounts found in surface sediments. Similar results were obtained for TN, with the concentration in SPM exceeding the concentration in sediment by a factor of 3±5. The concentrations of TP and TN in the SPM collected in the two areas were not signi®cantly di€erent. In contrast, the concentration of OC was signi®cantly higher (+60%) in the area dominated by Zostera (ANOVA, p < 0.001), in spite of the annual sedimentation rate recorded in this area. Sedimentation was ca. 6.2 times higher than that found in the area dominated by Ulva (Sfriso and Marcomini, 1997). The C:N:P atomic ratios in SPM were quite similar in both areas. However, C:P and C:N ratios of SPM were signi®cantly (ANOVA, p < 0.001) lower than in the surface sediments (Table 2), especially C:P in Ulva area and C:N in the station

294

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

Fig. 3. Nutrient concentrations in the SPM collected in the two areas. Precision was higher than 95%.

populated by Zostera. In contrast, the N:P ratios in the SPM of both areas were higher than in sediments, especially in the Zostera area. 3.4. Carbon, nitrogen and phosphorus concentrations in the macrophyte tissues There were no signi®cant di€erences in the concentrations of nutrients in the tissues of Ulva taken from both areas, and they were similar to those found in Zostera (Fig. 4). However, at both stations, the nitrogen and phosphorus concentrations in Ulva tissues during the biomass build up decreased by a factor of ca. 2±4 (Fig. 4) whereas the content of carbon in Ulva at Lido, in the same period, decreased by ca.

Fig. 4. Nutrient concentrations in Ulva and Zostera tissues. Precision was higher than 95%.

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309 295

296

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

Table 3 Mean C:N:P atomic ratios in Ulva rigida tissues Plant part

Location

Thallus Thallus Thallus Thallus

C:N

C:P

N:P

C:N:P

Authors

10 13 ÿ 15

336 1051 ÿ 320

35 80 7±33 22

336:35:1 1051:80:1 ÿ 320:22:1

Atkinson and Smith (1983) Atkinson and Smith (1983) Zavodnik (1987) Visentini Romanin (1989)

Annual mean on the whole thallus

Lido watershed

11

268

25

268:25:1

Sfriso et al. (1989)

Sacca Sessola

11

280

25.0

280:25:1

Annual mean on the young thalli Annual mean on the old thalli

Sacca Sessola

15

378

25.8

378:26:1

Sacca Sessola

9

224

24.5

224:25:1

Sfriso et al. (1993) Sfriso and Marcomini (1994) Sfriso et al. (1993) Sfriso and Marcomini (1994) Sfriso et al. (1993) Sfriso and Marcomini (1994)

Annual mean on the whole thallus (in cages)

Sacca Sessola

14

598

43.5

598:44:1

Sfriso (1995)

Fusina Lido watershed

11 13

368 930

32.5 72

368:32:1 930:72:1

Sfriso (1995) This paper

Petta di BoÁ

16

788

50

788:50:1

This paper

18 12 13

481 120 79

27 10 6

481:27:1 120:10:1 79:6:1

Petta di BoÁ

36 11 19

457 170 57

24 15 3

457:24:1 170:15:1 57:3:1

Petta di BoÁ

59

843

28

843:28:1

Birch (1975) Umebayashi (1989) Pellikaan and Nienhuis (1988) This paper Umebayashi (1989) Pellikaan and Nienhuis (1988) This paper

Annual mean on the whole thallus

C:N:P atomic ratios in Zostera marina tissues Leaves

Roots-rhizomes

24%. A similar change was found for the N and P concentrations in the shoot tissues of Zostera, which decreased by a factor of ca. 2±3 (Fig. 4). Shoots did not display any signi®cant variation in carbon content whereas an interesting springsummer increase (ANOVA, p < 0.01) took place in the root-rhizome system. On average, shoots showed N and P concentrations ca. 2±3 times higher than the rootrhizome system (ANOVA, p < 0.0001) displaying the highest di€erences in winter. The mean C:N:P atomic ratios both of Ulva thalli and Zostera shoots and rootsrhizomes are reported in Table 3 and compared with values obtained in previous studies. In particular, the Ulva N:P ratios appear higher than 5±10 years ago (Sfriso et al., 1989; Sfriso and Marcomini, 1994) when phosphorus in the water column was

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

297

more readily available because of more reduced conditions in surface sediments. Similarly Ulva N:P ratios were higher than in Zostera tissues, probably caused by the ability of this latter species to take up nutrients by the roots-rhizome system. In addition, C:N:P ratios were signi®cantly higher (ANOVA, p < 0.001) in roots-rhizomes than in shoots of Zostera emphasizing the ability of nutrient translocation from sediment to leaves via root-rhizome system. 3.5. Statistical analysis 3.5.1. Ulva station Signi®cant inverse correlations between the standing crop of Ulva and the concentration of nutrients in the surface sediment (r=ÿ0.53 for OC; r=ÿ0.66 for TN; r=ÿ0.87 for TP) were inferred from the matrix correlation coecients. High macroalgal standing crops are usually linked to low redox potentials and high phosphorus releases in the water column, as well as to high denitri®cation and decomposition rates, which are coupled with nitrogen and carbon losses (Sfriso and Marcomini, 1994). In contrast the Ulva per cent relative growth rate (%RGR) did not show any signi®cant correlation with the amount of nutrients in surface sediment but it was inversely correlated only with the concentration of dissolved inorganic nitrogen (DIN) in the water column (r=ÿ0.65), suggesting that nitrogen could be a limiting factor for macroalgal growth. The correlation between the biomass and the internal quota of nutrients was positive (TC: r=0.70; TN: r=0.59), since high standing crops, usually show low %RGR (Sfriso, 1995). The concentrations of inorganic phosphorus (IP) in sediment, and thus of TP, were inversely related to the tissue concentration of TC (r=ÿ0.72), TN (r=ÿ0.66) and TP (r=ÿ0.53). Usually phosphorus is trapped by the surface sediment under oxic conditions, i.e. when the biomass is low and the %RGR of Ulva is high. Under these conditions the internal quota of Ulva are quickly depleted. The principal component analysis (PCA) applied to the whole set of variables considered in the previous paper (Sfriso and Marcomini, 1997, i.e. physico±chemical parameters, nutrients in water, %RGR, %grazing) as well as in this work, con®rm the above relationships (Fig. 5). About 51% of the total variance is explained by the ®rst two principal components (Table 4). The variance in the ®rst component (27% of the total variance) was explained by the positive loading of a number of variables (namely by Ulva biomass and its internal quota of TC, TN and, to a lesser extent, TP), whereas the negative contributions were mainly due to the concentrations of TP and IP in the surface sediments. The variance in the second component (24% of the total variance) was related mostly to the negative contributions of pH and Eh in the surface sediment and to the positive loading of reactive phosphorus (RP) in porewater. The loading of temperature of the water column and the grazing pressure of benthic fauna were also signi®cant. The plot of the variable scores sorts samples in two seasonal groups, one corresponding to the January±May period, which is characterized by oxidised conditions and Ulva biomass production, and the other corresponding to the June±December period, governed by biomass decomposition processes.

Fig. 5. Principal component analysis between monthly averaged samples of the variables discussed in the Part I of this work (Sfriso and Marcomini, 1997) and those considered in this paper.

298 A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

299

Table 4 Extraction of principal components in the two areas a Eigenvalues (Petta di BoÁ)

1 2 3 4 5 6

Eigenvalues (Lido)

Eigenvalue

% total Cumul. variance eigenvalue

Cumul.%

Eigenvalue

% total Cumul. variance eigenvalue

Cumul.%

9.0 4.5 3.4 2.9 2.7 2.2

28.9 14.4 11.0 9.3 8.8 7.2

29 43 54 64 72 80

6.9 6.3 3.2 2.6 2.1 1.4

26.6 24.2 12.3 10.1 8.1 5.4

27 51 63 73 81 87

9 13 17 20 22 25

7 13 16 19 21 23

a The considered variables are: (1) Water column temperature (temp), (2) pH of the water column (pHw), (3) pH of the surface sediment (pHs), (4) Eh of the water column (Ehw), (5) Eh of the surface sediment (Ehs), (6) Chlorinity of the water column (Chlorin), (7) Oxygen saturation (Oxyg), (8) Light transmission (Trans), (9) Macrophyte biomass (Biom), (10) Water column reactive phosphorus (RPw), (11) Water column dissolved inorganic nitrogen (DINw), (12) Porewater reactive phosphorus (RPpor), (13) Porewater dissolved inorganic nitrogen (DINpor), (14) Amount of settled particulate matter (SPM), (15) Per cent relative growth rates (%RGR), (16) Per cent grazing pressure (%Graz) **, (17) Total carbon concentration of sediment (TCs), (18) Inorganic carbon concentration of sediment (ICs), (19) Organic carbon concentration of sediment (OCs), (20) Total nitrogen concentration of sediment (TNs), (21) Total phosphorus concentration of sediment (TPs), (22) Inorganic phosphorus concentration of sediment (IPs), (23) Organic phosphorus concentration of sediment (OCs), (24) Total carbon concentration of shoots (TCsh) *, (25) Total carbon concentration of rhizomes (TCrhiz) *, (26) Total nitrogen concentration of shoots (TNsh) *, (27) Total nitrogen concentration of rhizomes (TNrhiz) *, (28) Total phosphorus concentration of shoots (TPsh) *, (29) Total phosphorus concentration of rhizomes (TPrhiz) *, (30) Total carbon concentration of Ulva (TCulv), (31) Total nitrogen concentration of Ulva (TNulv), (32) Total phosphorus concentration of Ulva (TPulv). * Only at the Zostera station (Petta di BoÁ). ** Non available at the Zostera station.

3.5.2. Zostera station The biomass of Zostera appears directly correlated with OC (r=0.59) and inversely with IC (r=ÿ0.73) and TP concentrations in the surface sediments. This suggests an active uptake of carbon and phosphorus from sediments through the rootrhizome system and an accumulation of organic matter triggered by the decaying leaves. The biomass of Zostera was directly correlated also with the carbon concentration in tissues (increasing from the shoots which display a more active growth: r=0.38; throughout the rhizome-roots system: r=0.54; and the dead parts: r=0.60) and inversely with the concentration of nitrogen (shoots: r=ÿ0.65; rhizomes: r=ÿ0.40) and phosphorus (shoots: r=ÿ0.65; rhizomes: r=ÿ0.56; and dead parts: r=ÿ0.23) con®rming the hypothesis of a nutrient translocation from the sediments to the shoots, via the root-rhizome system. Similarly, the concentrations of nutrients in Zostera tissues were inversely correlated with the concentrations recorded in the sediments. In particular, the content of phosphorus in tissues was inversely related

300

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

Table 5 Principal variables contributing to the total variance at the two sampling areas Loading > 0.7

Ulva station (Lido)

First principal component

Second principal component

Zostera station (Petta di BoÁ)

First principal component

Negative

Positive

-Sediment inorganic phosphorus, -Sediment inorganic phosphorus. ÿ

-Total carbon concentration of Ulva, -Ulva biomass,

-pH of the surface sediment, -Eh of the surface sediment. ÿ -Water column temperature, -Zostera biomass. ÿ ÿ ÿ ÿ

Second principal component

-Total nitrogen concentration of sediment, -Total carbon concentration of sediment.

-Total nitrogen concentration of Ulva. -Porewater reactive phosphorus, -Water column temperature, -Percent grazing pressure. -Total nitrogen concentration of Ulva, -Total nitrogen concentration of shoots, -Total phosphorus concentration of shoots, -Total phosphorus concentration of Ulva, -Eh of surface sediment, -Water colum dissolved inorganic nitrogen. ÿ ÿ

to the concentration of IP (r=ÿ0.79 for shoots; r=ÿ0.48 for roots-rhizomes) in the surface sediment. Signi®cant positive correlations between the growth of shoots and the concentrations of nutrients in the surface sediment (r=0.49 for OC; r=0.59 for TN; r=0.46 for IP) were also recorded. The growth of shoots was also inversely related to the tissue concentration of nutrients, especially phosphorus (r=ÿ0.48). In this area dominated by Zostera, Ulva played a marginal role in the nutrient dynamics. The concentration of TN in the Ulva tissue was directly related to the nitrogen (DIN) concentration in the water column (r=0.71), whereas the concentration of TP was inversely related to the reactive phosphorus (RP: r=ÿ0.54) concentration. Similar to Zostera, the concentrations found in the Ulva tissue of this area were inversely related to the concentrations in the surface sediments, particularly in the case of the tissue TP with the sediment IP (r=ÿ0.72).

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

301

The plot of variable scores in the PCA (Fig. 5), clearly discriminates the period of Zostera growth (April±October) from that of low biomass production (November± March). The variance explained by the ®rst two PCs (43%, Table 4) appears slightly lower than that found for the area populated by Ulva. The variance of the ®rst PC (29%) was explained by the negative contribution (loading > 0.7) of the water temperature and the Zostera standing crop. The positive contributions resulted from the concentrations of TN and TP in Zostera and Ulva tissues, and from the redox potential of the surface sediment and the DIN in the water column. A signi®cant variable loading in the second PC (14% of the total variance) depended on the negative contribution of the concentrations of TC and TN in the surface sediment only (Table 5). 4. Discussion 4.1. Nutrient concentrations and atomic ratios A preliminary view of nitrogen and phosphorus concentration trends in the sediments of the two areas, especially in the top 0±5 cm layer, indicates that an opposite seasonal behaviour takes place (ANOVA, p < 0.001), i.e. a spring±summer nutrient enrichment in the area dominated by Ulva and a depletion, after an initial enrichment, in the area populated by Zostera. These ®ndings result from the different strategies of nutrient uptake by the two taxa. Ulva is a macroalga which, in sheltered bays and lagoons, lives preferentially free-¯oating in the water column, taking up nutrients throughout the whole ¯at distromatic thallus. During its luxurious growth, this species becomes greatly strati®ed and in the deeper layers, where photosynthesis is limited by light, the biomass decay supplies the surface sediment with N and P at a rate greater than the amounts released by mineralization processes. Moreover, nutrient enrichment on the surface sediment is frequently enhanced by biomass collapse during anoxic periods (Sfriso et al., 1987, 1988). In autumn±winter, an opposite situation takes place: The production of macroalgae and, consequently, nutrient ¯uxes to, and from, surface sediments are strongly reduced, thus restoring the nutrient concentrations found before the pre-growth explosion. In contrast, Zostera marina is a vascular plant made up of leaves (above-ground part) and a root-rhizome system (below-ground part). This species can take up nutrients both from the water column and the surface sediment as was observed in several estuarine systems (McRoy et al., 1972; Iizumi and Hattori, 1982; Iizumi et al., 1982; Short, 1987; Short and McRoy, 1984; Zimmerman et al., 1987; Pedersen and Borum, 1992). When the nutrient availability in the water column becomes critical, Zostera grows by pumping nutrients from the sediment through its root±rhizome system, thus behaving in the same way as terrestrial plants. According to this strategy, the concentration of N found in the top 5 cm layer of sediment, after an initial enrichment due to the nitrogen availability in the water column, decreased progressively to or below the pre-growth values; whereas the concentration of P,

302

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

negligible in the water column, was progressively reduced down by ca. 14%. In addition, the low N:P ratios found in the sediment of this area colonised by Zostera indicate that nitrogen probably was the critical element for biomass growth (Table 2). In other lagoonal systems, such as the lagoon of Thau in the Languedoc region (France) (De Casabianca et al., 1996; Rigollet et al., 1996) or the lagoons of Grevelingen and Veerse Meer (The Netherlands) (Pellikaan and Nienhuis, 1988; De Vries et al., 1988; Nienhuis, 1992; Van Lent and Verschuure, 1994a,b), where the nutrient availability in the water column is much higher than in the Venice lagoon and the mean water depth is ca. 5 m, Zostera prefers to take up nutrients from the water column through leaves. This results in a lower depletion of nutrients in the surface sediment. The role played by water or surface sediments as nutrient sources for the growth of macrophytes can be also inferred from the concentration of nutrients in their tissues (Fig. 4). In fact, the internal quota of N and P during the active growth period decreased by a factor 2±4 both in Ulva and Zostera and the pre-growth concentrations were restored in the successive cold season. Moreover, in the Southern part of the Venice lagoon, which displays features similar to other low eutrophicated environments (PeÂrez-LloreÂns et al., 1991) and sediment is the main nutrient source, shoot concentrations of N and P were ca. 2±3 times higher than in the root±rhizome system. Nutrients taken up from the surface sediment are mobilised through the root±rhizome tissues to the active growing parts of plants, especially to the younger leaves (Welsh and Denny, 1979; Iizumi and Hattori, 1982; Brix and Lyngby, 1985; PeÂrez-LloreÂns and Niell, 1989; PeÂrez-LloreÂns et al., 1991, 1993). Due to the signi®cant spring±summer decrease in TP and TN tissue concentration (Fig. 4), the mean C:N:P atomic ratios both in Ulva and Zostera exhibited a 2±3 fold increase during the warm season. However, the C:P and N:P ratios found in the shoots of Zostera were signi®cantly lower (ca. 51% and 67%, respectively) than the values recorded in Ulva. Conversely, the C:N ratios were ca. 2 (shoots) to ca. 4 (roots±rhizomes) times higher in Zostera than in Ulva, because of the higher carbon concentration in the rhizophyta. The high C:N:P atomic ratios in Zostera marina of the Venice lagoon (Table 3) and the di€erence between values found in shoots and rhizomes con®rm the low availability of N and P compounds in the water column and suggest an active translocation of these elements from the sediment to the leaves throughout the root± rhizome system. Gerlo€ (1975), reported critical limiting values for the aquatic macrophytes of 7.5 mg gÿ1 for N and 0.7 mg gÿ1 for P. As far as Zostera marina leaves are concerned, Duarte (1990) found critical tissue values <18 mg gÿ1 for N and <2.0 mg gÿ1 for P. Moreover, a C:N or C:P atomic ratio above 20 or 474, respectively, was suggested as evidence of growth limitation. According to Gerlo€ (1975), however, neither N nor P were limiting elements (Fig. 4). On the contrary, if one considers the N and P tissue concentrations and atomic ratios reported as critical by Duarte (1990), Zostera marina would be limited by both N and P during the biomass build up and its C:N ratio would be critical all the year round, even during winter and spring, when the availability of nitrogen is high.

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

303

Based on these results, it appears that the critical P and N tissue concentrations reported by Duarte (1990) may be more appropriate for the Venice lagoon than those reported by Gerlo€ (1975). In spite of the marked nutrient decrease observed during growth, the critical values reported by Gerlo€ were never found, not even in the root±rhizome system. As far as the critical tissue atomic ratios are concerned, critical values >40 for C:N and >500 for C:P are suggested for the Zostera marina growing in the Venice lagoon. The C:N:P atomic ratios in the Ulva tissues (Table 3) displayed both a wider variation and higher values in comparison to those recorded in Zostera possibly in response to the lower environmental variations found in the areas populated by phanerogams (Sfriso and Marcomini, 1997). The younger Ulva thalli showed greater C:N and C:P ratios than the older fronds which, on average, displayed higher nutrient contents and lower per cent relative growth rates (%RGR). The inverse relation between the %RGR and the C:N ratios was in agreement with Niell (1976), but the results on the thallus age found in the Venice lagoon di€ered from those obtained by Niell who studied marine species, characterized by long exposure times and low %RGR. Under these conditions, nutrients are progressively stored in the thallus. In general, the C:P ratios appear high in Ulva living in nutrient poor waters, such as sea waters, where phosphorus is usually the limiting factor. High C:P and N:P ratios were found also in Ulva suspended in the cages placed at Sacca Sessola, in the middle of natural biomass beds (Sfriso, 1995) and at the Lido watershed (Table 3). The di€erences recorded at the Lido watershed in the pre-1990 years (Sfriso et al., 1989) and in 1994 (this paper) are presumably due to the signi®cantly lower redox potential conditions recorded in the past, which increased the phosphorus availability in the surface sediments, thus decreasing the C:P and N:P ratios. Another possible explanation could be the low availability of carbon assimilable species (CO2 and, to a minor extent, HCO3ÿ; Lvov et al., 1996) during the period of high Ulva production and the high water pH values (up to 9.5) which have been monitored in the past over the whole central lagoon. However, a severe nutrient limitation for the macrophyte growth, in spite of these results and suggestions, appears questionable in the Venice lagoon. In fact ca. 60% of total water is renewed during a 12 h tidal cycle and nutrients are taken up by Ulva in ®eld at a rate of up to 47% dÿ1 for P and 20% dÿ1 for N (Sfriso, 1995). 4.2. Changes in nutrient concentrations, ¯uxes and balances The seasonal nutrient increase recorded at the Lido station in the surface sediment during the spring±summer Ulva decomposition, was signi®cantly lower than that found in the same area during the 1985±1986 period, when Ulva reached its maximum expansion, covering tens of square kilometres, with a biomass ranging from 5 to 20 kg mÿ2 fwt (Sfriso et al., 1993). In the summer of 1985 during the biomass build up, the concentrations of OC, TN and TP in the top 0±5 cm of sediment increased respectively by ca. 70%, 160% and 75% of the mean winter background values (Sfriso et al., 1988). In summer 1994, the increase of OC, TN and TP, found

304

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

in the surface sediment layers of the same station, was respectively only ca. 30%, 45% and 18% higher than the winter concentrations. This re¯ected the reduced in¯uence of biomass on the nutrient enrichment of the surface sediment. Although the area populated by Ulva in 1994 was covered by a biomass quite similar to that found in the past (range 0±12 kg mÿ2, fwt), Ulva populated a very limited lagoon surface (approximately ca. 2±3  0.2±0.4 km). Under these conditions, the highest sediment concentration of OC, caused by the biomass decay in spring and summer, was even lower than the winter concentrations found in 1985, when the massive Ulva proliferation and sub-sequent collapse was extended over the whole central lagoon. Based on the amount of SPM collected over a year and its nutrient content, the mean concentration of nutrients in Ulva tissues and the winter concentrations of nutrient in surface sediments, it was possible (Sfriso and Marcomini, 1994) to estimate the gross primary production (GPP) and the atmospheric losses of nitrogen and carbon (by denitri®cation and respiration/decomposition processes) taking place at the Ulva area. This estimation was possible because the station of Lido is situated near the Lido watershed, where the import and export of particulate matter can be assumed negligible, and a monospeci®c production of Ulva takes place. In this area, the current GPP has been calculated to be ca. 5.3 times higher than the net primary production (NPP), measured by the biomass change method. In the 1980s the GPP/NPP ratio was even higher (ca. 6.7) than this value (Sfriso and Marcomini, 1994), because of the frequent anoxic periods, which led to a higher amount of biomass decomposition. Estimations of N and C atmospheric losses over the areas covered by Ulva were 51% and 63% the amounts recycled by the GPP, respectively (Sfriso and Marcomini, 1994). Nowadays, with Ulva production/decomposition declined and the water and sediment oxygenation increased, the mean N and C losses have increased to 77%, and 80%, respectively. However, because of the disappearance of Ulva from great part of the lagoon basin, an extrapolation of these results to the whole central lagoon was not possible. Following the decline of the population of Ulva, the nutrient ¯uxes at the water± sediment interface of the lagoon also changed signi®cantly. On a yearly basis, the exchange of phosphorus at the water-surface sediment interface, in areas covered by Ulva, dropped by ca. 30% in comparison with ¯uxes recorded in the 1980s. Conversely, the ¯uxes of nitrogen and carbon increased by ca. 75% and 95%, in spite of the fact that a great part of these elements has been lost into the atmosphere. Unfortunately, the GPP of Zostera and the nutrient ¯uxes, in the area populated by the rhizophytes, could not be estimated according to the previous procedure (Sfriso and Marcomini, 1994) because of the high water exchange and water turbulence resuspending locally a signi®cant amount of sediment. However, based on the annual net production of Zostera marina (ca. 770,000 tonnes fwt., Sfriso and Marcomini, 1997), the mean dry/wet weight ratios of shoots and rhizome-root system (14.8% and 13.7%, respectively) and the mean tissue concentrations of nutrients, it was possible to estimate the amounts of C, N and P recycled by this species in the lagoon of Venice. The NPP of Zostera accounted for an annual C, N and P recycling of ca. 40,000, 2280 and 225 tonnes, respectively. The nutrient recycling by NPP should be increased by a factor ranging from 2 to 3 to be converted into the

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

305

recycling by the gross production (GPP) estimated for this species (Sfriso and Marcomini, 1997). Based on the fact that Zostera marina occupies ca. 39% of the surface covered by rhizophytes (Caniglia et al., 1990, 1992), the remaining surface being populated by Zostera noltii and Cymodocea nodosa, as a ®rst approximation, the total nutrient recycling by the three seagrass species was estimated ca. 200,000±300,000 tonnes for C; 11,700±17,500 tonnes for N and 1150±1730 tonnes for P. These values are ca. 3±5 times higher than the total nutrient inputs in the southern lagoon and exceed the total amounts of nitrogen and phosphorus ¯owing into the whole lagoon (N=ca. 8437 tonnes yÿ1, P=ca. 1148 tonnes yÿ1, Andreottola et al., 1990). Therefore, the results are similar to those found in the central lagoon before the Ulva decline (Sfriso and Marcomini, 1994; Sfriso et al., 1994) and tidal exchange with sea waters is expected to ensure a relevant nutrient supply for the observed production of seagrass biomass, especially as far as nitrogen is concerned. In fact, denitri®cation rates have also to be taken into consideration. In areas populated by Zostera, denitri®cation rates account for ca. 94 mg N mÿ2 dÿ1 (Silvestri et al., 1994), resulting in a N loss of ca. 8100 tonnes yÿ1. This value is quite similar to that estimated (10,000± 11,000 tonnes yÿ1) for the central lagoon populated by Ulva over the 1980±1990 period (Sfriso and Marcomini, 1994, Sfriso et al., 1994). 5. Conclusions The macroalga Ulva rigida and the phanerogam Zostera marina have a very different impact on the cycle of nutrients in the lagoon. During the spring and summer biomass production, Ulva temporarily enriches and Zostera depletes the nitrogen and phosphorus stocks of surface sediments. The principal component analysis con®rms the major role of these macrophytes in the environmental variability of the lagoon, which appears strongly a€ected by the production of biomass in the areas populated by rhizophytes, and by the degradation processes in the areas covered by Ulva. Under low nutrient availability in the water column, Zostera overcomes Ulva because of its ability to also take up nutrients from the sediment via the root±rhizome system. The decline of Ulva recorded in the central lagoon since 1990, signi®cantly improved the oxygenation of both water and sediment, allowing the seasonal enrichment of nutrients in the surface sediment to lower and the release of nitrogen and carbon into the atmosphere to increase. The amount of N and P annually recycled by Zostera marina and by the other lagoon rhizophytes (i.e. Zostera noltii and Cymodocea nodosa), is de®nitively higher than the total annual amount of nutrients entering the lagoon by both point and diffuse sources. In addition, in the areas populated by rhizophytes ca. 8100 tonnes yÿ1 of nitrogen are lost into the atmosphere as volatile species, by denitri®cation. Thus, the tidal water exchange with the sea de®nitely plays a key role as nutrient supplier. In view of the results obtained in this study, a possible further decrease in Ulva and, in the absence of limiting factors such as the mechanical dredging of Tapes

306

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

philippinarum Adams and Reeve (an edible bivalve recently spread over the lagoon), a re-population of rhizophytes in the central lagoon can be expected. Acknowledgements This work was ®nancially supported by the European Community in the framework of the EUMAC-project (EUtrophication and Macrophytes). Additional contribution came from the C.N.R. project ``The Venetian ecosystem, Line 4.1 (De®nition of criteria and methods for the mass and energy balances)''. The authors are grateful to Mrs. Sonia Ceoldo for technical assistance.

References Andreottola, G., Cossu, R., & Ragazzi, M. (1990). Nutrient loads from the Venice lagoon catchment area: comparison between direct and indirect assessment methods (in Italian). Ingegneria Ambientale, 19, 176±185. Aspila, K. I., Agemian, H., & Chau, A. S. J. (1976). A semiautomatic method for the determination of inorganic, organic and total phosphate in sediments. Analyst, 101, 187±197. Atkinson, M. J., & Smiths, V. (1983). C:N:P ratios of benthic marine plants. Limnology and Oceanography, 28, 568±574. Birch, W. P. (1975). Some chemical and calori®c properties of tropical marine angiosperms. Journal of Applied Ecology, 12, 201±212. Brix, H., & Lyngby, J. E. (1985). Uptake and translocation of phosphorus in eelgrass (Zostera marina L.). Marine Biology, 90, 111±116. Caniglia, G., Borella, S., Curiel, D., Nascimbeni, P., Paloschi, A. F., Rismondo, A., Scarton, F., Tagliapietra, D., & Zanella, L. (1990). Maps of seagrass distribution in the Venice lagoon (in italian). Giornale Botanico Italiano, 124, 212. Caniglia, G., Borella, S., Curiel, D., Nascimbeni, P., Paloschi, A. F., Rismondo, A., ScartonõÁ, F., Tagliapietra, D., & Zanella, L. (1992). Distribution of the marine phanerogams [Zostera marina L., Zostera noltii Hornem., Cymodocea nodosa (Ucria) Asch.] in the Venice lagoon (in italian). Lavori SocietaÁ Veneta di Scienze Naturali, 17, 137±150. Curiel, D., Bellato, A., Marzocchi, M., Solazzi, A., & Scattolin, M. (1996). Aspects of the distributive dynamic of the marine phanerogams in the Venice Lagoon (Malamocco basin) (in italian). Lavori SocietaÁ Veneta di Scienze Naurali, 21, 39±51. De Casabianca, M. L., Laugier, T., Soriano, E., Posada, F., Rigollet, V., & Pryor, M. (1996). Analysis of the principal macrophyte systems: Zostera, Ulva and Gracilaria, in an eutrophicated lagoon (Thau, France). In: J. W. Rijstenbil, P. Kamermans, & P. H. Nienhuis (Eds.), Eutrophication and Macrophytes (EUMAC), Synthesis report and Proceedings of the Second EUMAC Workshop. SeÁte, France, 29 February±3 March, 139±189. De Vries, I., Hopstaken, F., Grossens, H., de Vries, M., de Vries, H., & Herringa, J. (1988). GREWAQ: An ecological model for Lake Grevelingen. Report T-0215-03, Rijkswaterstaat DGW, Den Haag, Delf Hydraulics, Delft, pp. 159±183. Duarte, C. M. (1990). Seagrass nutrient content. Marine Ecology Progress Series, 67, 201±207. Gerlo€, G. C. (1975). Nutritional Ecology of Nuisance Aquatic Plants. Natural Enviromental Research Center, Oce of Research and Development, US Environmental Protection Agency, Corvallis, OR, p. 78. Kornfeldt, R. A. (1982). Relation between nitrogen and phosphorus content of macroalgae and the waters of Northern Oresund. Botanica Marina, 25(1), 197±201.

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

307

Iizumi, H., & Hattori, A. (1982). Growth and organic production of eelgrass (Zostera marina L.) in temperate waters of the Paci®c coast of Japan. III. The kinetics of nitrogen uptake. Aquatic Botany, 12, 245±256. Iizumi, H., Hattori, A., & McRoy, C. P. (1982). Ammonium regeneration and assimilation in eelgrass (Zostera marina) beds. Marine Biology, 66, 598±650. Lvov, S. N., Pastres, R., Sfriso, A., & Marcomini, A. (1996). Far-from-equilibrium thermodynamic modelling of aquatic shallow environments. The lagoon of Venice as a case study. In: P. Lassere, & A. Marzollo (Eds.), Venice Lagoon Ecosystem Project. Summaries of Results, UNESCO, pp. 1±10. Marcomini, A., Sfriso, A., & Zanette, M. (1993). Macroalgal blooms, nutrient and trace metal cycles in a coastal lagoon. In: J. W. Rijstenbil, & S. Hartonidis (Eds.), Macroalgae, Eutrophication and Trace Metal Cycling in Estuaries and Lagoons, EC Report BRIDGE-GG XII, pp. 66±90. Maroli, L., Pavoni, B., Sfriso, A., & Raccanelli, S. (1993). Concentrations of polychlorinated biphenyls and pesticides in di€erent species of macroalgae from the lagoon of Venice. Marine Pollution Bulletin, 26, 553±558. McRoy, C. P., Barsdate, R. J., & Nebert, M. (1972). Phosphorus cycling in an eelgrass (Zostera marina L.) ecosystem. Limnology and Oceanography., 17, 58±67. Niell, F. X. (1976). C:N ratio in some marine macrophytes and its possible ecological signi®cance. Botanica Marina, 19, 347±350. Nienhuis, P. H. (1992). Ecology of coastal lagoons in the Netherlands (Veerse Meer and Grevelingen). Vie Milieu, 42, 59±72. Pavoni, B., Calvo, C., Sfriso, A., & Orio, A. A. (1990). Time trend of PCB concentrations in surface sediment from a hypertrophic, macroalgae populated area of the lagoon of Venice. The Science of the Total Environment, 91, 13±21. Pedersen, M. F., & Borum, J. (1992). Nitrogen dynamics of eelgrass Zostera marina during a late summer period of high growth and low nutrient availability. Marine Ecology Progress Series, 80, 65±73. Pellikaan, G. C., & Nienhuis, P. H. (1988). Nutrient uptake and release during growth and decomposition of eelgrass, Zostera marina L., and its e€ects on the nutrient dynamics of Lake Grevelingen. Aquatic Botany, 30, 189±214. PeÂrez-LloreÂns, J.L., & Niell, F. X. (1989). Emergence and submergence e€ects on the distributional pattern and exchange of phosphorus in the seagrass Zostera noltii Hornem. Scientia Marina, 53, 497±503. PeÂrez-LloreÂns, J. L., Muchtar, M., Niell, F. X., & Nienhuis, P. H. (1991). Particulate organic carbon, nitrogen and phosphorus content in roots, rhizomes and di€erently aged leaves of Zostera noltii Hornem. In Oosterschelde Estuary (Southwestern Netherlands). Botanica Marina, 34, 319±322. PeÂrez-LloreÂns, J. L., de Visscher, P., Nienhuis P.H., & Niell, F. X. (1993). Light-dependent uptake, translocation and foliar release of phosphorus by the intertidal seagrass Zostera noltii Hornem. Journal of Experimental Marine Biology and Ecology, 166, 165±174. Rigollet, V., Laugier, T., De Casabianca, M.L., Sfriso, A., & Marcomini, A. (1996). Comparison of two populations of Zostera marina in two mediterranean lagoonds: the Thau lagoon (France) and Venice lagoon (Italy). In: J. W. Rijstenbil, P. Kamermans, & P. H. Nienhuis (Eds.), Eutrophication and Macrophytes (EUMAC), Synthesis report and Proceedings of the Second EUMAC Workshop. SeÁte, France, 29 February±3 March, pp. 250±253. Scarton, F., Curiel, D., & Rismondo, A. (1995). Aspects of the temporal dynamic of the rhizophyte meadows in the lagoon of Venice (in Italian). Lavori della SocietaÁ Veneta di Scienze Naturali, 20, 95±102. Sfriso, A. (1987). Flora and vertical distribution of macroalgae in the lagoon of Venice: a comparison with previous studies. Giornale Botanico Italiano, 121, 69±85. Sfriso, A. (1995). Time and spatial responses of Ulva rigida C.Ag. growth to environmental and tissue concentrations of nutrients in the lagoon of Venice. Botanica Marina, 38, 557±573. Sfriso, A. (1996). Decrease of production and changes on macrophyte typology and distribution in the Venice lagoon. (in Italian). Inquinamento, 5, 80±88. Sfriso, A., Marcomini, A., & Pavoni, B. (1987). Relationship between macroalgal biomass and nutrient concentrations in a hypertrophic area of the Venice lagoon. Marine Environmental Research, 22, 297±312. Sfriso, A., Pavoni, B., Marcomini, A. & Orio, A. A. (1988). Annual variation of nutrients in the lagoon of Venice. Marine Pollution Bulletin, 19, 54±60.

308

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

Sfriso, A., Pavoni, B., & Marcomini, A. (1989). Macroalgae and phytoplankton standing crops in the central Venice lagoon: primary production and nutrient balance. The Science of the Total Environment, 80, 139±159. Sfriso, A., Raccanelli, S., Pavoni, B., & Marcomini, A. (1991). Sampling strategies for measuring macroalgal biomass in the shallow waters of the Venice lagoon. Environmental Technology, 12, 263±269. Sfriso, A., Pavoni, B., Marcomini, A., & Orio, A. A. (1992). Macroalgae, nutrient cycles and pollutants in the lagoon of Venice. Estuaries, 15, 517±528. Sfriso, A., Marcomini, A., Pavoni, B., & Orio, A. A. (1993). Species composition, biomass and net primary production in coastal shallow waters: the Venice lagoon. Bioresource Technology, 44, 235± 250. Sfriso, A. Marcomini, A., & Pavoni, B. (1994). Annual nutrient exchanges between the central lagoon of Venice and the northern Adriatic sea. The Science of the Total Environment, 156, 77±92. Sfriso, A. & Marcomini, A. (1994). Gross primary production and nutrient behaviours in shallow lagoon waters. Bioresource Technology, 45, 59±66. Sfriso, A., & Pavoni, B. (1994). Macroalgae and phytoplankton competition in the central Venice lagoon. Environmental Technology, 15, 1±14. Sfriso, A., Pavoni, B., & Marcomini, A. (1995a). Nutrient concentrations in the surface sediments of the central lagoon of Venice. The Science of the Total Environment, 172, 21±35. Sfriso, A., Marcomini, A., & Zanette, M. (1995b). Heavy metals in sediments, settled particulate matter and phytozoobenthos of the Venice lagoon. Marine Pollution Bulletin, 30, 116±124. Sfriso, A., & Marcomini, A. (1996a). Decline of Ulva growth in the lagoon of Venice. Bioresource Technology, 58, 299±307. Sfriso, A., & Marcomini, A. (1996b). Chap. 15 Italy ± The lagoon of Venice. In: W. Schramm and P.N. Nienhuis (Eds.), Marine Benthic Vegetation, Ecological Studies. Vol. 123, Springer, Berlin-Heidelberg, 339±368. Sfriso, A., & Marcomini, A. (1996c). Macrophytes and nutrient cycles in the lagoon of Venice (Italy). In: J. W. Rijstenbil, P. Kamermans, & P. H. Nienhuis (Eds.), Eutrophication and Macrophytes (EUMAC), Synthesis report and Proceedings of the Second EUMAC Workshop. SeÁte, France, 29 February±3 March, pp. 221±248. Sfriso, A., & Marcomini, A. (1997). Macrophyte production in a shallow coastal lagoon. Part I: coupling with chemico-physical parameters and water nutrient concentrations. Marine Environmental Research, 4, 351±375. Short, F. T. (1987). E€ects of sediment nutrients on seagrasses: literature review and mesocosm experiments. Aquatic Botany, 27, 41±67. Short, F. T., & McRoy, C. P. (1984). Nitrogen uptake by leaves and roots of the seagrass Zostera marina L. Botanica Marina, 27, 547±555. Silvestri, C., Creo, C., Russo, P., Signorini, A., & Izzo, G. (1994). Estimates of denitri®cation and nitrogen ®xation in Venice lagoon water and sediment. Atti IV National Congress of Ecologia S.IT.E. Venice 26±29 September 1994, pp. 135±138. Strickland, J. D. H., & Parsons T. R. (1972). A Practical Handbook of Seawater Analyses, Fish. Res. Board of Canada, Ottana, p. 310. Umebayashi, O. (1989). Eelgrass productivity on an intertidal ¯at of Central Japan. Bulletin Tokai. Regional Fishery Research Laboratory, 127, 17±30. Van Lent, F., & Verschuure J. M. (1994a). Intraspeci®c variability of Zostera marina L. (eelgrass) in the estuaries and lagoons of the southwestern Netherlands. I. Population dynamics. Aquatic Botany, 48, 31±58. Van Lent, F., & Verschuure, J. M. (1994b). Intraspeci®c variability of Zostera marina L. (eelgrass) in the estuaries and lagoons of the southwestern Netherlands. II. Relation with environmental factors. Aquatic Botany, 48, 59±75. Visintini Romanin, M. (1989). Seaweed chemical composition in the Venice lagoon and their use as soil fertilizers (in italian). Agricoltura delle Venezie, 12, 513±525. Welsh, R. P. H., & Denny, P. (1979). The translocation of 32P in two submerged aquatic angiosperm species. New Phytologist, 82, 645±656.

A. Sfriso, A. Marcomini/Marine Environmental Research 47 (1999) 285±309

309

Zavodnik, N. (1987). Seasonal variation in the rate of photosynthetic activity and chemical composition of the littoral seaweeds Ulva rigida and Porphyra leucosticta from the North Adriatic. Botanica Marina, 30, 71±82. Zimmerman, R. C., Smith, R. D., & Alberte, R. (1987). Is growth of eelgrass nitrogen limited? A numerical simulation of the e€ects of light and nitrogen on the growth dynamics of Zostera marina. Marine Ecology Progress Series, 41, 167±176.