Dottorato di ricerca in Scienze Ambientali Scuola di dottorato in Scienze e Tecnologie Ciclo XXIII (A.A. 2009 - 2010) Multiscale dynamics of zoobenthic communities and relationships with environmental factors in the Lagoon of Venice SETTORE SCIENTIFICO DISCIPLINARE DI AFFERENZA : BIO/07 Tesi di dottorato di Marco Sigovini, matricola 955529 Direttore della Scuola di dottorato Tutore del dottorando Prof. Paolo Ugo Prof. Annamaria Volpi Ghirardini Co-tutore del dottorando Dott. Davide Tagliapietra The thesis project was conducted under the supervision of the Ca' Foscari University of Venice (prof.ssa Annamaria Volpi Ghirardini) and the Laboratory of Benthic Ecology of CNR-ISMAR (dott. Davide Tagliapietra). The aim of the thesis is to outline the spatial and interannual variability of the macrozoobenthic community and the structuring environmental factors in a typical estuarine lagoon. The study site is the Lagoon of Venice. The activities included a six-month period at the University of Murcia (Spain), under the supervision of prof. Angel Pérez-Ruzafa (Ecology and Management of Coastal Marine Ecosystems Research Group). INDEX 1. INTRODUCTION 3 1.1 Coastal transitional ecosystems 3 1.2 The bioindication in coastal transitional ecosystems by means of macrozoobenthos community 5 1.3 CTE as naturally stressed environments: the "Estuarine Paradox" 10 1.4 Dependence of the benthic community on environmental structure in CTE, with focus on estuarine lagoons 12 1.4.1 Salinity 13 1.4.2 Organic enrichment 14 1.4.3 Confinement 16 1.4.4 Biological factors: larval dispersion and colonization 19 1.5 Multiple scales in structure and functioning 20 1.6 The Lagoon of Venice 22 1.7 Brief overview of macrozoobenthos studies and monitoring in the Lagoon of Venice 24 2. OBJECTIVES 27 3. MATERIALS AND METHODS 29 3.1 Study area 29 3.1.1 Notes on hydrogeological zonation 30 3.1.2 Notes on tidal zonation 23 3.2 Environmental data sets 34 3.2.1 Sediment 35 3.2.2 Macrophytes 37 3.2.3 Intertidal surface 37 3.2.4 Hydrodynamics 37 3.2.5 Hydrological variables 38 3.3 Macrozoobenthos data sets 41 3.3.1 Source of the data: the MELa projects 41 3.3.2 Sampling and laboratory activities 42 3.3.3 Taxonomic list 43 3.3.4 Trophic groups 43 3.3.5 Operational data sets 43 3.4 Statistical tools: the R software environment 44 3.5 Spatial and interannual patterns of macrozoobenthos community at the lagoon scale 44 3.5.1 Univariate descriptors 45 3.5.2 Dominant taxa 46 3.5.3 Taxonomic and trophic composition 46 3.5.4 Analysis of hydrogeological zones 46 3.5.5 Analysis of multivariate structure 47 3.6 Relationships between macrozoobenthos community and environmental factors at lagoon scale 54 3.6.1 Normality and data transformation 54 3.6.2 Standardization 54 3.6.3 Explorative analysis of environmental factors 54 3.6.4 Relationship of univariate macrodescriptors of community to environmental data 55 3.6.5 Relationship of multivariate structure of community to environmental data 55 3.7 Spatial structures and multiscale analysis 57 4 RESULTS 67 4.1 Taxonomic list 67 4.2 Spatial and interannual patterns of macrozoobenthic community at the lagoon scale 69 4.2.1 Univariate descriptors 69 4.2.2 Dominant taxa 73 4.2.3 Taxonomic and trophic structure 75 4.2.4 Multivariate analysis 78 4.2.5 Analyses on hydrogeological zones 86 4.2.6 Cluster analysis 93 4.2.7 Ordinations constrained on basins, hydrogeological zones and years 104 4.3 Relationships between macrozoobenthos community and environmental factors at lagoon scale 111 4.3.1 Environmental variables data sets: exploratory analysis and collinearity 111 1 4.3.2 Operational data sets of environmental variables 118 4.3.3 Univariate macrodescriptors of community 122 4.3.4 Relationship of multivariate community data to environmental data 125 4.4 Spatial structures and multiscale analysis 132 4.4.1 PERMANOVA with nested design 132 4.4.2 Multi-Scale Ordination and relationship of main taxonomic groups to environmental variables 134 4.4.3 Spatial predictors: linear and PCNM models 138 5 DISCUSSION AND CONCLUSION 149 5.1 What is the variability over the years of the macrozoobenthic community structure at the whole lagoon scale? 149 5.2 On the bases of the hydrogeological zonation, what is the spatial and interannual variability of the benthic community? 152 5.3 Which is the role of environmental factors in structuring benthic communities? 155 5.4 What are the spatial scales of variability of the community, also in relationship to variability scales of environmental factors? 159 5.5 Final considerations and perspectives 163 ACKNOWLEDGMENTS 165 REFERENCES 167 LIST OF ABBREVIATIONS 185 APPENDICES 187 1 R Script: Recursive k-means algorithm (see Chapter 3.7) 2 List of taxa (see Chapter 4.1) 3 Interpolated maps of A, B and S for 2002, 2003, 2007 (59-station data sets) (see Chapter 4.2.1) 4 Dominant taxa (see Chapter 4.2.2) 5 Interpolated maps of selected environmental variables for 2002 (see Chapter 4.3.1) 2 Ch. 1 1. INTRODUCTION 1.1 COASTAL TRANSITIONAL ECOSYSTEMS Estuaries, rias, fjords, coastal lagoons, bahiras, river mouths, tidal creeks, deltas and similar coastal environments are often regarded as a single broad conceptual class (e.g. Guelorget & Perthuisot, 1983; Kjerfve, 1994; McLusky & Elliott, 2007). These water bodies are located within the coastline (e.g. lagoons, fjords) or cross through it protruding into the sea (e.g. deltas). Most of these nearshore, protected environments are related to the main estuarine and lagoonal types. "Brackish", "paralic" and "transitional" are the more inclusive terms used to designate collectively this class of environments. These terms also reveal the environmental models where they originated: "brackish" stresses the importance of freshwater inflow and seawater dilution, "paralic" underlines the proximity of the sea and the role of the marine component, "transitional" points out the presence of gradients and ecotonal traits. Nevertheless every term, generated from different historical perspectives and scientific points of view, excludes some of the above-mentioned environments (Tagliapietra et al. , 2009). A diagram showing relationships between the terms is presented in Figure 1.1. The term "Coastal Transitional Ecosystem" (CTE) has been proposed by Tagliapietra et al. (2009) with the intention of encompassing the whole class of environments, which in the same paper has been defined in a synthetic form as "coastal water bodies with limited seawater supply". Figure 1.1: Conceptual scheme of the relationships among the terms. The eccentricity of "estuarine system" set results from doubt about its applicability to rocky shores (Tagliapietra et al. , 2009). 3 Ch. 1 Estuaries, lagoons and other classes of CTE have many physical and ecological processes in common (Constable & Fairweather, 1999; Ketchum, 1983; McLusky & Elliott, 2004; Thrush & Warwick, 1997). The main physical factors that contribute to the genesis and characterization of CTE are climate, hydrodynamics and tidal range, coastal typology (Bird, 1994; Pethick, 1984; Tagliapietra & Volpi Ghirardini, 2006), as well as human action. The climate determines the hydrological balance through direct precipitation on the basins and evaporation, controlling the flow of the rivers which in turn cause erosion, sedimentation and the formation of alluvial plains. Climate directly and indirectly affects the saline balance and morphological processes (e.g. Nichols & Boon, 1994). The nature of the coast defines the horizon for the development of a lagoon. The relationships between coastal typology and tidal energy were described by Davies (1964), Hayes (1979), Davis & Hayes (1984). The tidal range determines a series of important features such as sediment dispersal patterns and sediment texture, morphology and residence time (Barnes, 1994b; Brambati, 1988; Kjerfve, 1994; Pethick, 1984). Microtidal low coasts, for example, are apt for coastal lagoon development, as they allow the formation of barrier islands whilst maintaining cyclical water exchange with the sea. The existence of characteristic tidal levels reflects in the vertical and horizontal development of typical landforms and consequently on the vertical and horizontal zonation of communities. In systems subjected to tides, ebbs and floods generate erosional and depositional processes that physically shape the substrate. Typical landforms/habitats, such as channels, subtidal flats, tidal creek and intertidal mudflats and salt marshes are structures generated principally by the tides (Albani et al. , 1984). Tides have a direct influence on emersion and submersion times and, consequently, on structure of intertidal biocoenoses. Vertical biological zonation is the result of physical zonation and biological interactions. CTEs are generated by the merging of sea, land and rivers and mark the passage between marine and non-marine realms. This merging gives rise to new, emergent properties shared by all these environments, including shallowness, shelter, the presence of strong gradients, variability in mesological parameters, prevalent sedimentary bottoms, high spatial heterogeneity in hydrological conditions, high biological production, susceptibility to anoxia and, generally, a significant departure of chemico-physical variables from the normal range of variation measured in the offshore waters or freshwater systems. This reflects on the communities structure and on the presence of a common set of species (Pérez-Ruzafa et al. , 2010; Tagliapietra et al. , 2009). Levin et al. (2001) highlighted their