AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS

Aquatic Conser�: Mar. Freshw. Ecosyst. 11: 281–287 (2001)

DOI: 10.1002/aqc.456

Changes and reco�ery of macrozoobenthic communitiesafter restoration measures of the Orbetello Lagoon

(Tyrrhenian coast, Italy)

CLAUDIO LARDICCI*, SERENA COMO, SERENA CORTI and FRANCESCA ROSSIDipartimento di Scienze dell’Uomo e dell’Ambiente, Uni�ersita di Pisa, Pisa, Italy

ABSTRACT

1. This paper describes the long-term dynamics of the macrozoobenthic communities in theOrbetello Lagoon, one of the largest Western Mediterranean lagoons, which was affected byeutrophication processes that began in the 1980s and peaked with two severe anoxic crises in 1992and 1993.

2. The aim of the present research was first to establish the characteristics of this basin prior tothe anoxic crises, and second to assess the recovery of the lagoon after various restoration measureswere completed in 1996. Investigations were carried out by studying macrozoobenthic communitiesin 4 years (1976, 1988, 1994, 1999) that were representative of the different (eu)trophic status in thelagoon.

3. Results of multivariate analyses indicated that each year was significantly different from theothers. The years 1976 and 1999 exhibited the highest number of species as compared with 1988 and1994. The majority of species characterizing the 1976 communities were marine taxa whereas 1988and 1994 showed a lower percentage of marine species and a higher percentage of opportunisticorganisms in comparison with 1976. The species assemblage in 1999 showed an intermediatecomposition between 1976 and 1988–1994.

4. Eutrophication processes caused a clear impoverishment of the macrobenthic communities in1988 and 1994. The increase in overall number of species during 1999 may have been due to improvedenvironmental conditions of the lagoon. However, the composition of the community suggested thatstill there were signs of disturbance in the lagoon in 1999, 6 years after the last intense anoxic crisesand even after completion of the environmental restoration measures.

5. It was hypothesized that secondary disturbance events, sustained by high seasonal release ofnutrients from the sediments, could cause the deviations from the expected improvement in benthicconditions.Copyright © 2001 John Wiley & Sons, Ltd.

KEY WORDS: anoxia/hypoxia; coastal lagoon restoration; macrozoobenthos; recovery; Western Mediterranean

INTRODUCTION

Many lagoon biotopes, especially along Italian coasts, have suffered increasing degradation in recentyears, on account of the increased discharge of effluents due to urbanization and aquaculture wastes

* Correspondence to: Claudio Lardicci, Dipartimento di Scienze dell’Uomo e dell’Ambiente, Universita di Pisa, Via A. Volta 6,I-56126, Pisa, Italy. E-mail: lardic@discat.unipi.it

Copyright © 2001 John Wiley & Sons, Ltd. Received 30 November 2000Accepted 22 March 2001

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(Sorokin et al., 1996; Lardicci et al., 1997). Such processes cause the progressive alteration of the lagoonfood webs. In the most severe cases, they led to the collapse of the ecosystem, resulting in the dominanceof pycocianobacteria and drastic depletion of all planktonic and benthic taxa, as was observed in theComacchio Lagoon system (Sorokin et al., 1996). However, to what extent coastal lagoon environmentsand their communities are threatened by eutrophication in many areas of Europe and how much time isneeded for recovery of the original conditions, is still unknown because of the lack of systematic studieson large spatial and temporal scales, despite the internationally acknowledged importance of theseecosystems (Council of European Communities, 1992; Barnes, 1995; Lardicci et al., 1997).

The Orbetello Lagoon, one of the largest Western Mediterranean brackish basins (2600 ha), supporteda rich species diversity at the end of the 1970s, mainly on account of the elevated heterogeneity of itshabitats (Cognetti et al., 1978). In addition, large meadows of marine phanerogams characterized thatlagoon. Over the following 15 years, the increase of urban waste water discharges (119 tonne year−1 ofnitrogen and 24 tonne year−1 of phosphorus) and aquaculture waste waters (37 tonne year−1 ofnitrogen and 1.2 tonne year−1 of phosphorus), due to the extensive development of tourism andaquaculture, caused marked changes in the environment. Summer dystrophic crises and algal bloomsincreased and marine phanerogams progressively disappeared. In 1992 and 1993, extended springmacroalgae (Cladophora �agabunda) blooms (4 kg m−2 wet weight) were followed by severe dystrophiccrises with fish mortality throughout most of the lagoon (Lardicci et al., 1997). In 1994, measures wereplanned in the attempt to remove the causes of the eutrophication of the lagoon, such as harvesting ofthe floating algae biomass, removal of all waste water inputs and sea channel enlargements by dredging.

The aim of this study was to compare the macrozoobenthic communities of the Orbetello Lagoon in 4different years (1976, 1988, 1994 and 1999) that were representative of its different (eu)trophic status toassess their recovery after the restoration measures (1995–1996), with respect both to the situation in1976 and to the years of the dystrophic crises (1988, 1994).

METHODS

Sampling methods and data analysis

Four stations (C, M, E, I), established on the basis of previous research as representative both of the seainlet neighbourhood and central areas of the Western and Eastern Lagoon sites, respectively (Lardicci etal., 1997), were sampled at intervals between March and December in 1999 (Figure 1). Three box-corersamples (225 cm2) were taken at each station. Replicates were sieved at 0.5 mm and preserved in 5%formalin. Macrofaunal organisms were sorted in the laboratory and identified to species level wherepossible. Data were compared with those recorded by previous studies at comparable stations in 1976,1988 and 1994. Three box-corer samples (225 cm2) were taken at each station in 1976 and 1994 whilethree van Veen grab samples (500 cm2) were taken at each station in 1988. All replicates in these 3 yearswere sieved at 0.5 mm (Cognetti et al., 1978; Morgana and Naviglio, 1989; Lardicci et al., 1997).

Presence–absence data of the species collected at each station for each year were used because noquantitative data were available from the investigations carried out in 1988. Formal significance tests fordifferences among the 4 years were performed using the one-way ANOSIM randomization/permutationtest from the Bray–Curtis similarity matrix (Clarke and Warwick, 1994). In addition, presence–absencedata were analysed using cluster analysis and the non-metric multi-dimensional scaling (nMDS)ordination based on the Bray–Curtis similarity matrix (Clarke and Warwick, 1994). Species making thegreatest contribution to dissimilarity between the different years were investigated by using the SIMPERprocedure (Clarke and Warwick, 1994).

Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser�: Mar. Freshw. Ecosyst. 11: 281–287 (2001)

RECOVERY OF LAGOONAL MACROBENTHIC COMMUNITIES 283

Figure 1. Sampling station in the Orbetello Lagoon. Each sampling station is indicated (C, E, I, M).

RESULTS

A total of 139 species represented by Polychaeta (74 species, 53.2%), Crustacea (30 species, 21.5%),Mollusca (25 species, 17.9%), Echinodermata (four species, 2.8%), Cnidaria (three species, 2.1%) andInsecta (three species, 2.1%) were recorded from the four stations over the 4 sample years.

Polychaeta diversity showed a decrease in 1988 in comparison with 1976, then exhibited a moderateincrease in 1994. In 1999, after completion of the lagoon restoration measures, Polychaeta species numberwas comparable with 1976. In particular, 1976 and 1999 exhibited the highest number of Syllidae whileno species were present at 1988 and only one taxon of this family was collected at 1994 (Table 1).Crustacea showed a more or less similar number of species throughout the 4 study years. The highestspecies number of Mollusca was observed in 1976 and the lowest in 1988 while a similar number of taxa

Table 1. Total number of species and taxa composition of macrozoobenthic community in eachsampling year

Number of species

1999199419881976

Total species 87 37 58 7645251843Polychaeta

21Mollusca 4 14 1110 14 1517Crustacea

1 23 2Echinodermata2 212Cnidaria

1Insecta 1 1 36Gasteropoda 415 2

Syllidae 1 1210 0

Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser�: Mar. Freshw. Ecosyst. 11: 281–287 (2001)

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were collected in 1994 and 1999. In particular, the highest number of Gastropoda was found in 1976(Table 1).

One-way ANOSIM showed significant differences among the 4 years (global R=0.884, p�0.001). Inparticular, pairwise comparison tests showed that each year was significantly different (p�0.05) from theothers. The nMDS ordination model confirmed the same pattern described above, with the station-pointsof each year grouped separately on the bidimensional plane of the plot except station M of 1994, whichwas close to the station I of 1976 (Figure 2).

The species accounting for the greatest contribution to dissimilarity among the 4 years (SIMPER,cut-off 60%) were 40 taxa of Polychaeta, 14 species of Crustacea, 12 species of Mollusca, three species ofEchinodermata, two species of Cnidaria and two species of Insecta. The majority of species thatdiscriminated 1976 samples in the SIMPER analysis were marine taxa with a lower percentage of so-calledopportunistic species indicating organic enrichment (Pearson and Rosenberg, 1978) (Table 2).Furthermore, 11 marine species, among which some species of Syllidae (Sphaerosyllis bulbosa, Syllideslongocirrata, Syllides prolifera), Phyllodocidae (Eulalia sanguinea, Phyllodoce �ittata) and Gastropoda(Cerithium �ulgatum, Hexaplex trunculus) associated with phanerogam meadows and fine sand, werepeculiar of that year only. In 1988 and 1994, a lower percentage of the marine organisms and a higherpercentage of the opportunistic ones in comparison with 1976 was observed while species contributing todissimilarity in 1999 exhibited an intermediate situation between 1976 and 1988–1994 (Table 2). The year1999 was also characterized by 11 species, among which two species of Syllidae (Eusyllis assimilis,

Figure 2. nMDS ordination model of presence–absence data. Stress=0.11. Symbols of each sampling year: �, 76; �, 88; �, 94;�, 99.

Table 2. Percentage differences (� and � ) of three different groups obtained by presence–absencedata of species which contribute to dissimilarity (cut-off 60%) between Bray–Curtis clusters at each

sampling year (SIMPER)

1976 1988 1994 1999

Marine species 73 � 50 � 52.3 � 57.721.15 �Opportunistic species 42.3 � 35.3 � 31.1

11.2�12.4�7.7�Brackish species 5.85

Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser�: Mar. Freshw. Ecosyst. 11: 281–287 (2001)

RECOVERY OF LAGOONAL MACROBENTHIC COMMUNITIES 285

Exogone naidinae) and two opportunistic species (Cirriformia tentaculata, Heteromastus filiformis), hadnot been recorded in any previous samples.

DISCUSSION

In Mediterranean coastal lagoons the macrozoobenthos is represented mainly by three groups ofspecies: a group of marine species commonly found in coastal semi-enclosed areas or associated withphanerogam meadows which prefer low hydrodynamic environments such as bays or harbours, agroup of so-called opportunistic species with high tolerance to organically enriched sediment, and agroup of typically euryhaline brackish-water species which are characteristic of lagoon zones (inter aliaGravina et al., 1989). The Orbetello Lagoon has been always characterized by a higher number ofmarine species in comparison with many other coastal lagoons (Cognetti et al., 1978) because thisbasin is a poly-hyperhaline lagoon, whose salinity values do not represent a boundary for manymarine species (Giangrande et al., 1984). Even in the inner areas, values below 20 PSU were veryrarely recorded (Lardicci et al., 1997). However, modifications of macrozoobenthic assemblages duringthe different 4 years provide evidence of sharp changes of environmental conditions in the OrbetelloLagoon over the last 20 years. These data confirm that 1976 was representative of the situation priorto the increasing organic enrichment of the lagoon and is an appropriate basis for comparison withthe other study years. In both 1988 and 1994 there was a decrease in the marine component ofPolychaeta (especially Syllidae), and Gastropoda diversity also exhibited a drastic reduction. Thesetaxa are known to be less tolerant to anoxic conditions (Lardicci et al., 1997) and many of them,being typically associated to phanerogams, suffered as a result of the decrease of seagrass meadowsover most of the lagoon habitat. Species such as the Gastropoda C. �ulgatum and H. trunculus werefound as a thanatocenosis in the lagoon sediment in 1994 by Lardicci et al. (1997).

Dissimilarity between 1988 and 1994 and the other 2 years (1976 and 1999) was due to the higherpercentage of opportunistic species. Throughout the 1980s and early 1990s, the Orbetello Lagoon wascharacterized by a sharp rise in organic enrichment caused by the increase of anthropogenic wastespoured in the basin, coming from the touristic and aquaculture activities. The pronounced springdevelopment of macroalgae biomass (mostly C. �agabunda) and its subsequent summer decompositioncausing anoxia and reduced conditions in the sediment was the dominant disturbance impact in thoseyears (Lardicci et al., 1997).

In 1999, after completion of restoration measures in 1996, an increase in total species numberoccurred and it was mainly due to higher Polychaeta diversity. In particular, in 1999 Syllidae showeda species number comparable with that of 1976. This increase in species number could be reasonablyattributed to the improved environmental conditions in the lagoon. However, the high percentage ofopportunistic species still present at 1999 and the low number of gasteropoda recorded in 1999 incomparison with 1976 indicate that the conditions of the lagoon during 1970s had not yet beenrecovered.

The benthic recovery processes observed in the Orbetello Lagoon after the removal of waste watersare similar to those observed by Karakassis et al. (1999) at an intensive aquaculture site in CephaloniaBay, Greece, after the removal of fish cages. In that case the values of geochemical sediment variablesshowed wide fluctuations, indicating incomplete recovery of the environment during the twosubsequent years of observations. Furthermore, the macrozoobenthic community at the aquaculturesite was still composed of opportunistic species 23 months after the removal of the cages. Seasonalrelease of nutrients from farm sediments triggered blooms of benthic algae and the subsequent decayof organic matter led to reduction of oxygen and redox values in the sediment, thereby creating

Copyright © 2001 John Wiley & Sons, Ltd. Aquatic Conser�: Mar. Freshw. Ecosyst. 11: 281–287 (2001)

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adverse conditions for macrofauna, at least for part of the year (Karakassis et al., 1999). In theOrbetello Lagoon, evidence of seasonal high release of nutrients from sediments was provided byCartei et al. (1998). These authors, sampling 23 stations fortnightly over 2 years, observed thatnutrient release from sediments peaked in winter (January–February), was synchronous in all stationsalthough not of the same entity in different areas of the lagoon, and was independent of thepresence/absence of sewage discharges. Nutrient production sustains primary production in latewinter–spring. In the Orbetello Lagoon such nutrient release probably sustains production ofmacroalgae with a short vegetative period (C. �agabunda). The presence of a high percentage ofopportunistic species in 1999 compared with 1976 was probably due to such phenomena.

Recovery processes may depend on several factors, among which the spatial and temporal scales ofthe disturbance, the type of stress and the hydrodynamism of the disturbed areas. Consequently, thetime needed for full recovery can vary considerably, ranging from 5 to 14 years in some organicallyenriched marine environments (Karakassis et al., 1999). In Mediterranean coastal lagoons, the lack oflong-term studies on the dynamics of macrobenthic communities makes it difficult to estimate the timeneeded for full recovery of these systems after disturbance events. The Orbetello Lagoon, a basin withpoor water circulation where stress due to organic enrichment has influenced the habitats along largespatial and temporal scales, still showed signs of disturbance in 1999, well 6 years after the lastextended anoxic crisis and even after completion of the environmental restoration measures in 1996.

Secondary disturbance events, basically autochtonous and sustained by organic degradation withinsediments that had been organically enriched for a long time, can maintain adverse environmentalconditions. Future management strategies of the coastal lagoons must take such processes intoaccount, especially in the Mediterranean basins where human exploitation of aquaculture and touristresources should always be linked with conservation of the natural habitats.

ACKNOWLEDGEMENTS

This work was supported by a grant (1999) of the Ministero dell’Universita e Ricerca Scientifica e Tecnologica, Italy,as a part of a national study on Italian coastal lagoons. The authors would like to thank two anonymous referees fortheir critical reading of the manuscript.

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