Patterns of colonization and succession of benthic assemblages in two artificial substrates

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  • Journal of Sea Research 88 (2014) 7886

    Contents lists available at ScienceDirect

    Journal of Sea Research

    j ourna l homepage: www.e lsev ie r .com/ locate /seares

    Patterns of colonization and succession of benthic assemblages in twoartificial substrates

    A. Spagnolo , C. Cuicchi, E. Punzo, A. Santelli, G. Scarcella, G. FabiNational Research Council-Institute of Marine Sciences (CNR-ISMAR), Largo Fiera della Pesca, 2-60125 Ancona, Italy

    Corresponding author. Tel.: +39 071 207881.E-mail address: a.spagnolo@ismar.cnr.it (A. Spagnolo)

    1385-1101/$ see front matter 2014 Elsevier B.V. All rihttp://dx.doi.org/10.1016/j.seares.2014.01.007

    a b s t r a c t

    a r t i c l e i n f o

    Article history:Received 8 August 2013Received in revised form 13 January 2014Accepted 16 January 2014Available online 24 January 2014

    Keywords:Artificial reefsArtificial substratesBenthic communitiesCommunity composition

    Benthic communities colonizing two different typologies of artificial structures, Tecnoreef pyramids (PY), andplinthmodules (PL), differing formaterial and shape,were investigated for three years after their deployment ona soft bottom offshore Pedaso (Western Adriatic Sea). The aims were to describe the colonization patterns ofbenthic assemblages on the two artificial modules, to highlight possible differences between them and to detectthe effectiveness of the artificial reef on the ecosystem functioning.The composition of the benthic communities settled on the two types of artificial substrates was different espe-cially just after the reef deployment. Abundance and species richness were higher on PL in the first two years,while an explosion of individuals characterized PY in the third year. This suggested a delay of about one yearin the colonization processes on PY likely due to the material and shape. The community settled of the artificialstructures was dominated by hard-substrate species which are commonly absent in the natural environment.The occurrence of these organisms enriched the local soft-bottom communities and contributed to habitat diver-sification. This, togetherwith the importance of these species in the diet of a few reef-dwelling fish, confirms thetrophic role and the ecological importance of artificial reefs in areas characterized by soft seabed.

    2014 Elsevier B.V. All rights reserved.

    1. Introduction

    An artificial reef is a submerged structure placed on the seabed de-liberately, to mimic some characteristics of a natural reef (UNEP-MAP,2005). In Europe this modern concept of artificial reefs was adopted inthe second half of the 1900s and, since then, artificial structures havebeen deployed in many countries (Fabi et al., 2011).

    Concrete is themost commonmaterial in Europe for construction ofartificial reefs (Fabi et al., 2011) because it ensures good stability andallows the realization of modules of various shapes and sizes. In 1980sresearch was carried out in Europe to test new materials and differentmodule shapes to reduce costs and obtain good ecological responseand structural stability. One of these materials is the cement-stabilizedcoal-ash coming from coal-fired power stations (Bombace et al.,1997; Jensen et al., 1994; Peter et al., 1982; Relini, 2000; Relini andPatrignani, 1992).

    The choice of material should consider the compatibility with themarine environment, the resistance to the chemical and physical forcesin constant action in themarinewaters, the time-life, and the suitabilityfor colonization by benthic communities, to induce the lowest environ-mental impact and to improve the natural environment. The ecological

    .

    ghts reserved.

    importance of fouling assemblages in artificial community developmentwas seldom the main focus of the studies carried out up to 1980s. Designof artificial reefs, as a matter of fact, has been typically driven by fisheriesecology whilst ignoring the role of epiflora and epifauna which wereinvestigated separately (Baine, 2001). Starting from '90s the potentialrole of macrobenthic communities in providing food for commercialfish faunawas recognized and studies concerningmacrobenthic coloniza-tion assumed increasing importance (Ardizzone et al., 1997; Badalamentiet al., 1993; Clynick et al., 2007; Collins and Jensen, 1996; Fabi et al., 2006;Farias-Franco et al., 2013; Johnson et al., 1994; Lindquist et al., 1994;Redman and Szedlmayer, 2009; Relini et al., 2002).

    Besides environmental factors (e.g., temperature, salinity, light,depth), substratum and relative position to the seafloor also play an im-portant role in the settlement, recruitment and growth of benthic or-ganisms (Glasby, 1999; Kocak and Zamboni, 1998). The material usedin construction of artificial reefs can strongly affect fouling assemblagedevelopment. For instance, Woodhead and Jacobson (1985) reportedsome differences in species preferences and colonization rates betweenartificial reefsmade from concrete and from coal combustionwastes, al-though the overall fouling assemblages were similar. Anderson andUndewood (1994), studying the effects of four different substrates,highlighted greater abundance of benthic species on concrete andplywood than on fiberglass or aluminum. In the northern Adriatic Sea,Bombace et al. (1997) found higher species richness on concrete

    http://crossmark.crossref.org/dialog/?doi=10.1016/j.seares.2014.01.007&domain=pdfhttp://dx.doi.org/10.1016/j.seares.2014.01.007mailto:a.spagnolo@ismar.cnr.ithttp://dx.doi.org/10.1016/j.seares.2014.01.007http://www.sciencedirect.com/science/journal/13851101

  • 79A. Spagnolo et al. / Journal of Sea Research 88 (2014) 7886

    modules in respect to coal-ash ones and a selective settlement of theburrowing bivalve Pholas dactylus on the horizontal surfaces of coal-ash blocks.

    Studies have also shown that rough surface texture enhancesbenthic settlement providing shelter and supporting greater diversity(Beserra Azevedo et al., 2006; Harlin and Lindbergh, 1977; Hixon andBrostoff, 1985). Other factors affecting the colonization processes of anartificial reef and the diversification of communities are shape, dimen-sion and extension along the water column as well as orientation ofsurfaces. Ardizzone and Chimenz (1982) found that a difference of2-m distance from the sea bottom was sufficient to modify the benthiccommunity at Fregene artificial reef (Tyrrhenian Sea). Very differenttypes of epibiotic assemblages have been shown to occur on surfacesof different orientation, upper vs lower surfaces, vertical vs horizontalones (Bombace et al., 1997; Connell, 1999; Hurlbut, 1991; Spagnoloet al., 2004; Todd and Turner, 1986; Wendt et al., 1989).

    In the case of eutrophic waters, the orientation of surfaces is strictlylinked to light and sedimentation rates. Indeed, in areas of strong sedi-mentation such as in front of a river mouth, the horizontal surfaces canbe covered by a very fine mud; conversely, hydrodynamism produces acontinuous turn-over on the vertical walls reducing accumulation ofsuspended material. As a consequence, the horizontal surfaces will besettled by both hard-substrate species and soft-bottom organismswhilstthe vertical walls will bemainly colonized by hard-bottom, filter-feederssuch as bivalves (e.g. Mytilus galloprovincialis, Ostrea edulis, Crassostreagigas), hydroids, and barnacles (Spagnolo et al., 2004).

    Therefore, it is likely that the combined effects ofmaterial and orien-tation may greatly influence the development of epibiotic assemblages.

    The present study reports on the differences in benthic settlementand species composition between two types of artificial modules

    Fig. 1. Location along the Adriatic coast of the Pedaso artificial reef and its pa

    (Tecnoreef pyramids and plinth-pole concrete modules) used for theconstruction of an artificial reef in the central Adriatic Sea. The twomodules differ for material and shape. Tecnoreef pyramids representa new module widely used in the construction of artificial reefs(Italy, Oman, Dubai, and Abu Dhabi). Fish repopulation and habitatdiversification are two potential functions of these structures but,at present, their scientific references are very scarce. Instead, anti-trawling is the main role of plinth-pole modules. The aims of thispaperwere to describe the colonization patterns of benthic assemblageson the two artificial modules, to highlight and analyze possible differ-ences between them and to detect the effectiveness of the artificialreef on the ecosystem functioning.

    2. Material and methods

    2.1. Study area

    Work was done at the Pedaso artificial reef (Western Adriatic Sea;Fig. 1), deployed in September 2005 and covering an area of 81 ha(225 m 3200 m). It is located at a distance of 3 nm from the coastand at 14.515.0 m depth, on a muddy bottom without natural rockyoutcrops or seagrasses. Benthic community inhabiting the natural softbottom is mainly represented by organisms belonging to the Biocoeno-sis of coastal terrigenousmud and offinewell-sorted sand (unpublisheddata). The sandy coast is protected by several breakwaters. The area isaffected by the inflow of five rivers (Chienti, Tenna, Aso, Tesino, andTronto); it is characterized by a horizontal thermohaline stratificationin summer, with a water temperature of 24.527.3 C at the surfaceand of 18.222.9 C close to the bottom (Campanelli et al., 2011).Salinity ranges from 35.0 to 36.0 psu near the surface and from 35.0 to

    rtial scheme. A particular of the two types of substrates is also reported.

  • 80 A. Spagnolo et al. / Journal of Sea Research 88 (2014) 7886

    38.0 psu close to the seabed (Campanelli et al., 2011). Themain bottomcurrent is towards South and sporadically reaches a speed of 30 cm s1

    (unpublished current meter data).Pedaso artificial reef was planned to respond to different require-

    ments. One of the main aims was to contrast the illegal trawlingwhich is often carried out in the coastal area inside the 3 nm offshore,where this type of fishery is forbidden (EC Reg. 1967/2006). Hence,214 plinth-pole structures, sufficiently heavy to stop the trawling nets,were placed along the artificial reef perimeter at a distance from eachother less than the free space needed by the fishing vessels to passwith the towed gear between one module and the other (Fig. 1).These structures consist of a plinth (2.1 2.1 1.3 m; hereafterindicated as PL) and a pole 4 m high, both made of common concrete(pH 12). The two elements have together a total height of 4.2 m and aweight of 8900 kg.

    The other structures constituting the Pedaso artificial reef wereTechnoreef pyramids (hereafter indicated as PY), deployed for finfishenhancement. Seventy-six PY were placed inside the reef to increaseshelter opportunities and to enhance the settlement of benthic organ-isms representing a source of food for finfish species, with subsequentdevelopment of a resident fish assemblage and increase, consequently,of biomass. PY are made of sea-friendly certified reinforced concrete,manufactured using only natural components without syntheticadditives (pH 9). The basic Tecnoreef module consists of an octagonalslab with circular holes within the structure itself. The slabs areconnected together to form a complex pyramidal structure, having aweight of 2700 kg, height of 2.4 m and occupying an area of 14 m2 onthe bottom.

    2.2. Sampling strategy

    The macrozoobenthic community was investigated for three yearsstarting upon reef deployment. Three surveys per year were carriedout in summer, after the main recruitment period of the benthic organ-isms occurring in late spring. In each survey three PY and three PL wererandomly chosen. Poles were excluded to minimize the environmentalvariability linked to a vertical gradient in terms of light, currents,temperature, and larvae availability. It is known, in fact, that in the cen-tral and northern Adriatic Sea the highest settlement density of mussels(M. galloprovincialis) takes place between 1 and 5 m below the seasurface (Fabi et al., 1985, 1989). PY and PL are characterized by differentshapes and materials but have similar height and therefore can becomparable.

    At each structure a standard area (40x40 cm) was randomly sam-pled on the vertical walls by means of the scraping technique, whichis commonly used to monitor benthic communities settled on artificialreefs (Relini and Relini, 1997): organisms were gently removed bydivers minimizing the samples lost and placed in net bags (mesh size:0.5 mm). Each sample represented a single replicate. The collectedmaterial was sieved on board through a 0.5mmmesh and all organismsretained were preserved in 5% buffered formalin. In the laboratory,macrofauna was sorted through a stereomicroscope and a binocularmicroscope, identified to species level when possible using standardnomenclature, quantified, and weighted. The affinity towards hard orsoft substrates of the taxa identified at species level was evaluatedusing available literature (Amouroux, 1974; Augier, 1992; BellanSantini and Ledoyer, 1972; Bellan et al., 1980; Bianchi et al., 1993;Bourcier et al., 1979; Chimenz Gusso et al., 2001; Nodot et al., 1984;Pres and Picard, 1964; Poppe and Goto, 1991, 1993; Rinelli andSpan, 1997; Ruffo, 1998; Salen-Picard, 1985).

    2.3. Data analysis

    2.3.1. Univariate analysesUnivariate measures such as species abundance (N; number of indi-

    viduals d m2), species richness, Shannon diversity (H; Pielou, 1974)

    and Simpson index (; Simpson, 1949) were calculated on benthicabundance data for each replicate. Prior to analysis, the species abun-dance data were log transformed as log (x + 1) to respect the assump-tion regarding the homogeneity of variancewithin each group. Changesin these biological indices were examined using a 3-way mixed factorsanalysis considering type of substrate (two levels and fixed factor),years (three levels and fixed factor) and surveys (three levels andrandom factor nested in year and orthogonal to substrate). as the inter-actions of the random factor were not significant the terms substrateand years were treated as orthogonal. In the case of significant interac-tions a pair-wise test was conducted comparing the two modulesin each year.

    Because the assumption of normality needed for ANOVA was notrespected for the four univariate measures, the analysis was conductedusing a permutation analysis of variance (PERMANOVA) based onEuclidean distances. Although PERMANOVA is designed formultivariateanalysis on dissimilarity matrices, it can be used to perform univariateanalyses if applied on a Euclidean distance matrix. In such case thesums of squares and F-ratios are exactly the same as Fisher's univariateF-statistic of traditional ANOVA. PERMANOVA calculates p-values usingpermutations, rather than relying on tabled p-values, which assumenormality. Therefore, in the case this assumption is not met, this ap-proach can be used to compare univariate measures (Anderson, 2005).

    2.3.2. Multivariate analysesMultivariate analyses were performed to identify how the benthic

    assemblage changed with time and type of module. Prior to any analy-sis, the species abundance data were log-transformed, considering thatthere were two orders of magnitude difference between abundant anduncommon taxa. BrayCurtis similarity matrix was calculated. The dif-ferences betweenmacrofauna assemblages at the two types of modulesduring the three sampling years were tested bymeans of a permutationanalysis of variance. This method allowed testing the general multivar-iate hypothesis of differences in the composition and/or relativeabundances of organisms of different species in samples from differ-ent groups (Anderson, 2001; McArdle and Anderson, 2001). In thePERMANOVA the same statistical design of the univariate ANOVA wasemployed. Since the test results showed a significant interactionbetween type of modules and year, a pair-wise test was conductedcomparing the two modules in each year. The unconstrained PrincipalCoordinates (PCO) plot on averaged data was used to confirmPERMANOVA results and a projection plot was drawn onto PCO axes toexamine their relationship with the abundances of species (Andersonet al., 2008). Successively, similarity percentage breakdown procedure(SIMPER; Clarke andWarwick, 2001) was used to determine the contri-bution of individual taxa towards the dissimilarity between the twotypes of modules and year groups.

    Both univariate and multivariate analyses were conducted withPRIMER ecological software package (Clarke, 1993; Clarke andWarwick, 2001). Levels of significance were set at p 0.01 (highlysignificant), and 0.01 b p 0.05 (significant) in both analyses.

    3. Results

    3.1. Univariate results

    A total of 65 taxa were collected during the overall period. Theyincluded 2 cnidarians, 1 platyhelminth, 18 molluscs, 24 polychaetes, 1sipunculid, 16 crustaceans, 1 bryozoan, 1 echinoderm, and 1 ascidian.Twenty-nine taxa were typical of hard bottoms and 24 of soft bottoms(Table 1). No algae were found.

    PY and PL were characterized by the same number of taxa (54). OnPY they were mainly polychaetes (19), molluscs (16) and crustaceans(15); the other taxa belonged to cnidarians (2), platyhelminthes(1) and ascidians (1). Hard-bottom species were more numerous thansoft-bottoms ones either in the overall (24 and 20 respectively) and in

  • Table 1List and mean density (n. ind. dm2) of taxa collected in each year on Pyramids and on Plinth modules. The total number of taxa is also reported. HS = hard substrate; SS = soft substrate; WER = wide ecological repartition.

    Phylum/class Substrate Taxa Pyramids Plinths Phylum/class Substrate Taxa Pyramids Plinths

    2006 2007 2008 2006 2007 2008 2006 2007 2008 2006 2007 2008

    Cnidarians Actiniaria nd 0.02 0.49 5.27 2.71 3.75 1.71 Polychaetes Nereis sp. 0.02Hydrozoa 0.01 0.02 0.01 SS Phyllodoce mucosa 0.03 0.02 0.03

    Platyhelminthes Platyhelminth nd 0.02 0.19 0.06 0.15 0.07 0.08 Phyllodoce sp. 0.01Molluscs SS Abra alba 0.01 HS Polydora ciliata 0.09 2.29 5.54 1.54 1.16 2.95

    SS Anadara demiri 0.32 0.04 0.20 0.10 0.01 0.07 HS Pomatoceros triqueter 0.03 4.59 2.61 12.15 6.14 1.63HS Anomia ephippium 0.09 3.17 0.08 0.09 0.11 SS Sabella pavonina 0.01 0.01 0.01 0.02SS Antalis inaequicostatum 0.01 HS Sabellaria spinulosa 0.05 2.13 0.51 3.04 3.10 2.05

    Chlamys sp. 0.01 Sabellidae nd 0.2SS Flexopecten glaber 0.04 SS Scoletoma impatiens 0.01 0.01SS Gastrochaena dubia 0.03 0.06 0.02 HS Serpula vermicularis 0.09 0.04 0.03 0.32 0.24SS Hexaplex trunculus 0.05 0.04 0.04 HS Syllis gracilis 0.38 0.67HS Hiatella arctica 0.02 0.17 0.08 0.48 0.57 0.20 Syllis sp. 0.01 0.38 0.01 1.01SS Kurtiella bidentata 0.01 0.01 0.01 Sipunculids Sipuncula nd 0.01HS Mimachlamis varia 0.02 0.02 0.08 0.06 Crustaceans SS Alpheus dentipes 0.01 0.06 0.04 0.13 0.13 0.03HS Modiolarca subpicta 0.03 0.30 0.02 0.10 SS Alpheus glaber 0.05HS Mytilus galloprovincialis 0.04 0.28 1.01 0.19 0.44 0.13 HS Amphibalanus improvisus 0.02 0.04 0.03SS Nassarius incrassatus 0.01 HS Athanas nitescens 0.01 0.02 0.05 0.15 0.07 0.02SS Nassarius nitidus 0.01 0.01 HS Balanus trigonus 0.02 0.10 0.05SS Nucula nitidosa 0.01 HS Elasmopus rapax 0.01 2.81 3.49 0.01 0.15 0.17HS Ostrea edulis 0.01 0.01 0.08 0.01 0.04 0.04 HS Erichtonius punctatus 0.42 5.09 2.07 0.21 0.61SS Paphia aurea 0.02 WER Macropodia rostrata 0.01

    Polychaetes HS Ceratonereis costae 0.07 0.04 0.04 0.07 0.02 HS Monocorophium acherusicum 1.62 16.84 55.81 24.15 31.13 21.95HS Eunice vittata 0.01 HS Perforatus perforatus 0.01 0.10 0.04 0.04 0.04SS Harmothoe areolata 0.01 HS Pilumnus hirtellus 0.01 0.08 0.54 0.29HS Hydroides elegans 0.01 HS Pilumnus spinifer 0.02 0.03HS Hydroides norvegica 0.01 HS Pisidia longicornis 0.13 0.13 0.55 0.26 0.09HS Hydroides pseudouncinata 0.10 0.03 0.26 0.11 Stenothoe sp. 0.01SS Lumbrineris gracilis 0.01 0.02 0.01 0.02 0.03 HS Stenothoe valida 0.70HS Lysidice ninetta 0.09 0.04 0.01 0.25 0.10 HS Thoralus cranchii 0.09 0.04 0.19 0.23 0.02SS Malmgreniella lunulata 0.01 0.03 Bryozoans HS Scizoporella errata 0.01SS Minuspio cirrifera 0.10 0.04 0.02 0.12 0.03 Echinoderms SS Amphiura chiajei 0.01SS Marphysa sanguinea 0.23 0.05 0.04 0.18 0.03 Ascidians SS Phallusia mammillata 0.01 0.34 0.08 0.77 0.01

    Nereidae juv 0.04 Total density 2.27 32.21 85.00 48.84 50.93 33.69Total richness 21 40 35 37 56 34

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    7886

  • Fig. 2. Total species richness and mean abundance (N. ind. dm2 SD) of hard- and soft-bottom species sampled on the two substrates. PL = plinth module; PY = pyramid module.

    82 A. Spagnolo et al. / Journal of Sea Research 88 (2014) 7886

    each year (Fig. 2). They doubled in the second year (2006: 10; 2007:23), slightly decreasing in 2008 (21). Only 6 soft-bottom specieswere collected in 2006; they reached a peak in 2007 (16) and reducedin 2008 (11). Also the abundance of hard bottom species was alwayshigher than the soft-bottom ones, showing an increase over time(Fig. 2).

    Polychaetes also dominated on PL (21 taxa), followed by crustaceans(13) and molluscs (13). In addition, 2 cnidarians, 1 platyhelminth, 1sipunculid, 1 bryozoan, 1 echinoderm, and 1 ascidian were collected.On these modules 21 taxa were typical of soft-bottoms and 21 of hardsubstrates. The number of hard-bottom taxa did not change in the firsttwo years (2006 and 2007: 22) and slightly decreased in 2008 (20);soft-bottom species, instead, showed a peak in 2007 (18; Fig. 2). Theabundance of species with affinity towards hard substrates was alwayshigher than the soft-bottom taxa but, unlike PY, it showed a decrease in2008 (Fig. 2).

    The statistical analysis highlighted significant interactions betweenSubstrate and Year for all indices (Table 2). The mean species richness(Sm) was significantly higher on PL in the first two years of study,while during the last year the two substrates showed similar values(Table 2; Fig. 3a). Significant differences over time were obtained forN, due to higher values on PL in the first two years and on PY in thethird year (Table 2; Fig. 3b). On PY this index increased over time dueto some taxa such as Actiniaria nd, Elasmopus rapax, Erichtoniuspunctatus, Polydora ciliata, Anomia ephippium, M. galloprovincialis and,above all, Monocorophium acherusicum, which became gradually moreabundant (Table 1). Similar values among the years were obtained onPL. On this substrate the most abundant species were M. acherusicum,Actiniaria nd, P. ciliata, Sabellaria spinulosa, and Pomatoceros triqueter,the last one showing a decrease from 2006 to 2008 (Table 1). Also Hshowed different patterns between the two substrates, with a highlysignificant difference during the first year due to higher values on PL.On the contrary, PY showed a significantly higher value in 2007. No

    Table 2Summary of 3-way PERMANOVA applied tomean values of mean species richness (Sm), abunda() per each substrate during the threemonitoring years. Not significant p N 0.05; significant 0.0residuals under a reduced model.

    Source of variability d.f. Sm N

    MS Pseudo-F p(perm) MS F

    Year = Y 2 254.51 5.4179 0.046 1218.400 17.928Substrate = S 1 104.71 28.806 0.004 820.130 40.614Survey (Y) 6 46.976 2.9556 0.065 0.006 1.7991S Survey (Y) 6 3.635 0.22871 0.953 0.007 0.597Y S 2 362.68 99.775 0.001 587.620 48.11Residuals 36 24.093 33.796

    Pair-wise tests for term Y S2006 2007 2008 2006 2007p= 0.001 p= 0.006 p= 0.057 p= 0.007 p= 0.019

    differences were highlighted in 2008 (Table 2; Fig. 3c). The low valueof H during the first year on PY was due to the high dominance ofM. acherusicum which contributed alone with more 70% to the totaldensity (Table 1). Accordingly, index followed opposite trends inrespect to H with statistical differences between the two substrates in2006 and 2007 (Table 2; Fig. 3d). M. acherusicum represented themain contributor to these trends.

    3.2. Multivariate results

    PERMANOVA analysis showed a significant interaction betweensubstrates and years due to the different evolution of the benthic assem-blages on the two types of structures (Table 3). PCO plot (84.8% of totalvariation) well visualized this different temporal evolution (Fig. 4).Almost 70% of the PCO variation was due to the assemblage found in2006 at PY, characterized by the exclusive presence of Kurtiellabidentata, a greater abundance of A. demiri in respect to PL, and the ab-sence of many species found on PL. The two substrates became similarduring 2007 and slightly different in 2008, as a consequence of a greateroccurrence on PY of a few organisms such as M. galloprovincialis,P. ciliata and, above all, M. acherusicum characterized by one order ofmagnitude difference in abundance compared to the other species.

    SIMPER analysis confirmed these temporal trends on the two mod-ules, with a greater dissimilarity between PY and PL in the first year(60.20%), lower in 2007 (27.42%) and intermediate in 2008 (32.41%).Indeed, in 2006 only a few taxa were collected on PY; in addition,these species showed lower densities compared to PL. The majorcontributors to these dissimilarities were hard-bottom species such asP. triqueter, M. acherusicum, S. spinulosa, E. rapax, and E. punctatus.

    On PY the low abundance and species richness recorded in the firstyear led to the highest dissimilarities between 2006 and the other twoyears (2006 vs 2007: 66.69%; 2006 vs 2008: 66.56%). Themajor contrib-utors were over all hard-substrate taxa that increased their densities

    nce (N; Log x+ 1), mean ShannonWeaver Diversity index (H) andmean Simpson index5 N p N 0.01; highly significant p b 0.01, p-values are obtained using 4999 permutations of

    H

    p MS F p MS F p

    0.001 0.550 45.424 0.001 0.171 67.997 0.0010.001 0.401 2230.500 0.001 0.136 2251.100 0.0010.257 0.012 2.865 0.621 0.003 2.190 0.6570.867 0.004 0.043 0.856 0.002 0.052 0.9850.001 0.379 2107.700 0.001 0.157 2600.600 0.001

    0.003 0.001

    2008 2006 2007 2008 2006 2007 2008p= 0.006 p= 0.001 p= 0.019 p= 0.052 p= 0.001 p= 0.016 p= 0.096

    image of Fig.2

  • Fig. 3. Temporal variation of univariate indices of macrofaunal communities (SD) on each substrate type. PL = plinth module; PY = pyramid module.

    83A. Spagnolo et al. / Journal of Sea Research 88 (2014) 7886

    over time or settled starting from the second monitoring year. Theywere E. rapax, P. triqueter, and M. acherusicum between 2006 and2007, and M. acherusicum, E. punctatus and Actiniaria nd between2006 and 2008. On PL, the dissimilarities between years were alwayslower than those on PY ranging from 31.69% (2006 vs 2007) to 40.95%(2006 vs 2008). The major contributors to the dissimilarity betweenthe first two years were Lysidice ninetta, E. punctatus, and Syllis gracilis;the dissimilarity between 2006 and 2008 was mainly due to Pilumnushirtellus, Syllis sp., E. punctatus, and P. triqueter.

    4. Discussion

    The detailed knowledge of the benthic communities colonizing anartificial reef is essential to assess the real effectiveness of the man-made structures in enhancing some ecological processes in the marineenvironment (Charbonnel et al., 2011). The biodiversity of an artificialreef is related to different environmental and structural factors, suchas depth, temperature, turbidity, concentration of nutrients along thewater column, morphological complexity of the reef, material, rough-ness of surfaces, shape, and orientation of modules. The deployment ofdifferent types of structures may increase this biodiversity.

    Table 33-way PERMANOVA analyzing separately differences among assemblages at substratetypes (pyramids and plinths) during the three monitoring years. Not significantp N 0.05; significant 0.05 N p N 0.01; highly significant p b 0.01, p-values are obtainedusing 4999 permutations of residuals under a reduced model.

    Source of variability d.f. MS Pseudo-F p (perm)

    Year = Y 2 15,957 27.155 0.001Substrate = S 1 14,416 71.386 0.001Survey (Y) 6 587.62 0.92581 0.557S Survey (Y) 6 201.94 0.31816 0.955Y S 2 11346 56.186 0.001Residuals 36 522.64Pair-wise tests for term Y S2006 2007 2008p (perm)= 0.0010 p (perm)= 0.0040 p (perm)= 0.0040

    The aim of this paper was to evaluate potential differences in thebenthic assemblage between two different types of artificial structuresconstituting the Pedaso artificial reef (Tecnoreef pyramids and con-crete plinths; PY and PL, respectively) and to detect the effectivenessof these structures on the ecosystem functioning.

    The plinth structures showed a consistent settlement of benthicorganisms just after their deployment in agreement with what alreadyobserved on other concrete substrates deployed in the Adriatic Sea(Bombace et al., 1997; Castriota et al., 1996). Instead, a delay of aboutone year in the benthic colonization occurred on PY, as suggested bythe lower density and species richness characterizing these structuresin 2006.

    This difference in the colonization time could be due to the differentcomposition of the concrete utilized for PY and PL, so PY needed of a lon-ger time to become suitable for the settlement of benthic organisms.This result was unexpected as the sea-friendly concrete had beenthought to be more efficient for the benthic colonization. As suggestedby Glasby (2000), the diverse settlement time could be also due to theshape and orientation of the modules: PL are characterized by verticaland continuous surfaces which could be more suitable to pick up theplanktonic larvae. PY have a lot of open spaces and a limited extensionof the surfaces that could make difficult the settlement of larvae duringtheir transport by currents. Moreover, the inclination of the octagonalslabs favors a deposit of a very fine mud on the surfaces; the superficiallayer of this mud may be frequently reshuffled by current and waveaction, with consequent loss of sessile organisms just settled. Neverthe-less, over time a thin layer of mud can cover the structures allowing thesettlement of soft-bottom species.

    Soft sediment can be also entrapped in the interstices amongthe valves, calcareous plates and byssus filaments of some sessile spe-cies, such as mussels and barnacles. This phenomenon has been widelydescribed in previous studies on artificial reefs in the Adriaticand Tyrrhenian seas (Ardizzone et al., 1989; Bombace et al., 1997;Castriota et al., 1996; Nicoletti et al., 2007; Spagnolo et al., 2004).

    Some differences in the composition of the community settled on thetwo types of artificial structures were also highlighted, especially duringthe first monitoring year. Just after the reef deployment most of taxasettled on the modules were sessile, pioneer and fast-growing species,

    image of Fig.3

  • Fig. 4. PCO ordination with projection of individual taxa onto the ordination axes. PL = plinth module; PY = pyramid module.

    84 A. Spagnolo et al. / Journal of Sea Research 88 (2014) 7886

    some of them producing large numbers of planktonic larvae for extendedperiods over the year. They were encrusting polychaetes (P. triqueter,Hydroides pseudouncinata), barnacles (Amphibalanus improvisus,Perforatus perforatus, Balanus trigonus), amphipods (Monocorophiumacherusicum, E. punctatus), and bivalves (M. galloprovincialis, O. edulis,A. ephippium). All these species were collected on PL and only few ofthem (P. triqueter, P. perforatus, M. acherusicum, M. galloprovincialis,O. edulis) on PY. Despite the capability of these organisms to colonizenew substrates, only a few of them such as P. triqueter, Sabellaria spinulosaand, above all,M. acherusicum showed a consistent settlement. P. triqueteris reported as one of the most abundant species in the colonization ofartificial habitats and it is considered a primary fouling organism oncommercially important structures such as buoys, ships' hulls, docksand offshore oil rigs (Crisp, 1965; Gravina et al., 1989; OECD, 1967).This serpulid maintained higher densities in 2006 and 2007 on PL andon PY in 2008. As it is a mussel-fouling species (Cotter, 2003; Keen andNeil, 1980), its different abundances on the two types of modules werelikely linked to the greater occurrence of mussels on PL in the first twoyears after deployment and on PY in the third year. The density ofS. spinulosa was higher on PL during the overall monitoring period. Thispolychaete builds thin crusts of fused tubes frommud, sand or shell frag-ments; it has a relevant bio-construction role (Limpenny et al., 2010) pro-viding a secondary substrate with consequent increase of heterogeneityand species diversity (Reise, 2002). At Pedaso artificial reef only singleworm-tubes and little veneers were observed, likely due to the limitedtemporal observations. Nevertheless, studies carried out in the AdriaticSea showed an abundant settlement of this species on artificial modules(Bombace et al., 1997; Castriota et al., 1996; Fava et al., 2010; Pontiet al., 2010; Spagnolo et al., 2004), where it can develop biogenic hardbottoms. This aspect is very important especiallywhere natural hard sub-strates are absent or rare such as in the northern and central Adriatic Sea.

    Everywhere the most important species during the whole samplingperiod was the invasive, opportunistic amphipod M. acherusicum. Thisspecies is very common in harbor environments, near floating buoysand on artificial structures (Reish et al., 1975; Ruffo, 1982). In fact, itwas always recorded at artificial reefs in the northern and centralAdriatic Sea (Bombace et al., 1997; Castriota et al., 1996; Fabi et al.,1998, 2006; Fava et al., 2010; Ponti et al., 2010). Although this amphipodis typical of hard substrates it is known to require soft sediment to con-struct its tubes (Daniels et al., 2009) and this could explain the greatersettlement on PL in the first two years and on PY in 2008 linked to thedifferent colonization of barnacles, mussels and other species capableto entrap soft sediment. This sediment also provided a suitable habitat

    for a number of soft-bottom invertebrates more abundant on PL in2006 and 2007.

    It is noteworthy that in the first monitoring year the soft-bottombivalve Anadara demiriwas the only species more abundant on PY com-pared to PL and that Kurtiella bidentatawas exclusively collected on PY.It suggests a sort of migration of these organisms from the seabedtowards the PY covered by a greater amount ofmud due to their inclina-tion. In addition, K. bidentata is a common component of disturbed ordredged communities in soft sediments and A. demiri is a second-order opportunistic species able to adapt to physical disturbance(Hill et al., 2011; ICES, 2004), represented in our case by the artificialreef deployment.

    Differences between the two structures reduced in the secondmonitoring year, as suggested by multivariate analyses. In fact, despiteabundance and species richness continued to be higher on PL, a strongincrease in number of individuals and species occurred on PY in 2007compared to 2006, with consequent increase of diversity and reductionof dominance of few species. The changes appeared less important onPL, suggesting the start of the community stabilization on these mod-ules. It is known that the temporal evolution of a benthic communitysettled on new substrates occurs through some ecological successionsmainly consisting of the settlement of pioneer organisms, followed byan explosion of species and then a decrease of richness. Unlike PY, thissituation clearly appeared on PL, where a reduction of individuals andspecies was recorded in 2008. Actually, it is reported that artificialreefs in the northern and central Adriatic Sea reach the equilibriumafter 23 years from the deployment (Bombace, 1987). These findingspartially disagree with the results obtained by Fava et al. (2010) whodid not observe differences in density and/or diversity comparing thebenthic assemblages settled on Technoreef pyramids and on cubicbundles of concrete tubes having similar dimensions in the third yearafter their deployment offshore Po river delta (northern Adriatic Sea).Taking into account that such area is strongly affected by a highsedimentation rate, these disagreements suggest the need to deepenthe knowledge on the colonization time and ecological efficiencyof Technoreef structures in different environments for their futureutilization in planning new artificial reefs.

    In spite of the differences in the colonization time of the two types ofstructures, the overall results indicated that the Pedaso reef can play arelevant role fromanecological point of viewbeing some species settledon the artificial modules (i.e.M. acherusicum, Athanas nitescens, Alpheusdentipes, Marphysa sanguinea, M. galloprovincialis) favorite or preferen-tial prey items of a few reef-dwelling fish such as the brown meagre

    image of Fig.4

  • 85A. Spagnolo et al. / Journal of Sea Research 88 (2014) 7886

    Sciaena umbra, shi drum Umbrina cirrosa, annular seabream Diplodusannularis, striped seabream Lithognathus mormyrus, and comberSerranus cabrilla inhabiting the artificial reefs deployed in the Italianseas (Ardizzone et al., 1997; Fabi and Fiorentini, 1994; Fabi et al.,1998, 2006; Relini et al., 2002; unpublished data). Therefore, themacrozoobenthic species commonly preyed upon by fish and otherpredators certainly constitute an important portion of the trophicnetwork. The isolation of the artificial reef makes possible to confirmthat the hard-substrate species settled on the structures are new tothis locality, previously inhabited by only soft-bottom species(unpublished results). This likely contributed to the creation of anew feeding area, increasing trophic efficiency (Bombace, 1989).Indeed, this role was confirmed by the increased occurrence at thePedaso reef of reef-dwelling fish which are rare in the naturalsandy-mud habitat, such as U. cirrosa (unpublished data).

    Acknowledgments

    Authors acknowledge Marche Region for the financial aid. Manythanks also to the staff of Marine Environment Management Unit ofISMAR Ancona and the crew of the R/V Tecnopesca II who activelycontributed to the data recording.

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    Patterns of colonization and succession of benthic assemblages in two artificial substrates1. Introduction2. Material and methods2.1. Study area2.2. Sampling strategy2.3. Data analysis2.3.1. Univariate analyses2.3.2. Multivariate analyses

    3. Results3.1. Univariate results3.2. Multivariate results

    4. DiscussionAcknowledgmentsReferences

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