Structure and Secondary Production of a Soft Bottom Macrobenthic Community in a Brackish Lagoon (Sacca di Goro, north-eastern Italy)

Estuarine, Coastal and Shelf Science (2001) 52, 605–616 doi:10.1006/ecss.2001.0757, available online at http://www.idealibrary.com on

Structure and Secondary Production of a Soft Bottom Macrobenthic Community in a Brackish Lagoon (Sacca di Goro, north-eastern Italy) M. Mistri, R. Rossi and E. A. Fano Dipartimento di Biologia, Via L. Borsari 46, I-44100 Ferrara, Italy Received 14 August 2000 and accepted in revised form 27 November 2000 The composition and distribution of the macrobenthic community in a lagoon in the Po River delta was investigated by taking monthly samples at three sites during 1994. A total of 38 macroinvertebrate taxa, representing five phyla, were identified. Gastropods, amphipods, and chironomid larvae dominated the macrofauna in term of abundance, while in terms of biomass bivalves were the dominant taxon. Monthly total invertebrate abundance showed considerable fluctuations, depending on the season and on the presence of the red macroalgae Gracilaria verrucosa. In the central area of the lagoon, a significant relationship was demonstrated between macrobenthic community parameters and amount of macroalgal cover. Taking the most important species, i.e. those that contributed most to similarity within sites, only Cerastoderma glaucum was found to be negatively related to the amount of macroalgal biomass. Mean annual secondary production varied between 50 and 75 g AFDW m
2 yr
1 depending on the site, yielding P/B ratios between 1·02 and 1·08. Confinement and moderate disturbance due to the presence of algal cover are hypothesized to determine structure, composition, and production of the macrobenthic community in the Sacca di Goro.  2001 Academic Press Keywords: macrobenthos; confinement; Gracilaria verrucosa; Sacca di Goro; Italian Adriatic coast

Introduction Natural and man-induced disturbance usually causes non-linear responses in coastal lagoon ecosystems (Cade´e et al., 1994). These patterns depend on a number of biological and biogeochemical processes which act as buffers. These inherent buffering capacities contribute to the resistance and resilience of the lagoon ecosystems, thereby contributing to their stability or sustainability (Sherman, 1994). Important non-linear responses were demonstrated in eutrophic lagoons including vegetational community shifts from seagrasses to ephemeral seaweeds (Sand-Jensen & Borum, 1991; Valiela et al., 1997). A case study of particular interest is represented by the progressive increase of opportunistic green macroalgae such as Ulva rigida, Enteromorpha spp., and Cladophora spp.; the increased biomass of these invasive green algae is linked to eutrophication, and is a widespread phenomenon in Italian coastal lagoons (Sfriso et al., 1985; Bombelli & Lenzi, 1996; Viaroli et al., 1996; Tagliapietra et al., 1998). The Sacca di Goro is a microtidal, coastal lagoon located in the southernmost Po Delta area (northern Adriatic Sea) (Figure 1). The Sacca, which has a surface area of approximately 26 km2, with an average 0733–5210/01/050605+12 $35.00/0

depth of about 1·5 m, is spatially enclosed by a long natural sandbank. The lagoon receives nutrient rich fresh water primarily from the Po di Goro and the Po di Volano, and is characterized by limited water circulation. Water exchange in the lagoon has been estimated by models based on temperature and salinity gradients (O’Kane et al., 1992). In 1994, seasonal trends in the hydrology of the Sacca were different (Bartoli et al., 1996) from those observed in the previous years, when large parts of the lagoon experienced severe summer anoxia (Viaroli et al., 1993). Since 1993 the summer dystrophic episodes have been reduced in intensity and duration, due to increased seawater inflow through a large channel cut through the southern sandbank, and, as a consequence, growth of previously dominant macroalgae, Ulva rigida, has been restricted to the south-central area of the lagoon (Viaroli et al., 1996). This has led to several changes in benthic communities in the other areas including the establishment of a patchy, thick, almost monospecific algal cover of Gracilaria verrucosa. The aims of the present study were to describe community composition, distribution, and abundance of the benthic macroinvertebrate fauna in three different areas of the Sacca di Goro, to assess secondary  2001 Academic Press

606 M. Mistri et al.

Goro

Venice Po Pula Study area a cc Sa

Stn A

di G o or

1 km Stn B

Po di

Stn C

o

or

G

Adriatic Sea

44°45' N

12°15' E

F 1. Study sites location. Arrows are proportional to hydrodynamic force at flood tide (redrawn from Figure 8, in Brath et al., 2000).

production, and to evaluate the effect of the macroalgae Gracilaria verrucosa on the benthic community. Materials and methods Study area and abiotic data Three sampling sites (A, B, and C) were chosen along a NW–SE transect (Figure 1), reflecting a gradient of confinement (Brath et al., 2000). Site A (4450.112 N, 1217.422 E) was located in the northern, most sheltered, area of the Sacca; site B (4449.617 N, 1218.478 E) was located in the central area of the lagoon, and, finally, site C (449.094 N, 1219.960 E) was positioned in the easternmost part of the lagoon, closest to the new sea mouth. Characteristics of the surface sediment at the three sampling sites were determined. Three 10 cm deep cores (4·5 cm i.d.) were collected. Sand-silt-clay ratios were determined by wet sieving using a 0·063 mm mesh sieve to capture sand-sized particles, and undertaking pipette analysis of the washings for silt- and clay-size particles (Folk, 1980). Fraction weights were determined by drying at 100 C to a constant

weight. Sediment organic matter content was obtained by weight loss after drying (48 h at 80 C) and incineration (8 h at 450 C) (Craft et al., 1991). Mean monthly values of bottom water temperature, salinity, and dissolved oxygen at each site were averaged from daily measurements gathered by the personnel of the Amministrazione Provinciale di Ferrara by means of an Idronaut Ocean Seven 316 CTD probe. Biotic data: sampling and processing Benthic fauna at each site was sampled monthly from January to December 1994, with the exception of August because of technical constraints. Sampling was by means of a Van Veen grab (area 0·06 m
2) with a penetration depth of about 12 cm in the centre of the grab (about 10 cm at the edge). Three randomly positioned replicates, being the number of sampling units sufficient to collect a high proportion (about the 80% of the total number of species collected with 8 sampling units) of the species complement from the quite homogeneous bottom of the Sacca (M. Mistri, unpubl. data), were removed from the substratum at each sampling site. The contents of the grab were

Macrobenthic community structure and production in a lagoon 607

gently washed on a 0·5 mm sieve. Material retained on the sieve was fixed in 8% buffered formalin, and stained with Rose Bengal to facilitate sorting and identification. The abundance of individuals of each taxon, identified at the species level when possible, was measured for each sample. Macroalgae present in each replicate were separated and washed, and their dry weight estimated (48 h at 80 C). Because Gracilaria verrucosa thalli do not float but settle on the bottom, and since almost monospecific populations of G. verrucosa were found, it was assumed that grab sampling was representative at least of this particular macroalgae population. The faunal biomass was estimated by direct measurement, since negligible differences were found in the comparison between fresh and fixed marine fauna composition (Danovaro et al., 1999). Individual mean weight (as ash-free dry weight, AFDW, after drying at 80 C for 48 h, and incineration at 450 C for 4 h) was measured as the average weight of three replicated subsets constituted by a minimum of two (larger bivalves) up to 200 (small corophiids) individuals per taxon. Additional samples were collected during the year, and the largest specimens of the most common taxa were sorted and weighed in order to obtain the maximum individual body weight, for secondary production estimates. Data analysis The significance of the differences in abiotic data at the three sites was tested using one-way ANOVA. Since sediment parameters were only gathered occasionally, these were not included in the analysis. Macroinvertebrate community structure was described at each site at each sampling date (month) on the basis of the following parameters: abundance, number of taxa, richness (as Margalef’s d), diversity (as Shannon-Wiener’s H ), and evenness (as Pielou’s J ). Differences between sites and dates were tested using ANOVA, and whenever Levene’s tests indicated significant heterogeneity of variances, the data were log-transformed. One-way ANOVAs were performed to determine whether significant differences in macroinvertebrate community parameters existed at different sampling dates and biomass of algal cover. Dry weight of macroalgae at each replicate was a continuous independent variable and date (month) was a categorical independent variable. Factors detected to be significant by ANOVAs were further analysed using a post-hoc Tukey HSD test set at the 5% significance level. A fourth-root transformation was applied to macrofaunal abundance data, and lower triangular similarity

matrices were constructed using the Bray-Curtis similarity index. Data were ordinated by means of nonmetric multidimensional scaling (MDS). The faunal groups contributing to dissimilarity between samples observed in the MDS ordination were investigated using the similarities percentages procedure (SIMPER, Clarke, 1993), and these results were used to assist in interpretation of the faunal changes causing the patterns observed in the ordination. The contribution that each species made to the average similarity within each group was also examined using the same software. Two-way ANOVAs were used to ascertain whether the abundance of the species which mostly contributed to average similarity differed among sites, dates and biomass of algal cover. For this purpose, the abundance of a given species was the dependent variable, dry weight of macroalgae was a continuous independent variable, and site and date were categorical independent variables. Continuous variables were log-transformed prior to analysis. The relationship between measured water variables and macrobenthic community structure was explored by means of BIOENV analysis (Clarke & Ainsworth, 1993), i.e. by correlating euclidean distance similarity matrices of water variables with Bray-Curtis similarity matrices from macrobenthic abundance data. The estimated production rates at the three sampling sites were calculated using the method of Tumbiolo and Downing (1994). The authors derived an equation which incorporated annual mean bottom water temperature (Tb, C) and depth (Z, m) to estimate production (P, g AFDW m
2 yr
1) from annual mean biomass (B, g AFDW m
2) and individual body weight (Wm, mg DW) of marine benthic invertebrates: log P=0·18+0·97 log B
0·22 log Wm +0·04 Tb
0·14 Tb log (Z+1). Results Environmental characteristics and algal cover Table 1 summarizes the main characteristics of the sampling sites. In the sediment, the silt fraction predominated in the north-central area of the Sacca, while the eastern area had more sand; sediment organic matter content exhibited a spatial gradient from the innermost to the outer site. Bottom water temperature at the sampling sites ranged from 5·7 to 28·5 C, following a clear seasonal trend with minima occurring in January and maxima in July. Salinity showed fluctuations due to the lagoonal characteristics of the area, but site C differed significantly (1-way ANOVA, F=5·23, P<0·05) from the others because of lower salinity values all year long. Dissolved oxygen

608 M. Mistri et al. T 1. Summary of the main characteristics of the sampling sites Water Site A B C

Depth (m)

Salinity (mean and range)

Temperature (C) (mean and range)

2·0 1·9 1·6

27·2 (20–36) 27·4 (22–35) 22·3 (17–32)

17 (7·7–28·3) 17·3 (6·8–28·5) 16·4 (5·7–27·5)

Biomass (gDW m–2)

300

Sediment Dissolved oxygen (mg l (mean and range)


1

)

9·5 (5·9–13·6) 8·7 (1·4–14·5) 9·4 (3·2–12·3)

1186

Texture

Organic matter (%) (SE)

clayey-silt clayey-silt silty-sand

16·4 (0·1) 15·1 (0·2) 12·0 (0·1)

385

200

100 ns 0

J

F

M

A

M

J J Month

A

S

O

N

D

F 2. Monthly mean algal cover biomass (August missing) at the three study sites (site A: black; site B: shaded bars; site C: white). Standard errors are also given.

followed a seasonal trend, ranging from 14·5 (March) to 1·4 mg l
1 (July), but no significant differences were detected between the three sites. Algal cover was present at all sites during most of the year (Figure 2). The dominant species at the three sampling sites was Gracilaria verrucosa. Algal biomass varied during the year with different numbers of peaks; maximum values were observed in March (1186 g DW m
2) and July (385 g DW m
2) at site B. Two-ways ANOVA (factors: site and date) indicated that the algal cover biomass collected in each sample differed greatly between dates (F=8·03, P<0·001), and that there were site per date interactions (F=6·15, P<0·001). Macroinvertebrate community abundance and descriptors A total of 38 benthic taxa, belonging to five phyla, were recovered and identified (Table 2). The most abundant taxon lagoon-wide was the snail Hydrobia sp., which constituted 20·4% (335 ind m
2) of the total macrofaunal abundance, followed by Chironomus salinarius (19·2%, 315 ind m
2), Corophium insidiosum (9·8%, 160 ind m
2) and Capitella capitata (8·8%, 144 ind m
2). The highest abundance of macroinvertebrate was found at site A (December,

7095 ind m
2), and the lowest in June at site A, and in February at site C (222 and 228 ind m
2 respectively). Two-way ANOVA of log-transformed abundance data (factors: site and date) showed that there were significant differences between sites (F=4·97, P<0·01), between dates (F=8·34, P<0·001), and that there were also higher order interactions (F=6·56, P<0·001). The number of taxa (S) caught each month ranged from 5 to 21 at site A, from 10 to 19 at site B, and from 7 to 14 at site C. At site A, both the highest (April, d=2·71) and the lowest (September, d=0·524) values of Margalef’s richness index were found. Conversely, sites B and C respectively had the highest (September, H =2·56, J =0·904) and the lowest (July, H =0·524, J =0·252) values of diversity and evenness indices. In Table 3, community parameters are reported. Variations in community parameter values were always found significantly different at site B. At site B, there was also a significant negative correlation between algal cover biomass and abundance, S, d, and H (1-way ANOVA, P<0·01). At the other two sites, covariate correlations were not significant. In Table 4, 1-way ANOVA and Tukey HSD test results for the three sampling sites are reported.

Macrobenthic community structure and production in a lagoon 609 T 2. Faunistic inventory and mean annual abundance (ind m
2) at the three sampling sites (SE: standard error) Site A

Site B

Site C

Taxon

mean

SE

mean

SE

mean

SE

Actiniaria Turbellaria Bittium reticulatum Hydrobia sp. Hinia reticulatus Cyclope neritea Haminoea hydatis Scapharca inaequivalvis Mytilus galloprovincialis Mytilaster minimus Crassostrea sp. Cerastroderma glaucum Tellina sp. Abra ovata Tapes philippinarum Polydora ciliata Prionospio multibranchiata Spio decoratus Streblospio shrubsolii Capitella capitata Heteromastus filiformis Mysta picta Phyllodoce linneata Neanthes succinea Nephtys hombergi Pectinaria koreni Ficopomatus enigmaticus Hydroides dianthus Oligochaeta Balanidae Idotea baltica Corophium insidiosum Gammarus sp. Microdeutopus gryllotalpa Brachynotus sexdentatus Palaemon elegans Carcinus aestuarii Chironomus salinarius

14·6 — 3·0 773·8 1·0 3·0 0·5 2·0 2·0 5·6 — 18·7 1·0 11·6 3·0 82·3 5·1 0·5 28·8 284·3 — 1·5 0·5 47·0 2·5 — 12·6 20·7 29·3 15·7 2·0 34·8 146·5 89·4 — — 0·5 930·8

8·4 — 1·8 164·7 0·6 3·2 0·6 1·5 1·1 3·4 — 3·5 1·3 2·6 1·1 36·3 4·3 0·6 23·3 22·0 — 1·4 0·6 19·2 2·6 — 16·2 19·6 34·9 8·2 1·7 7·9 65·1 66·1 — — 0·6 116·4

10·6 2·0 20·7 99·5 5·6 13·1 — 4·0 3·0 2·0 — 25·8 — 25·8 3·5 226·3 — — 91·4 87·4 0·5 2·5 — 73·7 1·5 0·5 2·0 10·1 53·0 81·4 3·5 152·0 64·6 76·8 0·5 0·5 2·0 83·3

1·6 2·0 3·9 24·9 1·3 2·9 — 1·1 1·5 0·6 — 5·3 — 6·0 1·1 50·8 — — 18·5 30·4 0·6 1·3 — 10·6 0·9 0·6 2·0 8·4 12·0 18·3 1·6 45·6 26·5 26·2 0·6 0·6 1·2 16·4

8·1 0·5 1·0 81·3 0·5 — — 1·5 3·0 — 0·5 21·2 — 3·0 7·6 15·2 2·0 — 15·7 66·7 — — 0·5 136·4 — — 38·9 163·6 252·5 9·1 — 331·8 15·7 5·1 5·1 — 40·9 16·2

3·3 0·6 0·9 50·9 0·6 — — 1·0 1·8 — 0·6 11·8 — 1·7 3·0 5·1 1·7 — 5·4 16·0 — — 0·6 11·8 — — 17·9 71·4 31·2 3·7 — 38·6 10·6 3·9 2·8 — 35·6 3·7

Multivariate analyses Ordination was performed on fourth root transformed abundance data. In Figure 3, MDS plot, with superimposed groups generated by cluster analysis (UPGMA on Bray-Curtis similarity matrix), is shown: a spatial segregation of the sample points reflecting a gradient of shelter or confinement is recognizable in the ordination, with most of the sample points from sites A, B, and C respectively on the left, on the middle, and on the right hand side of the ordination plane. A gross seasonal trend in the macrobenthic community structure, thus confirmed by analysing through non-metric MDS the three sites separately

(stress: A=0·11; B=0·12; C=0·12; plots not shown), is also evident. An analysis of the contribution from individual species abundance to the average Bray-Curtis dissimilarity between the three sites using the similaritypercentage analysis (SIMPER), showed that differences were mainly due to the average higher proportion of Chironomus salinarius, Hydrobia sp., and Capitella capitata at site A, and of Hydroides dianthus and Oligochaeta at site C. Average dissimilarity between sites A and B was 58·1%, between sites A and C was 63·2%, and finally between sites B and C was 56·9%. Species breakdown of similarities for each site showed that while at site A only 10 species

610 M. Mistri et al. T 3. Community parameters for each site at each sampling date Site

S

N

d

H

J

JAN FEB MAR APR MAY JUN JUL SEP OCT NOV DEC

8 9 13 21 20 12 6 5 8 9 9

467 483 2617 1589 2500 728 222 2078 6572 3978 7095

1·14 1·29 1·52 2·71 2·43 1·67 0·925 0·524 0·796 0·965 0·902

1·48 1·78 1·54 1·62 2·2 1·05 1·04 1 1·08 0·912 1·34

0·711 0·81 0·601 0·532 0·735 0·424 0·583 0·622 0·518 0·415 0·608

B

JAN FEB MAR APR MAY JUN JUL SEP OCT NOV DEC

10 10 15 18 17 19 14 17 18 10 13

856 894 339 1139 1622 822 4211 544 1011 1189 1006

1·33 1·32 2·4 2·42 2·16 2·68 1·56 2·54 2·46 1·27 1·74

1·46 0·603 2·18 2·05 2·02 2·44 1·51 2·56 1·92 1·85 1·92

0·635 0·262 0·803 0·71 0·713 0·827 0·571 0·904 0·666 0·805 0·749

C

JAN FEB MAR APR MAY JUN JUL SEP OCT NOV DEC

12 12 7 14 12 13 8 13 13 10 13

1517 228 244 839 783 811 1761 1572 2194 2178 1456

1·5 2·03 1·09 1·9 1·65 1·79 0·937 1·63 1·56 1·17 1·65

2·06 1·82 1·53 1·68 1·67 1·73 0·524 1·68 1·57 1·5 1·3

0·828 0·731 0·788 0·638 0·674 0·674 0·252 0·653 0·612 0·651 0·509

A

Month

S, total number of taxa present; N, total number of individuals m
2; d, Margalef’s richness index; H , Shannon-Wiener diversity index; J , Pielou’s evenness index.

contributed for >90% of this similarity, at sites B and C they were respectively 17 and 13. Two-way ANOVAs showed that the abundance of each of the 10 most important species which contributed to similarity within sites (contribution >5%: Bittium reticulatum, Hydrobia sp., Cerastoderma glaucum, Capitella capitata, Neanthes succinea, Ficopomatus enigmaticus, Hydroides dianthus, Oligochaeta, Corophium insidiosum, and Chironomus salinarius) differed significantly amongst months, and that the site per month interaction term was significant (Table 5), indicating that inter-site differences changed seasonally. Finally, all the aforementioned species but C. capitata showed a negative correlation with algal biomass, but only the abundance of C. glaucum was found to be significantly related (P<0·05).

The results of BIOENV analysis showed various degrees of correlation between log-transformed water variables and fourth-root transformed abundance of macrofauna: at site A, the highest rank correlation (R=0·391) occurred with the complete set of variables (dissolved oxygen, salinity, and temperature), indicating that abiotic parameters played a role in structuring the benthic community; at sites B (R=0·435), and C (R=0·620) it occurred with the only variable temperature, thus reflecting a seasonal effect. Macroinvertebrate biomass and secondary production Mean annual bottom fauna biomass was 62·1 g AFDW m
2. Bivalves contributed most to the biomass, with Cerastoderma glaucum constituting 56·3% of the total biomass (39·3 g AFDW m
2), followed by Scapharca inaequivalvis (17%, 11·8 g AFDW m
2), Tapes philippinarum (6·2%, 4·3 g AFDW m
2), and Mytilus galloprovincialis (5·4%, 3·7 g AFDW m
2). Comparing the three study sites (2-way ANOVA), annual biomass was significantly lower (F=3·73, P<0·05) at site A, and there were also site per date interactions (F=2·02, P<0·05). Mean annual biomass was 46·4 (14·8 SE), 73·6 (13·8 SE), and 66·3 (23·5 SE) g AFDW m
2 at site A, B, and C respectively. The range in production estimates was relatively consistent among the three sites. Total annual secondary production was estimated as 49·8, 75, and 71·3 g AFDW m
2 yr
1 at site A, B, and C respectively; annual P/B ratios were calculated as 1·07 (site A), 1·02 (site B), and 1·08 (site C). In Table 6, biomass and secondary production estimates, together with specific P/B ratios, are reported. Discussion With this study, we hypothesize that two different factors act to determine the structure and composition of the macrobenthic community in the Sacca di Goro. These are shelter or confinement and disturbance due to the presence of algal cover. Macrofauna community composition and distribution The species composition of the macrobenthic community in the Sacca di Goro seems quite similar to the situation previously found in other Mediterranean lagoonal ecosystems (Guelorget & Michel, 1979; Arias & Drake, 1994; Mistri et al., 2000), that is a limited number of species, a strong dominance in abundance by a few of these species, and a relatively low diversity. Seasonal patterns of macroinvertebrate abundance in temperate soft-bottom habitats have

Macrobenthic community structure and production in a lagoon 611 T 4. One-way ANOVA on macrobenthic community parameters at sites A, B, and C. Date was the categorical variable, and biomass of macroalgae in each replicate was the continuous variable. Mean values of the dependent variable in months joined by underline were significantly different at 5% level using Tukey HSD test Covariate Variable

Factor

F

P

r

F

P

Months

Site A N

0·339

ns


0·13

9·371

<0·001

A7

A1

A2

A6

A3

A4

A5

A8

A10

A9

A11

S

0·09

ns

0·07

2·841

<0·05

A5

A4

A3

A6

A10

A11

A1

A2

A9

A7

A8

d

0·252

ns

0·11

3·208

<0·05

A5

A4

A3

A6

A10

A11

A1

A2

A7

A8

A9

H

0·484

ns

0·15

1·369

ns

A5

A1

A2

A3

A4

A6

A7

A8

A9

A11

A10

J

0·315

ns

0·12

2·136

ns

A1

A2

A3

A4

A5

A6

A7

A8

A9

A10

A11

Site B N

8·046

<0·01


0·53

9·131

<0·001

B3

B8

B1

B6

B2

B4

B10

B11

B9

B5

B7

S

12·706

<0·01


0·61

3·76

<0·01

B5

B6

B4

B7

B8

B9

B10

B11

B1

B3

B2

d

9·929

<0·01


0·57

3·774

<0·01

B1

B2

B3

B4

B7

B9

B10

B11

B5

B6

B8

H

8·215

<0·01


0·53

7·906

<0·001

B6

B1

B2

B8

J

0·099

ns


0·07

5·698

<0·001

(*)

Site C N

2·437

ns


0·32

3·176

<0·05

C2

C3

C1

C4

C5

C6

C7

C8

C9

C10

C11

S d H

0·328 0·12 0·16

ns ns ns


0·12
0·08
0·09

1·29 1·089 3

ns ns <0·05

C1 C1 C7

C2 C2 C3

C3 C3 C4

C4 C4 C5

C5 C5 C8

C6 C6 C9

C7 C7 C11

C8 C8 C1

C9 C9 C2

C10 C10 C6

C11 C11 C10

J

0·009

ns


0·02

5·118

<0·001

C7

C11

C1

C2

C3

C4

C5

C6

C8

C9

C10

(*)

N: abundance; 2S: number of taxa; d: richness; H : diversity; J : evenness; r: covariate coefficient; ns: not significant. Month codes: A1, A2, . . . A11, January to December at site A, etc.; (*): all remaining post-hoc comparisons significantly different except with B2.

frequently been found, with a peak of abundance in spring and, sometimes, a second peak in autumn (Guelorget & Michel, 1979; Friligos & Zenetos, 1988; Castel et al., 1989; Kalejta & Hockey, 1991; Arias & Drake, 1994), and, at our study sites too, macrofaunal dynamics followed this general trend. Only at site A marked qualitative and quantitative impoverishment of the fauna was recorded from June onwards: it was apparent that some kind of stress resulted in a change in the community structure of benthic macroinvertebrates, also reflected as a depression of community indices. Immediately after summer impoverishment a higher abundance of individuals was recorded, supporting the observation that total density of individuals is higher in stressed areas due to adaptive strategies of opportunistic species that allow rapid local recruitment (Dauer et al., 1992). Macrobenthic

fauna at the other two study sites, on the contrary, showed less marked fluctuations in abundance and community parameters. Stress episodes were evident, and, at site B, were associated with abnormal algal growth. A scientific literature has been produced on the ecology of Mediterranean lagoons, focusing on the development of the concept of paralic (brackish) dominion centered on the notion of confinement. Guelorget and Perthuisot (1983) proposed the theory of confinement as a model to explain the zonation of benthic assemblages in coastal lagoons, thus indicating the turnover time of marine waters as the main parameter in governing biological gradients. The species distribution observed at our three sites seems to conform to this theory. A slightly increasing gradient of confinement or shelter seems to exist from

612 M. Mistri et al.

A7 B6

A1

B2

B5 C2

A3 B3 A4

B4

C3 A9

A5 C4

B1 A2

B8

C6 B7

B9

A11 A10

A8

C1

B6

B11

C5

C11 C10

B10

C7

C8

C9 Stress = 0.21

F 3. Non-metric multidimensional scaling ordination plot derived from fourth root transformed abundance data (sample points codes: A1, A2, . . . A11, January to December at site A, etc.). T 5. Mean squares (MS) and significance level (P) for 2-ways ANCOVA of the log-transformed abundance of the 10 most discriminating (through SIMPER analysis) species. Site (St) and Date (D) were categorical variables and the DW of macroalgae was the continuous variable

Covariate Species Bittium reticulatum Hydrobia sp. Cerastoderma glaucum Capitella capitata Neanthes succinea Ficopomatus enigmaticus Hydroides dianthus Oligochaeta Corophium insidiosum Chironomus salinarius

Interaction StD (20 df)

Main effects

P

r

Site (2 df) MS

ns ns <0·05 ns ns ns ns ns ns ns


0·08
0·09
0·29 0·14
0·18
0·07
0·08
0·17
0·15
0·1

3·99 20·36 1·29 5·31 6·38 1·96 5·52 11·95 4·6 7·5

site A to site B and C. The macrobenthic community at site A was characterized by a higher abundance of opportunistic species (e.g. small polychaetes), and by species dominant in stagnant waters (e.g. chironomid larvae); its higher sediment organic content may justify the higher abundance of opportunists (mainly Hydrobia sp. and Capitella capitata), and probably shows higher sedimentation rates, and thus accumulation of organic matter, associated with slow water movements. Conversely, the communities at site B and C were characterized by molluscs (bivalves and larger gastropods) and larger polychaetes (particularly Neanthes succinea), together with Oligochaeta and

P

Date (10 df) MS

P

MS

P

Residual (65 df) MS

<0·001 <0·001 <0·05 <0·001 <0·001 <0·01 <0·001 <0·001 <0·001 <0·001

0·56 3·03 1·46 2·9 0·63 0·44 1·04 2·45 2·88 8·56

<0·05 <0·01 <0·001 <0·001 ns ns ns <0·001 <0·001 <0·001

0·41 1·59 1·31 2·17 1·38 0·32 0·6 1·6 2·41 1·62

ns ns <0·001 <0·001 <0·001 ns ns <0·001 <0·001 <0·001

0·27 0·96 0·34 0·62 0·39 0·39 0·63 0·46 0·45 0·18

corophiid crustaceans. The community structure seems to change from larger-sized, more K-selected species, to small-sized, more r-selected taxa along a spatial gradient from the seamouth to the innermost area of the lagoon. This pattern could be explained as a consequence of the water dynamics at the three different sampling sites: site A was a low energy habitat, mainly due to slow water exchanges, whereas site C and, partially, B were most influenced by tidal currents (see Figures 8 and 9 in Brath et al., 2000). This statement is also confirmed by the higher sediment sand content, and by the mean annual lower salinity at site C, due to the inflow of freshwater from

Macrobenthic community structure and production in a lagoon 613 T 6. Mean annual biomass (B, gAFDW m
2) and secondary production (P, gAFDW m
2 yr
1) of the macrobenthic community at the three study sites Site A Taxon Actiniaria Turbellaria Bittium reticulatum Hydrobia sp. Hinia reticulates Cyclope neritea Haminoea hydatis Scapharca inaequivalvis Mytilus galloprovincialis Mytilaster minimus Crassostrea sp. Cerastroderma glaucum Tellina sp. Abra ovata Tapes philippinarum Polydora ciliata Prionospio multibranchiata Spio decoratus Streblospio shrubsolii Capitella capitata Heteromastus filiformis Mysta picta Phyllodoce linneata Neanthes succinea Nephtys hombergi Pectinaria koreni Ficopomatus enigmaticus Hydroides dianthus Oligochaeta Balanidae Idotea baltica Corophium insidiosum Gammarus sp. Microdeutopus gryllotalpa Brachynotus sexdentatus Palaemon elegans Carcinus aestuarii Chironomus salinarius

Site B

Site C

B

P

P/B

B

P

P/B

B

P

P/B

0·828 — 0·076 0·147 0·891 0·449 0·008 9·121 2·725 0·046 — 26·883 0·025 0·282 2·832 0·042 0·005 0·0005 0·015 0·145 — 0·012 0·0038 0·655 0·078 — 0·015 0·027 0·020 0·078 0·0036 0·0035 0·259 0·088 — — 0·037 0·642

1·912 — 0·169 0·762 0·957 0·643 0·032 7·476 3·021 0·130 — 22·128 0·083 0·889 2·153 0·299 0·038 0·004 0·108 0·994 — 0·046 0·016 1·629 0·220 — 0·084 0·137 0·123 0·309 0·019 0·022 1·134 0·528 — — 0·218 3·520

2·31 — 2·22 5·18 1·07 1·43 4·00 0·82 1·11 2·83 — 0·82 3·32 3·15 0·76 7·12 7·60 8·00 7·20 6·86 — 3·83 4·16 2·49 2·82 — 5·60 5·07 6·15 3·96 5·28 6·29 4·38 6·00 — — 5·89 5·48

0·600 0·0067 0·517 0·019 4·901 1·945 — 18·242 4·087 0·017 — 37·056 — 0·626 3·304 0·115 — — 0·047 0·045 0·0005 0·019 — 1·029 0·047 0·0005 0·0024 0·013 0·037 0·457 0·006 0·015 0·114 0·075 0·0028 0·048 0·147 0·058

1·443 0·052 1·123 0·108 5·159 2·751 — 15·109 4·619 0·050 — 31·166 — 1·986 2·580 0·822 — — 0·341 0·326 0·004 0·077 — 2·602 0·138 0·004 0·015 0·070 0·225 1·766 0·035 0·094 0·529 0·470 0·005 0·088 0·863 0·350

2·41 7·76 2·17 5·68 1·05 1·41 — 0·83 1·13 2·94 — 0·84 — 3·17 0·78 7·15 — — 7·26 7·24 8·00 4·05 — 2·53 2·94 8·00 6·19 5·38 6·08 3·86 5·83 6·27 4·64 6·27 1·79 1·83 5·87 6·03

0·514 0·0017 0·025 0·015 0·446 — — 6·841 4·087 — 11·196 30·516 — 0·074 7·080 0·0077 0·002 — 0·008 0·034 — — 0·0038 1·902 — — 0·047 0·213 0·174 0·045 — 0·033 0·028 0·005 0·028 — 2·986 0·011

1·188 0·013 0·057 0·085 0·482 — — 5·582 4·418 — 6·340 24·695 — 0·238 5·169 0·057 0·016 — 0·059 0·240 — — 0·020 4·520 — — 0·246 1·004 0·980 0·180 — 0·193 0·128 0·032 0·048 — 15·274 0·068

2·31 7·65 2·28 5·67 1·08 — — 0·82 1·08 — 0·57 0·81 — 3·22 0·73 7·40 8·00 — 7·38 7·06 — — 5·26 2·38 — — 5·23 4·71 5·63 4·00 — 5·85 4·57 6·40 1·71 — 5·12 6·18

the Po di Goro during high tide. Arias and Drake (1994) advanced the hypothesis that the species that dominate confined environments would be tolerant species but less competitive than marine species, and that they would be the most abundant only in sufficiently confined areas, where the environmental conditions would avoid high reproductive and immigration rates of marine species. Our observations give support to this hypothesis. Effect of macroalgae The biomass of algal cover is recognized as an important factor in determining the abundance of benthic

fauna in marine and lagoonal ecosystems: on the whole, the abundance of macrofauna is higher in zones with vegetative cover than in bare zones (Lewis, 1984; Edgar, 1990). A number of papers highlight the response of benthic algal communities to the impact of eutrophication, referring to the occurrence of excessive growths of macroalgae (a phenomenon commonly termed ‘ green tide ’) and the resultant detrimental ecological and environmental consequences (see review in Fletcher, 1996). The effects of accumulation and decomposition of huge biomasses of Ulva rigida on benthic communities are well known: subsequent dystrophic crises usually lead to massive mortality of benthic fauna (Sfriso

614 M. Mistri et al.

et al., 1985; Viaroli et al., 1992; Tagliapietra et al., 1998). The perennating Rhodophyta Gracilaria verrucosa is considered to be amongst the seaweeds which take advantage from eutrophication, and typically thrive with very high biomass in eutrophic environments (Charlier & Lonhienne, 1996). Our study sites were characterized by the presence of almost monospecific G. verrucosa populations, but with lower biomass than those reported elsewhere for other species (e.g. Ulva rigida: 15– 20 kg wet weight m
2; Sfriso & Marcomini, 1996). Modification of biotic interactions, such as predation and availability of food and living space (Lewis, 1984; Stoner, 1985), and of sediment characteristics (Kalejta & Hockey, 1991), are among the main effects that the presence of algal cover exert on macroinvertebrate communities. At sites A and C, where algal biomass never exceeded 150 g DW m
2, such effects were probably operating, but we did not find any significant correlation between G. verrucosa presence and macrobenthic community parameters. At site B, however, where an abnormal growth of the macroalgae (with biomass >1 kg DW m
2) was observed during the period of investigation, a significant negative correlation between G. verrucosa biomass and macroinvertebrate community parameters was found. The benthic community was not heavily impacted by such abnormal algal growth: in fact, probably because of the location of site B, within an area of the lagoon still influenced by water exchange with the sea, such growth of G. verrucosa was not followed by dystrophic events. The presence of G. verrucosa also had a negative influence on abundance of the dominant bivalve species at our study sites, Cerastoderma glaucum, probably by interfering with its filter-feeding activity. A similar pattern was observed by Everett (1991) in a central California lagoon, while Olafsson (1988) reported the inhibition of larval bivalve settlement by algal mats in a sheltered bay in Sweden. Since we collected only adult specimen of C. glaucum, such an interference could also be operating at our study sites. Macrofauna production Tumbiolo and Downing (1994) have adapted the Plante and Downing (1989) model to marine populations developing a general equation that includes the effect of environmental variables, like temperature and depth, which were supposed to have strong influence on marine benthos production. Although it is rather difficult to make detailed comparison among different studies and locations because of differences in sampling procedures, taxa considered, mesh size, and

the calculation method adopted, our production estimates are within the range of other figures found in similar environments by other authors (Wolff & De Wolf, 1977; Edgar, 1990; Fredette et al., 1990; Kalejta & Hockey, 1991; Arias & Drake, 1994; Heck et al., 1995). In natural populations and communities, the P/B ratio has been shown to decrease with the age of an organism, and depends on factors such as the age structure of the population and taxonomic group composition (Waters, 1979). Higher P/B values are to be expected for populations dominated by younger individuals, and for non-molluscan groups such as polychaetes (Moller, 1985) and crustaceans (Ceccherelli & Mistri, 1991), while low values are expected for long-living organisms (Mistri & Ceccherelli, 1994) and for bivalve species (Mistri et al., 1988). In the Sacca di Goro, community biomass was dominated by adult bivalves (Table 6), and this explains the relatively low values of our estimates of P/B ratio. The numerically dominant, smaller organisms, despite their high abundance, contributed very poorly to the community production. On the other hand, since P/B declines with body size (Saiz-Salinas & Ramos, 1999), such species exhibit higher renewal rates and are more resilient to environmental perturbations (Tumbiolo & Downing, 1994). Specific contribution to community secondary production is directly proportional to body size and metabolic rate (Peters, 1983). The role of Cerastoderma glaucum seems to be crucial in structuring the community functioning at our study sites. Bivalves are slow-growing and long-lived organisms, which sustain high biomass over long times, and may be considered a biomass sink (Schwinghamer, 1983). Considering their low P/B ratio, and their reduced biological and ecological ability to survive after catastrophic decline, Tumbiolo and Downing (1994) predicted that marine biodiversity will be lost first in the largest organisms when communities are perturbed or environmental conditions are degraded. The fact that, at our study sites, most of the biomass (and, thus, a large part of the secondary production) was due to bivalves is a feature that probably means that environmental and biotic disturbance in the Sacca di Goro is not so harsh (at least in the study year) to prevent the existence of such K-selected populations. Several authors (Cloern, 1982; Rodhouse & Roden, 1987; Nore´ n et al., 1999) showed that in shallow estuarine habitats suspensionfeeder bivalves may be a controlling factor for the phytoplankton, while the stabilizing properties of such organisms have been discussed by Herman and Scholten (1990). We too hypothesize that C. glaucum

Macrobenthic community structure and production in a lagoon 615

(together with the other bivalve species present at our study sites) may play a role in stabilizing the system by storing energy in large individuals where the respiration per unit biomass is far lower than in other species. From a functional point of view, these bivalve species could be stabilizing because (a) they were permanently present in the Sacca, at least in the year of study, (b) it is known that their filtration rate does not level off with increasing food availability (Newell & Bayne, 1980), and thus they may exert a top-down control on phytoplankton, and (c) they have a low biomass turnover rate. It has been argued (Ott & Fedra, 1977) that storage of energy and nutrients in such large animals with low maintenance costs stabilizes the ecosystem, and, from the results of this study, this could be the case of the Sacca di Goro. The reverse of the model is that a sudden change in the suspension-feeders biomass may have dramatic consequences: an ecosystem stabilized by its suspensionfeeders is also most vulnerable to whatever happens to the suspension-feeders themselves (Herman & Scholten, 1990). Long-term studies are needed, however, to distinguish meaningful change from mere local variations in the overall structure and interactions in benthic assemblages in the Sacca di Goro. Conclusions In the Sacca di Goro, a horizontal biological zonation of the macrobenthic community along a gradient of confinement or shelter was observed. The community of the innermost area (site A) lived in almost stagnant waters and its species composition and abundance reflected such stressful environmental conditions. The benthic fauna of the central (site B) and, specially, of the eastern (site C) area of the Sacca, being more influenced by tidal waters, were characterized by different community composition and dynamics. At the three sites, the macroalgae Gracilaria verrucosa was present during all over the year even if in different amounts. Site B, which also experienced the heaviest algal biomass growth, was characterized by quite wide fluctuations of algal cover. But, on the whole, the benthic community at this site exhibited higher values of richness, diversity, and evenness. Such algal cover biomass fluctuations could be interpreted as perturbation events, but the appreciable water movement at this site probably made such perturbations ‘moderate’. Moderate disturbance could limit the competitive advantages of potentially dominant species (those which numerically dominate at site C) causing a rather high degree of community richness, diversity, and evenness (Huston, 1979). The patterns of the benthos in the Sacca di Goro exhibit the resilience

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