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Functionaldiversityofthesoft-bottommacrobenthoscommunityat3kmofftheEmilia-Romagnacoastline

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Studi Trent. Sci. Nat., 89 (2011): 99-105© Museo delle Scienze, Trento 2011

Functional diversity of the soft-bottom macrobenthos community at 3km off theEmilia-Romagna coastline

Department of Earth and Environmental Sciences, University of Pavia, via S. Epifanio 14,27100 Pavia, Italy* E-mail dell·autoreperlacolTispondenza:danielepaganelli@unipv.it

SUMMARY - Functional diversity of the soft-bottom macrobenthos community at 3km off the Emilia-Romagna coastline - Functionaldiversity can be defined as the variety of bio-ecological characteristics each species in a community displays. A species' functional roleis described by its bio-ecological traits set, such as: growth form, trophic group, type of movement. Analyzing the functional diversity ofa community provides information on how it functions and may be used as a tool to understand its responses to the changing environ-mental conditions. The functional diversity of benthic communities in four stations along the Emilia-Romagna coast (NW-Adriatic Sea)was measured by means of the functional diversity index. The index was calculated on ten bio-ecological traits displayed by the benthiccommunity. Samples were placed along a North-South gradient of increasing distance from the Po river delta, in order to determine theeffect of freshwater and nutrient loads on the functional diversity of the communities in this region. The analyses highlighted an increaseof functional diversity with increasing distance from the Po river delta, suggesting an improvement of environmental conditions. In thesouthernmost stations, the functional structure of the community was more complex than the northern stations. A two-way ANOVA sup-ported the influence of the geographical factor on the functional diversity, while there was no evidence of temporal effects.

RIASSUNTO - Diversitafun~ionale delta comunita macrobentonica difondo mobile a 3 km dalte coste dell' Emilia Romagna - La diversi-ta funzionale puo essere definita come la varieta di ruoli funzionali presentati dalle specie di una comunita e, come la diversita di specie, Iesue variazioni possono essere utilizzate per analizzare Ie risposte delle comunita ai cambiamenti dell'ambiente. Il ruolo funzionale di unaspecie e descritto dall'insieme delle sue caratteristiche bio-ecologiche, come ad esempio la forma del corpo, il gruppo trofico di apparte-nenza, il tipo di movimento. In questo lavoro si analizza la diversita funzionale di comunita bentoniche marine dell' Adriatico attraversoilfunctional diversity index. I campioni sono stati raccolti in quattro stazioni lungo un transetto a 3 kIn dalla linea di costa dell' Emilia-Romagna allo scopo di verificare l'effetto degli apporti del flume Po sulla comunita macrobentonica. La complessita funzionale dell a co-munita, calcolata con FD index, e risultata maggiore nelle stazioni pili meridionali, dove anche altri indici suggeriscono un miglioramentodelle condizioni ambientali. L'analisi della varianza a 2 vie ha evidenziato come il fattore spaziale influenzi la diversita funzionale, mentrene il fattore temporale, ne l'interazione tra Ie due variabili risultano statisticamente significativi.

Key words: Adriatic Sea; marine benthic communities; biological traits; functional diversityParole chiave: mare Adriatico; comunita bentoniche marine; caratteristiche bio-ecologiche; diversita funzionale

The soft-bottom community is very often studiedusing methods based on its taxonomic composition to de-fine environmental conditions. Recent studies confirm thattaxonomic analysis should be integrated with informationon the functional attributes to achieve a comprehensive de-scription of communities (Petchey & Gaston, 2002; Botta-Dukar, 2005).

In fact, taxonomically related species do not alwaysrespond to environmental stress in the same way becausethey do not totally share the same bio-ecological character-istics (Chevenet et al., 1994). Equally, taxonomically dis-tinct species (sensu Clarke & Warwick, 1998) can be char-acterized by the same bio-ecological characteristics set andthis allows a comparison between different taxa (Charvet etal., 2000; Bremner et al., 2003a). Therefore, the bio-eco-

logical characteristics (bio-ecological traits) of each speciesin the community has been used as a tool to understand thearray of adaptations each species exhibits in response to thevariability of the environmental conditions (Bremner et al.,2003a). Some phylogenetically different organisms mighthave evolved similar bio-ecological traits, thus they mightpresent a high functional imilarity, combined with taxono-mic dissimilarity (Usseglio-Polatera et al., 2000; DolMec& Stamer, 1994).

Functional di\-ersity is an important property of acommunity as it an h lp us to understand how the com-munity reacts to e \-ironmental changes (Leps et al., 2006);anthropogeni - an es to the ecosystem could cau-se a pani ular fun tional response in the macrobenthos(Doled . ram i". 199'+).

Hi~ - - ·onal di\"ersity could be interpreted in twowa\" e a high exploitation of niches, or

z~<r<r

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zb-i<r -OKm 5Km 10Km 5Km 20Km 25Km

12.2°E 12.3°E 12.4°E 12.5°E

Fig. 1 - Emilia-Romagna coast. Sampling sites collected in 2004at 4 stations (Porto Garibaldi: nPG; Ravenna: nRA; Cesenatico:nCE; Cattolica: nCA) along a transect parallel to the Emilia-Ro-magna coastline, 3km offshore.Fig. 1-Costa dell'Emilia-Romagna. Campioni prelevati nel2004in quattro stazioni (Porto Garibaldi: nPG; Ravenna: nRA; Ce-senatico: nCE; Cattolica: nCA) lungo un transelto a 3km dallalinea di costa e parallelo ad essa.

if there are species \\ith multi-faceted habits, it could leadto overestimating the potential of a given environment. Inall environments, high fun tional diversity provides greaterresilience and resistance. Lo\\- functional diversity, instead,could indicate that some a\-' 'Ie environmental resourcesare not utilized by the communil.· "\lason et al., 2005); anenvironment with a lot of avail e ni~hes could be subjectto biological invasions (Dukes, _OO~ . In the same way, inan environment that is under stres. :0':; tional diver-sity might indi ate that all niches are y the fewspecies in the en\-ironment and there i 0"" 'ogi al spacefor other species (Tilman. 1996).

The relationship between environmental change andfunctional diversity within a community is still uncertainfor many ecosystems, especially marine habitats (Doledec& Stazner, 1994; Micheli & Halpern, 2005; Petchey &Gaston, 2006). The FD index was developed to describethe variation of the functional structure in a plant commu-nity (Walker et al., 1999; Petchey & Gaston, 2002; Masonet al., 2005), or to understand the complexity of food webs(Hulot et al., 2000).

Functional diversity can be defined in many dif-ferent ways. Some Authors define it as the difference be-tween the bio-ecological traits of the species a communityis composed of (Tilman, 2001; Petchey & Gaston, 2002and 2006). Some other researchers define functional diver-sity as the range and relative abundance of traits (Diaz &Cabido, 2001). In benthic studies, functional diversity hasoften been used as a synonym for trophic group diversity(Word, 1978; Fano et al., 2003; Gerino et al., 2003; Gamito& Furtado, 2009). More recently, multivariate analyses ofbiological traits have been performed on marine and transi-tional water community (Bremner et al., 2003a,b; Cooperet al., 2008; Frid et al., 2008; Marchini et al., 2008).

Shannon-Wiener diversity (Shannon &Wiener,1949) has sometimes been considered a surrogate for func-tional diversity (Diaz & Cabido, 2001). However, somespecies show multi-faceted behaviour that leads to a poorcorrelation between structural diversity and functional di-versity (Von Euler & Svensson, 2001).

Consequently, it is necessary to use a specific indexto evaluate functional diversity, such as the FD index (Lepset al., 2006). This index translates the functional role ofeach species into important functional information (Garnieret al., 2004).

This paper presents the evaluation of functionaldiversity by means of the FD index on the macrobenthoscommunity in the marine area in front of the Po river delta(Italy, NW Adriatic Sea).

The Po is the most important river to flow into theNW Adriatic Sea, influencing its haline stratification, sedi-ment texture patterns and nutrient load (de Witt & Ben-doricchio, 2001). Since the 1970s, nutrient loads broughtby this river have been regarded as one of the main causesof a general environmental impairment in the North-WestAdriatic Sea (Vollenweider et al., 1992; Justic et al., 1995).Several studies have confirmed detrimental effects on bi-otic communities (Rinaldi et al., 1995; Forni & Occhipinti-Ambrogi,2007; 'Siala et al., 2008).

The macro benthic community in this area is charac-terized by the presence of few dominant species and a lotof secondary species with low abundance (Ambrogi et al.,1990; Occhipinti-Ambrogi et al., 2002; Occhipinti-Ambro-gi et al., 2005; Forni & Castellazzi, 2007; Paganelli et al.,in press).

Samples were collected in June, July and October(12 samples in total) in 2004 at 4 stations (Porto Garibaldi:nPG; Ravenna: nRA; Cesenatico: nCE; Cattolica: nCA)along a transect parallel to the Emilia-Romagna coastline,3km offshore (Fig. 1). These stations had been chosen toverify whether the freshwater input and trophic load from

Tab. 1 - Biological traits and relative modalities.Tab. 1 - Caratteristiche bio-ecologiche e relative modalita.

Biological Traits

Growth form

Trait modalities

Dorso-ventral compressed

Laterally compressed

Globose

Vermiform

Filter feeder

Carnivore-Omnivore

Deposit feeder

Sub-surface Deposit feeder

Swimmer

Burrower

Crawler

Walker

Tube dwelling

Bun'ow dwelling

Free living

Mobile

Moderately mobile

Sessile

Diffusive mixing

Surface deposition

Conveyer belt transport

No bioturbation

Reproductive technique Asex

Sex: gonocoric

Sex: hermaphrodite

Planktotrophic

Leci totrophic

Direct development

Brooding

Short

Medium

Ecological group(AMEl)

Long

SensitiveIndifferentTolerantSecond order opportunisticFirst order opportunistic

the Po river had an influence on the benthic community.Therefore, distance from the Po river delta was determinedby the time in which the sampling survey took place. Forexample, in winter, the Po waters penetrate the coastal areasouth of the delta, causing relevant salinity decreases. Inthis case, distances were calculated from the "Po di Goro"area; whereas, in summer, when the direction and inten-sity of Adriatic cunents are influenced by winds (mainlydirected south-westward) distances are calculated from the"Po di Maestra" area (Montanari et al., 2006).

For each sample, four replicates were collected us-ing a 0.06 m2 Van Veen grab. The fifth replicate was frozenfor granulometric analysis of the sediment. In the labora-tory, sediments were separated into four classes accordingto particle size: Sand (> 150 m}!), Very Fine Sand (150-163m}!), Coarse Silt (62.9-15.6 m}!) and Fine Silt/Clay « 15.5m}!), according to Buchanan's method (1984).

The biological material was sieved through 1 mmmesh and all the organisms were identified to species leveland then counted.

As proposed by several Authors, we used 9 bio-ecological traits (Bremner et al., 2006; Petchey & Gaston,2006; Frid et al., 2008) to determine functional characteris-tics of the soft-bottom macrobenthos community along theEmilia-Romagna coastline: growth form, trophic group,type of movement, habit, adult mobility, method of biotur-bation, reproductive technique, development mechanismand life span (Table 1). Data was collected from relevantliterature including journal papers and websites of scientificinstitutions (www .marinespecies .org, www.marlin.ac.uk).

To provide an additional ecological characteristic,each species was also classified in accordance with thefive ecological groups from the AZTI list, used to calculateAMBI index (Borja et al., 2000), a widely used biotic indexfor the assessment of ecological status of marine coastalwaters using benthic macro invertebrates. The AZTI listpresents a classification of the macro benthic species in 5ecological groups in accordance with Hily (1984) and Gle-marec (1986): group I,Sensitive species; group II, Indiffer-ent species; group III, Tolerant species; group IV, Secondorder opportunistic species and group V, First order oppor-tunistic species. AMBI is calculated as a linear combina-tion of the relative abundances of the five ecological groupslisted above. AMBI decreases with increasing ecologicalstatus, ranging from 0 (no environmental stress) to 6 (to-tally altered environment).

The 10 bio-ecological traits were subdivided into 37modalities, as reported in table 1, in order to evaluate theaffinity of each species to more than one modality. All ofthese traits can provide information about the functioningof the entire ecosystem (Diaz & Cabido, 2001).

For some species and some traits, it is difficult to as-sess single modalities; many species display multi-facetedbehavior, depending on the specific conditions and resourc-es. Therefore, a fuzzy-coding approach was adopted as itrepresents a suitable solution for this problem. Fuzzy cod-ing allows each species to be classified depending on itsdegree of affinity for each modality (Chevenet et al., 1994).A score between 0 and 3 \\'a given to all modalities, where3 corresponded to the maximum affinity for that modal-ity, 1 or 2 to partial affinity and 0 to no affinity. Wheneverinformation wa not ayailable. a score of 0 was given to allmodalities, so as not to influence the analyses (Chevenetet al., 1994). To determine the frequency of each modal-ity in the macrobenthi ornmuniry. the "affinity score" foreach modality 0 ea h pe ie was multiplied by the rela-tive abundanc of tb pe ie in each station (Charvet et al.,2000: Bremner er aJ .. _006).

The re-ulting da t \\-as used for the calculation of

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Fig. 2 - CorrelationbetweenPo river distance and FD index values.Fig. 2 - Correla:ione tra la distanza dal delta del Po e i valoridell'indice FD.

FD, which is created for fuzzy-coded data (Ricotta, 2005;Leps, 2006, Petchey & Gaston, 2006). The FD index wasdeveloped on the same principles as the Simpson diversityindex but it uses fuzzy-coded data (Ricotta, 2005; Leps,2006; Petchey & Gaston, 2006).

It calculates the weighted average of individualtraits for the entire community, which translates into im-portant functional information on the composition of thecommunity (Garnier et ai., 2004).

The results obtained by applying the FD index to the12 samples were then analyzed by means of 2-way ANO-VA, considering the spatial and temporal factors, in orderto detect differences in the functional composition of thebenthic communities.

To calculate the FD index, a free software called"FunctDiv.xls" developed by Leps et ai. (2006) was used.The macro and its instructions are available on the websiteof the Department of Botany of the University of SouthBohemia (http://botanika.bf.jcu .cz/suspalFunctDiv .php).

The results of the FD index were then correlated tothe distance of each sample from the Po river delta and toother indices of community structure: number of species,Shannon-Wiener's diversity index (Shannon & Wiener,1949), Simpson's dominance index (Simpson, 1949). Fur-thermore, we investigated the relationship between FD in-dex and AMBI index (Borja et ai., 2000). The comparisonbetween the FD index and the other four indicators (S; H',c, AMBI) was performed by means of a non-parametricSpearman correlation and all statistical analyses were car-ried out by means of the MINITAB 12.0 software package.

The grain size of samples was affected by distancefrom the Po river: the average granulometry composition instations nRA, nCE and nCA was: 2.4% sand, 82.6% veryfine sand, 12.6% coarse silt, and 2.4% fine silt/clay.

The closest station to the Po river delta, nPG, dis-played a higher percentage of the smaller-sized fractions(coarse and fine silt and clay) than the other three stations.The sediment in this station was composed of 1.8% sand,

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Fig. 3 - COlTelationbetween Shannon diversity index (H') and FDindex values.Fig. 3 - Correlazione tra i valori dell'indice di diversita di Shan-non (H') e i valori dell'indice FD.

33.7% very fine sand, 24.7% coarse silt, and 39.8% finesilt/clay.

The "species x traits" matrix involved assessing1280 traits (128 species x 10 traits), of which 26 cases wereimpossible to assign because of lack of information. Themissing information is especially related to the traits repro-ductive technique (not assessed for 6 species) and life span(not assessed for 10 species).

The community at 3km off shore is mainly com-posed by species with dorso-ventral compressed or ver-miform body shape, moderately mobile burrowers or tubedwellers. The main trophic group is deposit feeder. Mostspecies have a ShOlt life span, planktotrophic larval stageand sexual reproduction.

According to the classification proposed by theAZTI list, the community is mainly composed by Sensi-tive (group I), Indifferent (group II) and Tolerant species(group III).

Three out of the ten bio-ecological traits that wereconsidered (growth form, habit, level of bioturbation) high-lighted relevant differences in the functional structure ofthe communities at the four stations.

Considering growth form, the macrobenthic com-munities at the stations near the Po river delta (nPG andnRA) are characterized by species with dorso-ventral com-pressed body shape, whereas in the other two stations (nCEand nCA) all the modalities of this trait are equally distrib-uted.

The species that live at Porto Garibaldi and Ravennaare mainly tube dwellers, while in Cesenatico and Cattol-ica they are mainly burrow dwellers. These modalities arelinked to the level of bioturbation: near the Po river deltathe community is mainly dominated by surface depositionspecies, instead in the southern stations the frequencies ofeach modality are equally distributed.

To synthesize the bio-ecological trait informationthe FD index was used. The index ranged from 0.23, ob-tained in October at Ravenna, and 0.54, obtained in Mayat Cattolica.

The mean values (± standard deviation) of the FDindex at each station show an improvement from North (FDindex: 0.33 ± 0.01) to South (FD index: 0.44 ± 0.01).

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Fig. 4 - Conelation between Simpson dominance index (c) andFD index values.Fig. 4 - Correlazione tra i valori dell'indice di dominanza (c) e i,"alori dell'indice FD.

The most important structural indices of the commu-nity (number of species, S; Shannon diversity, H'; Simpsondominance index, c) were calculated for each sample. Thehighest number of species was found in nCAS (Cattolica,May, S=66) and the lowest in nRA5 (Ravenna, May, S=26).

The highest value recorded by the Shannon indexwas in Cattolica (nCAS, H'=2.83) and the lowest was inPorto Garibaldi (nPG7, H'=1.87). The highest value of theSimpson's dominance index OCCUlTedin Porto Garibaldi(nPG7, c= 0.34), and the lowest value in Cesenatico (nCE7,c=O.lO).

Each structural index showed an improvement ofcommunity structure from North to South.

When the AMBI index was applied, the best sam-ple was nCES (AMBI=1.42) and the worst was nRAIO(AMBI=3.31).

All indices showed an overall improvement of thebenthic communities from North to South. Stations nCE(Cesenatico, mean AMBI=I.6S) and nCA (Cattolica, meanAMBI=1.61) are characterized by lower values of theAMBI index, compared to stations closer to the Po riverdelta (nPG mean AMBI= 2.56; nRA mean AMBI= 2.94).

The FD index was positively correlated with the dis-tance from the Po (R=0.S6, p: 0.06) (Fig. 2) and Shannondiversity (R=0.76, p: 0.005) (Fig. 3), whereas it was nega-tively correlated with the dominance index (R=-O.78, p:0.003) (Fig. 4) and AMBI (R=-0.76, p: 0.003) (Fig. 5). Onthe other hand, the correlation with the number of species(S) was weak and not significant (R=0.36, p> 0.05) (Fig. 6).

A 2-WAY ANOVA was carried out to test the signifi-cance of spatial and temporal effects on the FD index. Theresults showed a statistical significance of the differencebetween stations (DF=I; F=9.81; p<O.OS) and time (DF=2;F=3.11; p>O.OS). Conversely, the interaction between thetwo factors was not significant (DF=2; F=O.77; p>O.OS).

Several Authors have proved that bio-ecologicaltraits are useful tools to analyse ecological integrity, espe-cially for aquatic ecosystems (Charvet et al., 2000; DolMec

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Fig. 5 - Correlation between AMBI and FD index values.Fig. 5 - Correlazione fra i valori dell'indice AMBI e i valoridell'indice FD.

et al., 1999; Statzner et al., 2004; Usseglio-Polatera et al.,2000; Bremner et al., 2003b; Bremner et al., 2006; Cooperet al., 2008; Frid et al., 2008; Marchini et al., 2008).

The functional analysis should involve as manytraits as possible, in order to provide a thorough pictureof the community under study. The information about thetraits of single species should derive from relevant litera-ture. For the marine benthos, however, it has already beenobserved that there is much less information available(Bremner et al., 2003b; Tillin ef al., 2006; Marchini et al.,2008) compared to freshwater macrobenthos (Charvet etal., 2000; Stazner et al., 1994). Therefore, the fulfilment ofthe traits matrix for marine benthos might be a difficult andtime-consuming task, especially when highly diverse com-munities are considered and many traits are involved in theanalysis. The choice of how many traits to include in theanalysis should therefore be a balance between complete-ness and feasibility. In our study, we included 9 biologi-cal traits and 1 ecological trait (ecological groups from theAZTI list) whose relevance had been proved by other stud-ies on functional structure of the marine benthos (Bremneret al., 2003a, b; Tillin et al., 2006; Marchin.i et al., 2008),and whose information was more easily accessible from theliterature sources: in fact, only a small percentage (2.03%)of the involved traits could not be assessed due to lack ofinformation.

In the case of our study, the FD index proved to becapable of differentiating stations according to a spatialgradient, which is also a gradient of substrate compositionand general environmental disturbance. Station nPG, whichis right in front of the Po river delta, and station nRA,which is affected by both its closeness to the Po delta andthe presence of a commercial and tourist harbour, showeda significantly lower functional diversity than the southern-most stations nCE and nCA.

For example, station nPG, where the fine silt/clayfraction was prevailing, displayed a dominance of spe-cies with dorso-ventral compressed body shape, whichare mainly tube dwellers and surface depositors; whereasat stations nCE and nCA, all the modalities of the trait"growth form" \vere equally distributed.

Comparing the FD index with most indicators of

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Fig. 6 - Correlation between number of species (S) and FD indexvalues.Fig. 6 - Correlazione tra il numero di specie (S) e i valori dell'in-dice FD.

taxonomic structure revealed a significant correlation,however the correlation with the number of species wasweak and not significant.

A community composed by few species could actu-ally have a high FD value because particular species mayhave multiple different strategies to adapt to changing en-vironmental conditions; similarly, the presence of manyspecies does not guarantee high functional diversity (Botta-Dukat, 2005). This appears to be the case for the macrob-enthos in the Emilia-Romagna coast: the total number ofspecies observed in our stations was fairly high (5=128),but most of them displayed similar functional traits.

Functional structure, which was evaluated by meansof the FD index, succeeded in identifying a Northward dis-turbance gradient for the Emilia-Romagna benthic commu-nity and reflected the ecological quality status which wasassessed using biotic indices (Forni & Occhipinti-Ambro-gi, 2007); on the other hand, taxonomic approaches such asevaluating average taxonomic distinctness and variation intaxonomic distinctness failed (Forni & Castellazzi, 2007).

Therefore, functional diversity should be not con-sidered an alternative, but an addition to taxonomic rich-ness and diversity when analysing a community. It behavesindependently from indicators that are based on the sim-ple presence and relative abundance of species that do notconsider their functional role in the ecosystem (Peru &Doledec,2010).

The negative correlation of the FD index with AMBIshould be interpreted as a positive correlation of functionaldiversity with ecological quality status (sensu the WaterFramework Directive, EUI2000/60); it is acknowledgedthat poor ecological status is associated with poor func-tional structure, whereas improved quality status allows thedevelopment of a more complex community, with a highernumber of exploited ecological niches.

The Authors thank Cristina Mazziotti (Oceanogra-phy centre Daphne, ARPA Emilia-Romagna) for the im-

portant information about the Emilia-Romagna coast --Charlotte Buckmaster for the revision of the English tex:-

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