Functional structure of marine benthic assemblages ...

Estuarine, Coastal and Shelf Science 96 (2012) 245e256

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Functional structure of marine benthic assemblages using Biological Traits Analysis (BTA): A study along the Emilia-Romagna coastline (Italy, North-West Adriatic Sea) Daniele Paganelli*, Agnese Marchini, Anna Occhipinti-Ambrogi Department of Earth and Environmental Sciences, University of Pavia, Via S. Epifanio 14, 27100 Pavia, Italy

a r t i c l e i n f o

a b s t r a c t

Article history: Received 18 January 2011 Accepted 7 November 2011 Available online 15 November 2011

The functional diversity index has shown that the functional diversity of the macrobenthic community increased along a spatial gradient of distance from the Po river delta (Emilia-Romagna coast, Italy, NorthAdriatic Sea), which suggests that riverine inputs have a detrimental effect on community functioning. This study focuses on two different depths along a southward gradient of increasing distance from the Po river delta where the Po river is the main source of freshwater and nutrient inputs in the North-Adriatic Sea. A Biological Traits Analysis (BTA) was used to examine a dataset of 156 soft-bottom macrobenthic species that were collected at eight stations in this area. Instead of comparing communities on the basis of their taxonomic composition, BTA uses a series of life history, morphological and behavioural characteristics of species to indicate aspects of their ecological functioning. The variability of the EmiliaRomagna dataset was governed by relatively few biological traits: growth form, trophic group, type of movement, habit, adult mobility and bioturbation activity. The community closer to the coastline was mainly composed of moderately mobile vermiform organisms with burrowing or tube-dwelling behaviour, and deposit feeding behaviour. However, the offshore community was mainly characterized by organisms with a laterally compressed or globose body and tube-dwelling behaviour; filter feeders and deposit feeders were dominant. ! 2011 Elsevier Ltd. All rights reserved.

Keywords: Adriatic Sea macrobenthos biological traits analysis community functioning

1. Introduction The Northern Adriatic Sea is a shallow, semi-enclosed marine region characterized by moderate tides and is strongly influenced by the Po river runoff that induces a well known marine current. Since the 1970s, the Po river has been regarded as one of the main causes of eutrophication and environmental degradation in the North-West Adriatic Sea (Vollenweider et al., 1992; Justic et al., 1995; Mingazzini and Thake, 1995; Cozzi et al., 2005). The main effects of the Po inputs are: increased nutrient load, high trophic state, significant haline stratification and changes in the sediment texture of the coastal area. The direct consequence of eutrophication is a pathological condition of hypoxia in the sediment that leads to the reduction or disappearance of sensitive organisms (Vollenweider et al., 1992; Grall and Chauvaud, 2002).

* Corresponding author. E-mail address: [email protected] (D. Paganelli). 0272-7714/$ e see front matter ! 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2011.11.014

The benthic community of the North-Adriatic coast has long been studied at population (Ambrogi et al., 1995) and community level (Ambrogi, 1989; Ambrogi et al., 1989, 1990; Moodley et al., 1998; Occhipinti-Ambrogi et al., 2002, 2005; Forni and Occhipinti-Ambrogi, 2007; N’Siala et al., 2008; Paganelli and Forni, 2008), following a taxonomic approach. These studies showed a relationship between changes in taxonomic composition in the soft-bottom community and environmental parameters. The macrobenthic community in the Adriatic Sea displays a high capacity to thrive and adapts to the peculiar environmental conditions of the area; it is characterized by a high abundance of a few dominant species (the bivalve Corbula gibba and the crustacean Ampelisca diadema), which are occasionally subjected to demographic blooms, and by a lower abundance of many other species (Occhipinti-Ambrogi et al., 2002, 2005; Forni and Occhipinti-Ambrogi, 2007; N’Siala et al., 2008; Paganelli and Forni, 2008). However, there is a lack of knowledge regarding the functional structure of these communities and the relationship between functional structure and gradients of environmental change.

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D. Paganelli et al. / Estuarine, Coastal and Shelf Science 96 (2012) 245e256

The functional structure of a community can be represented by a set of traits describing behavioural and morphological characteristics displayed by the observed species. The traits and their interactions both determine the functioning and stability of communities and ecosystems (Loreau et al., 2001), and provide information about how communities respond to environmental stress (Lavorel and Garnier, 2002). Therefore, to give a comprehensive description of communities and ecosystems, Biological Traits Analysis (BTA) should be combined with taxonomic analysis (Diaz and Cabido, 2001; Villeger et al., 2010). BTA is based on the assumption that phylogenetically unrelated organisms might have evolved similar biological adaptation, thus leading to functional similarity, combined with taxonomic dissimilarity (Dolédec and Statzner, 1994; Usseglio-Polatera et al., 2000). Nevertheless, organisms that perform similar ecological roles may not always respond to stressors in the same way as, although they share some important attributes, they are likely to differ in other, more subtle ways (Ramsay et al., 1998). Functional diversity, i.e. the diversity of species traits, is an important property of a community as it measures the role organisms have in communities and ecosystems (Schleuter et al., 2010). The relationship between environmental change and functional diversity within a community is still uncertain for many ecosystems, especially marine habitats (Dolédec and Statzner, 1994; Micheli and Halpern, 2005; Petchey and Gaston, 2006). Therefore, the measurement of functional diversity by means of appropriate indices can help to understand how the community reacts to environmental changes (Dolédec and Statzner, 1994; Lep"s et al., 2006; Flynn et al., 2009; Loiola et al., 2010; Schleuter et al., 2010; Wan Hussin et al., 2011). In order to perform a BTA, information is needed about the biological traits of all the species in a community. Unfortunately, there is much less information on soft-bottom marine macrobenthos than on freshwater macrobenthos (Chevenet et al., 1994; Dolédec and Statzner, 1994; Charvet et al., 2000; Statzner et al., 2004), and the available information is sometimes contradictory. This is one of the problems with applying BTA to coastal environments (Bremner et al., 2003; Tillin et al., 2006; Marchini et al., 2008). BTA and functional diversity consider a range of biological characteristics expressed by each species in a community, thus they deal with a multi-dimensional cloud of points in trait space, where coordinates correspond to various traits (Schleuter et al., 2010). Therefore, specific tools are required to measure the functional diversity of communities and to compare communities according to their functional structure instead of their taxonomic composition. A multivariate approach for the analysis of biological traits of benthic communities was proposed by Statzner et al. (1994) for freshwater macrofauna. Further applications of this approach to coastal and marine benthic communities have mainly been in North-European countries (Bremner et al., 2003; Larsen et al., 2005; Tillin et al., 2006; Cooper et al., 2008; Frid et al., 2008; Jones and Frid, 2009; Boström et al., 2010; Aarnio et al., 2011; Barrio Froján et al., 2011; Wan Hussin et al., 2011), and there have been very few studies on Mediterranean communities (De Juan et al., 2007; Marchini et al., 2008; Pranovi et al., 2008). Here, BTA is applied to marine communities of the North-Adriatic sea, following a southward gradient of increasing distance from the Po river delta. This study aims to improve the overall knowledge of the macrobenthos of this coastal region providing information on another characteristic of the benthic assemblages, namely their functional structure. The research focuses on two aspects: (i) the dominant traits of the benthic assemblages and (ii) the differences between the functional structure of macrobenthic communities at different levels of depth and distance from the delta of the Po river.

2. Material and methods 2.1. Study area and sample collection Emilia-Romagna is one of the administrative regions of Italy and comprises 130 km of coastline in the North-West Adriatic sea (Fig. 1). Its northern border follows the course of the longest Italian river, the Po, which flows 652 km eastward across northern Italy and has a densely populated and highly exploited drainage area of 74,000 km2. Struglia et al. (2004) indicated that 57% of discharge in the Adriatic Sea is mainly due to this river, which reaches 2000 m3 s!1 in spring and autumn. Other smaller river systems in the Emilia-Romagna region also contribute to the nutrient enrichment of its shallow sandy coasts. In order to compare the functional structure of the benthic community at different depths and distances from the Po river mouth, 24 samples were collected during three seasonal surveys (May, July and October) along two levels of depth and four different distances from the Po. Samples were collected at four localities, from North to South: Porto Garibaldi (PG), Lido Adriano-Ravenna (RA), Cesenatico (CE), Cattolica (CA), along two parallel transects, placed 3 km offshore at 9 m depths and 10 km offshore at 14 m depths (Fig. 1). The labelling of single samples followed three criteria: (i) capital letters identify localities; (ii) presence or absence of the letter “n” identifies stations (two depth levels for each locality, where the letter “n” indicates the 3 km set and its absence indicates the 10 km set); (iii) a number indicates seasonal samples, and directly refers to the sampling month. For example, the label nPG7 indicates the sample collected at Porto Garibaldi, at 3 km, in July, while CA10 indicates the sample collected at Cattolica, at 10 km, in October. For each sample, five replicates were collected using a 0.06 m2 Van Veen grab. Four replicates were sieved through 1 mm size mesh and preserved in a formaldehyde seawater solution (10%) for further biological analyses. The fifth replicate was frozen for granulometric analysis of the sediment. In the laboratory, the benthic community was identified to species level, and sediments were separated into four classes according to particle size, following Buchanan’s methodology (Buchanan, 1984): Sand (>150 mm), Very Fine Sand (150e163 mm), Coarse Silt (62.9e15.6 mm) and Fine Silt/ Clay ( 0.05) and seasons (DF ¼ 2; F ¼ 0.67; p > 0.05). The interaction between the two factors was not significant (DF ¼ 2; F ¼ 1.42; p > 0.05). To explain the results of these ANOVA tests, we hypothesized that the

Table 3 Comparative table between macrobenthic functional compositions at different depths. Stations Distance from Modalities the coast nPG nRA

3 km

$ $ $ $ $ $ $ $ $

Globose growth form (mod. Gl) Filter feeders (mod. SF) Burrow dweller (mod. Bd) Moderately mobile (mod. DiscM) Sexual gonocoric reproduction technique (mod. Sex_G) Planktotrophic larval stage (mod. Pl) Long life span (mod. Lg) Tolerant (mod. III) and second-order opportunistic species (mod. IV) Sandy mud substratum (mod. SM)

nCE nCA

3 km

$ Vermiform growth form (mod. Vf) $ Carnivore-omnivore (mod. CO) or sub-surface deposit feeders (mod. SsdF) $ Mobile organisms (mod. Mob) $ Hermaphrodite (mod. Sex_H) $ Sensitive species (mod. I) $ Sandy bottoms (mod. CCS/FCS)

CE7 PG10 PG7 CA7

10 km

$ Dorso-ventral growth form (mod. DVc) $ Filter feeders (mod. SF) $ Direct development (mod. Dd)

RA7 PG6 RA10 CA10 CE10 CA6

10 km

$ $ $ $

RA6 CE6

10 km

$ Laterally compressed growth form (mod. Al) $ Tube dweller (mod. Td) or swimmer (mod. Sw) $ Indifferent species (mod. II)

Fig. 5. a. Spearman correlation values between FD index values and the distance from the Po river mouth of each sample (expressed in km). b. Spearman correlation values between Shannon diversity index (H0 ) values and the distance from the Po river mouth of each sample (expressed in km).

FD index strongly responded to a spatial gradient of distance from the Po delta. A Spearman correlation analysis was carried out to verify the relationship between both FD and Shannon diversity indices with the distance from the Po river delta. The results showed a positive correlation (r ¼ 0.473*, p < 0.05) between FD and distance from the Po (Fig. 5a); whereas the correlation between

Sessile species (mod. Sd) Lecitotrophic larval stage (mod. Le) Medium life span (mod. Md) Muddy bottoms (mod. Mu)

Fig. 6. Spearman correlation values between percentage of Very Fine Sand (VFS) and the 22 modalities which explain the most variability on the first two axes of the Correspondence Analysis. See Table 1 for labels.

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Fig. 7. Spearman correlation values between percentage of Coarse Silt (CS) and Fine Silt/Clay (FSC) and the 22 modalities which explain the most variability on the first two axes of the Correspondence Analysis. See Table 1 for labels.

Shannon diversity and distance followed a negative trend (r ¼ !0.715**, p < 0.001) (Fig. 5b). 3.5. Correlation between traits modalities and sediment composition Spearman correlation analyses were carried out to verify the significance of the relationship between sediment composition and the frequency of each modality in each sample. We correlated the percentage of the principal sediment component at 3 km, Very Fine Sand (VFS), and the principal components at 10 km, Coarse Silt (CS) and Fine Silt/Clay (FSC), to only 6 traits (22 modalities in total) that were responsible for most of the variability on the first two axes of the FCA: growth form, trophic group, type of movement, habit, adult mobility and level of bioturbation. Eight of the twenty-two modalities were significantly correlated with the percentage of Very Fine Sand: ‘vermiform’ body shape (Vf, r: 0.708**); the trophic groups ‘surface deposit feeders’ (SdF, r: 0.487*) and ‘sub-surface deposit feeders’ (SsdF, r: !0.66*); ‘burrower’ movement (Bu, r: 0.42*); ‘burrow dwelling’ habit (Bd, r: 0.667**); ‘surface deposition’ (SD, r: 0.703**), ‘conveyer belt transport’ (CbT, r: 0.518**) and absence of bioturbation (noB, r: 0.455*). All of these correlations were positive, except for the modality ‘sub-surface deposit feeders’, which followed an inverse trend (Fig. 6). Only four modalities were significantly correlated with the percentage of Silt and Clay (CS and FCS): ‘vermiform’ body shape (Vf, r: 0.55**); the trophic group ‘surface deposit feeders’ (SdF, r: !0.433*); ‘burrow dwelling’ habit (Bd, r: !0.531**) and ‘surface deposition’ (SD, r: !0.57**). In some cases, modalities that were positively correlated with Very Fine Sand (SdF, Bd, SD) were negatively correlated with Silt & Clay, thus contributing to the dissimilarity between assemblages; the modality ‘vermiform’ body shape was positively correlated with both types of sediment (Fig. 7). 4. Discussion 4.1. Choice of biological traits For an analysis to be complete and informative, it should consider a large number of traits rather than only the ones that are

generally regarded as important (Bremner et al., 2006; Marchini et al., 2008). In marine benthic ecology, the functional approach has often considered single traits to be indicators of community functions. In particular, ‘trophic group’ diversity has often been considered as a relevant way of describing community functioning and ecosystem-level processes, as it is related to resource availability and food web interactions (e.g. Word, 1978; Gaston et al., 1998; Brown et al., 2000; Fano et al., 2003; Gerino et al., 2003; Gamito and Furtado, 2009). Some authors have suggested that another effective way of assessing community changes is to consider the metric ‘body size’ (Basset et al., 2004; Mouillot et al., 2006; Reizopoulou and Nicolaidou, 2007). This suggestion is based on the idea that body size reflects species’ physical and lifehistory traits, thus indirectly influencing community function (Jennings et al., 2002; Olabarria and Thurston, 2003; Robson et al., 2005). However, others have questioned the effectiveness of this metric as a way of describing community functioning (Robson et al., 2005). In some studies, ‘body size’ has resulted less effective than other biological traits in describing the variability of benthic assemblages in marine and transitional waters (Parry et al., 1999; Bremner et al., 2006; Marchini et al., 2008). We therefore decided to exclude this biological trait from the set of traits used for multivariate analyses. Other functional traits are generally disregarded in benthic studies even though they are considered to be important when defining community structure. Auto-ecological information is often missing or incomplete in the literature, especially for “unpopular” traits such as ‘reproductive strategy’ and ‘life span’, and for less abundant species, as highlighted by Bremner et al. (2003) and Marchini et al. (2008). Indeed, the choice of traits included in our analysis combines ecological relevance, verified by previous BTA studies (Bremner et al., 2003; Tillin et al., 2006; Marchini et al., 2008), and information availability: only a small percentage (1.63%) of the traits we included could not be assessed due to lack of information. Our analyses showed that several traits contribute to the variability of the Emilia-Romagna benthic assemblages in different ways. This community is more governed by traits related to lifestyle and behaviour of the species (body shape, trophic group, type of movement, habit, adult mobility and bioturbation). Similar results had also been obtained by Bremner et al. (2003, 2006) off the British Atlantic coasts and by Marchini et al. (2008) in Northern Adriatic lagoons. However, traits related to life-cycle properties (reproductive strategy, patterns of development and life span) were poorly correlated with both FCA axes. This might be due to the homogeneous dominance of single modalities; for example, species with planktotrophic larva largely dominate over species with other types of development in all samples. The type of larva an organism produces reflects its adaptation to environmental variability: species with a planktotrophic larval development display greater dispersive potential and smaller extinction risk than organisms with other types of development (McHugh and Fong, 2002). Dominance of species with planktotrophic larva is therefore a response to highly variable environments such as the EmiliaRomagna coast, which is subject to intermittent recovery from periodic disturbance events (Forni and Occhipinti-Ambrogi, 2007). Life-cycle traits are related to the reproductive strategy of a species and to its habit; in an area with a high level of disturbance, such as the Emilia-Romagna coast, we expected to find a marked difference between life-cycle traits in the communities at stations closer to the Po river delta and the communities at the stations further away from this disturbance source. Instead, the differences were not very noticeable and a medium life-cycle pattern prevailed everywhere. The ecological trait ‘ecological groups-AMBI’, which synthesizes a number of biological traits, as suggested in the Grall and Glémarec


model (1997), provided a higher contribution to the variability of assemblages than life-cycle-related traits, but a lower contribution than lifestyle-related traits. Therefore, using the AMBI index to assess the benthic assemblages in the Emilia-Romagna coast might not be able to provide a thorough picture of the community under study. Previous studies have indeed highlighted that variations in AMBI in this area were not very high (Forni and OcchipintiAmbrogi, 2007; Paganelli et al., 2011). AMBI ecological groups merge a number of biological traits into a single ecological trait, whereas the BTA approach treats single traits as independent variables. Furthermore, AMBI allows us to summarize the complexity of a benthic assemblage and translate it into a numerical score of easy interpretation, while BTA decomposes the assemblages into smaller functional components and uses an analytical approach that requires careful ecological interpretation. Therefore, BTA has the potential to identify subtle differences between groups of samples and give a pertinent image of the mechanisms structuring benthic communities, although trade-offs between traits can sometimes make the data analysis and interpretation more difficult (Usseglio-Polatera et al., 2000). 4.2. Functional composition of the Emilia-Romagna benthic community The benthic assemblages along the Emilia-Romagna coast are characterized by the dominance of a few species, combined with a large pool of (more or less) rare species (Ambrogi et al., 1990; Albertelli et al., 1998; Forni, 2003; N’Siala et al., 2008). The observed assemblages at the two different depths (3 km and 10 km offshore) reflect the Pérès and Picard (1964) classification of benthic communities. Assemblages collected 3 km offshore are characterized by the molluscs Donax spp., Tellina spp., Pharus sp., Spisula spp., the crustaceans Iphinoe spp., Ampelisca spp., Diogenes spp., and the polychaetes Nephthys spp., Glycera spp., typical of the ‘Well sorted fine sand biocoenosis’. Further away from the coast (10 km from the coastline), the community is dominated by the bivalve Corbula gibba and the amphipod Ampelisca diadema which makes it characteristic of ‘Coastal Terrigenous Muds biocoenosis’ (Ambrogi et al., 1990; Daelli et al., 2000; Schiaparelli et al., 2000; Occhipinti-Ambrogi et al., 2005). The dominant functional traits reflect the functional characteristics of the dominant species, especially C. gibba and A. diadema. Corbula gibba is an indicator of sedimentary instability (Aleffi et al., 1995), organic enrichment and anoxic environments (Diaz and Rosenberg, 1995). The burrower Ampelisca diadema, through its bioturbation activities (Sanders et al., 2007), allows rapid oxygenation of the sediment and consequently an increase in the processes of nitrification (Aller, 1982; Rhoads and Boyer, 1982). The fossorial activity of this crustacean, when it is present in high abundance, can facilitate the establishment of other more sensitive species that would not be able to live in the anoxic sediment (Gallagher and Keay, 1998; Gomez-Gesteira and Dauvin, 2000). Previous studies (Dauvin, 1988; Dauvin and Bellan-Santini, 1990; Moodley et al., 1998; Occhipinti-Ambrogi et al., 2005) have shown that the inter-specific competition between C. gibba and A. diadema appears to be very strong: they are both filter-feeding/deposit feeding and they prefer a habitat with fine sediment. Our data have not confirmed the existence of a negative correlation between densities of the two dominant species; inter-specific competition is likely to be mitigated by the fact that they assume different behaviour (type of movement, habit and adult mobility) in relation to the environment. The comparison between benthic assemblages in the EmiliaRomagna coast at 3 km and at 10 km from the coastline has

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highlighted depth-related dissimilarities in the functional composition, which represent responses to the existing differences in the sediment composition. While some traits (e.g. reproductive strategy and developmental patterns) displayed the same pattern of dominant modalities at both depths, other traits (e.g. growth form, bioturbation level and ecological groups) allowed us to identify differences in the abundance patterns of single modalities. The observed functional patterns were driven by differences in species densities. This emphasizes the importance of density shifts in driving the functional attributes of habitats (Bremner et al., 2003; Hewitt et al., 2008). The assemblages collected 3 km off the coast displayed high functional heterogeneity. For example, all the four modalities of the biological trait ‘growth form’ were almost equally represented. The high variability of this area is also reflected by the presence of organisms belonging to all five AMBI ecological groups, the different relationships the organisms have with the substrate (level of bioturbation), the prevalence of a planktotrophic larval stage (mod. Pl), and the simultaneous presence of organisms with different life spans (Forni and Occhipinti-Ambrogi, 2007). At 3 km from the coastline, samples highlight an increase in the functional complexity of the community with increasing distance from the Po river mouth. This result confirms what had already been observed after the application of taxonomic-based methods and indices (Forni and Occhipinti-Ambrogi, 2007; Simonini et al., 2009; Paganelli et al., 2011). Furthermore, the assemblages collected 10 km off the coast were dominated by just a few modalities for each trait. Functional composition reflected the higher environmental stability that occurs at this distance from the coast (OcchipintiAmbrogi et al., 2005). In our case study, the FD index calculated with Rao’s coefficient proved to be capable of responding to the increasing distance from the Po river delta, which is also a gradient of substrate composition and general environmental impairment (Paganelli et al., 2011). Stations situated near the Po river delta, which are more disturbed by river inputs and, in the case of Ravenna, by the presence of a commercial and tourist harbour, showed a low functional diversity. Functional structure gradually increased towards the less impacted southernmost stations. Conversely, Shannon diversity index was not able to highlight this environmental improvement, probably due to the high dominance of a few species in many samples collected in the southernmost region. In the present study, the behaviour of Rao’s coefficient resulted independent and even contrasting with the response of taxonomic diversity. Rao’s coefficient, which is influenced by both species-abundance based diversity and trait differences among species, has already been seen to decrease as a consequence of an increasing number of species (Botta-Dukàt, 2005; Barrio Froján et al., 2011; Wan Hussin et al., 2011). Furthermore, the measure of functional diversity following the biological traits approach is a relatively new concept for marine ecology, thus more research is needed to clarify the relationship between taxonomic and functional levels of coastal benthic communities. In marine benthic communities, several feeding groups are known to coexist in different proportions, according to sediment characteristics. In sandy sediments the community is usually dominated by suspension feeders, whereas in muddy sediments it is dominated by detritus feeders. Suspension feeders are in fact disadvantaged in muddy sediments due to the clogging effect of resuspended particles and the destabilizing effect of deposit feeders on the sediment (Rhoads and Young, 1970; Levinton, 1972). The benthic community in the Emilia-Romagna coast fits this model. Bioturbation activity of species influences the penetration of oxygen into the sediment and it could extend the redox potential discontinuity as an irregular surface, deep in the sediment. By

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burrowing into the sediment, these species oxygenate the first few layers of the bottom and increase the hospitable environment for other organisms that cannot gather dissolved oxygen directly from the sediment (Levinton, 1995). The sandy bottom of stations located 3 km offshore is a typical habitat for species that cause a vertical bioturbation, which means that the activity of free-living polychaetes (surface deposit feeders and burrow excavating species) produce diffusive transport. Correlation between abundance of these traits (mentioned above) and percentage of very fine sand in the sediments was actually positive and significant. At 10 km, the muddy bottom favours species which mainly concentrate their activity on the surface of the sediment, like filter and sedentary bivalve. As shown in the correlation analysis, ‘surface deposition’ species are negatively correlated with the percentage of mud, whereas the presence of ‘diffusive mixing’ species is positively and directly influenced by the percentage of fine texture. The ‘diffuse mixing’ species may consume fine particles, transport them to the surface and thereby create a new substratum. Another important biological trait is the species’ habit, in particular the modality ‘burrow dwelling’ is positively correlated to the percentage of sand in the bottom and negatively to the percentage of small-sized particles (fine silt þ clay). Species with this type of habit strongly affect the chemistry and the composition of sediment. Some macrobenthic species have an important role in ecological processes that modify the environment. For example, movement type or fossorial activity could have a high impact on the sediment: burrower species could increment the oxygen level in the bottom or could influence the concentration of organic matter (Aller, 1982, 1983; Rhoads and Boyer, 1982). Other macrobenthos studies using the BTA approach have underlined the relationship between the functional structure of the macrobenthic community and anthropic activity, in particular trawling fisheries (Jennings and Kaiser, 1998; Bremner et al., 2003; Larsen et al., 2005; Tillin et al., 2006). Villnäs et al. (2011) and other studies (Norkko and Bonsdorff, 1996; De Juan et al., 2007; MacLeod et al., 2008; Papageorgiou et al., 2009) have highlighted that stressed benthic communities are dominated by opportunistic species which are characterized by traits such as burrowing detritivores, short life span and tube-dwelling habit. The results of these studies support the predictions that opportunistic traits are beneficial in disturbed areas (Dayton et al., 1995; Bremner et al., 2005). However, the direct effects of disturbance on variations in community functions have not yet been demonstrated. De Juan et al. (2007) in fact emphasized that it is difficult to understand whether the functional structure of the community in an impacted area is due to anthropic activities or if it represents a characteristic of muddy bottom communities. Our research on the EmiliaRomagna benthic community leads to a similar consideration: the observed dominance of opportunistic traits (e.g. deposit-feeding, bioturbation activity, short-medium life span, plancktotrophic larval stage) could be due to either natural characteristics of the area, such as substratum texture, or to anthropogenic disturbance. The long history of exploitation of Mediterranean benthic communities might have selected less vulnerable organisms that have adapted to this type of environmental stress (Dayton et al., 1995; Tuck et al., 1998; Thrush and Dayton, 2002). 5. Conclusions The Emilia-Romagna coast is characterized by instable environmental conditions and the macrobenthic communities are dominated by few species. The BTA applied to the benthic assemblages of the Emilia-Romagna coast showed that the biological traits of these communities respond to spatial gradients; this

corresponds to differences in substrate composition and influence of river inputs from the Po delta. The functional composition of assemblages near the coast (3 km offshore) responded more noticeably to the “Po effect”: functional complexity increased with increasing distance from the river delta. However, assemblages collected in deeper water (10 km offshore) displayed a more homogeneous functional composition, and were more affected by substratum structure than by Po river proximity. In this case study, the functional approach allowed us both to perform a careful analysis of community structure and functioning, and to recognize environmental gradients. The interpretation of results could be improved by comparative approaches, that at present are difficult to perform due to the low number of studies which apply this method to Mediterranean coastal areas. Furthermore, it is difficult to compare BTA studies because each of them use different combinations of traits and different combinations of modalities within a trait, on the basis of the specific aims of each research project. This difficulty probably also depends on the availability of information required to fulfill the traits matrix. In ideal conditions, complete information would be available for all traits and all species, all studies would utilize the same broad set of traits, and medium and large-scale comparisons would be feasible. Finally, an important product of this study is the functional database, which will serve as a starting point for further functional analyses of benthic communities in the Adriatic Sea.

Acknowledgements This study was partly developed within the European Commission Seventh Framework Programme (FP7) project VECTORS (Vectors of Change in Oceans and Seas Marine Life, Impact on Economic Sectors; Contract Number 266445). The oceanography centre Daphne (ARPA Emilia-Romagna) provided logistic support for all sampling surveys; we thank all its staff, in particular Dr. Cristina Mazziotti for the continuous, valuable information exchange over the years. The authors gratefully thank Charlotte Buckmaster for revising the English text.

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