INTRODUCTIONTop

Introduced seaweeds are responsible for severe worldwide biological invasions, with important effects on native macroalgal and animal assemblages (Piazzi et al. 2001Piazzi L., Ceccherelli G., Cinelli F. 2001. Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Mar. Ecol. Progr. Ser. 210: 149-159., Buschbaum et al. 2006Buschbaum C., Chapman A.S., Saier B. 2006. How an introduced seaweed can affect epibiota diversity in different coastal systems. Mar. Biol. 148: 743-754., Schaffelke and Hewitt 2007Schaffelke B., Hewitt C.L. 2007. Impact of introduced seaweeds. Bot. Mar. 50: 397-417., McKinnon et al. 2009McKinnon J.G., Gribben P.E., Davis A.R., et al. 2009. Differences in soft-sediment macrobenthic assemblages invaded by Caulerpa taxifolia compared to uninvaded habitats. Mar. Ecol. Prog. Ser. 380: 59-71., Byers et al. 2010Byers J.E., Wright J.T., Gribben P.E. 2010. Variable direct and indirect effects of a habitat-modifying invasive species on mortality of native fauna. Ecology 91: 1787-1798., Pacciardi et al. 2011Pacciardi, L., De Biasi A.M., Piazzi L. 2011. Effects of Caulerpa racemosa invasion on soft-bottom assemblages in the Western Mediterranean Sea. Biol. Inv. 13: 2677-2690.). Effects of invasion may be particularly serious when habitat-forming species are involved, as each change in population of these organisms may have severe effects on associated assemblages (Gribben et al. 2009Gribben P.E., Byers J.E., Clements M., et al. 2009. Behavioural interactions between ecosystem engineers control community species richness. Ecol. Lett. 12: 1127-1136.). Macroalgae are important habitat-forming organisms in temperate coastal systems, providing a suitable habitat for many epiphytes and mobile invertebrates (Edgar and Moore 1986Edgar G.J., Moore P.G. 1986. Macro-algae as habitats for motile macrofauna. Monogr. Biol. 4: 255-277., Taylor and Cole 1994Taylor R.B., Cole R.G. 1994. Mobile epifauna on subtidal brown seaweeds in northeastern New Zealand. Mar. Ecol. Progr. Ser. 115: 271-282., Cacabelos et al. 2010Cacabelos E., Olabarria C., Incera M., et al. 2010. Effects of habitat structure and tidal height on epifaunal assemblages associated with macroalgae. Estuar. Coast. Shelf Sci. 89: 43-52.) and influencing the structure and the biodiversity of coastal systems (Tanaka and Leite 2003Tanaka M.O., Leite F.P.P. 2003 Spatial scaling in the distribution of macrofauna associated with Sargassum stenophyllum (Mertens) Martius: analyses of faunal groups, gammarid life habits, and assemblage structure. J. Exp. Mar. Biol. Ecol. 293: 1-22., Bates and Dewreede 2007Bates C.R., Dewreede R.E. 2007. Do changes in seaweed biodiversity influence associated invertebrate epifauna? J. Exp. Mar. Biol. Ecol. 344: 206-214., Wikström and Kautsky 2007Wikström S.A., Kautsky L. 2007. Structure and diversity of invertebrate communities in the presence and absence of canopy-forming Fucus vesiculosus in the Baltic Sea. Estuar. Coast. Shelf Sci. 72: 168-176.).

In the Mediterranean Sea, species of genus Cystoseira are the most important habitat-forming species in shallow rocky bottoms (Ballesteros 1990aBallesteros E. 1990a. Structure and dynamics of the Cystoseira caespitosa Sauvageau (Fucales, Phaeophyceae) community in the North-Western Mediterranean. Sci. Mar. 54: 155-168., bBallesteros E. 1990b. Structure and dynamics of the community of Cystoseira zosteroides (Turner) C. Agardh (Fucales, Phaeophyceae) in the northwestern Mediterranean. Sci. Mar. 54: 217-229.), where they play a key role in determining patterns of diversity (Sales and Ballesteros 2009Sales M., Ballesteros E. 2009. Shallow Cystoseira (Fucales: Ochrophyta) assemblages thriving in sheltered areas from Menorca (NW Mediterranean): relationships with environmental factors and anthropogenic pressures. Estuar. Coast. Shelf Sci. 84: 476-482.). The erect structure of Cystoseira thalli, like those of other canopy species, can limit the spread of most invasive seaweeds, constituting a mechanical barrier against the invasion (Bulleri et al. 2010Bulleri F., Balata D., Bertocci I., et al. 2010. The seaweed Caulerpa racemosa on Mediterranean rocky reefs: from passenger to driver of ecological change. Ecology 91: 2205-2212.). However, invaders such as the Rhodophyta Lophocladia lallemandii (Montagne) F. Schmitz (Bedini et al. 2011Bedini R., Bonechi L., Piazzi L. 2011. Spread of the introduced red alga Lophocladia lallemandii in the Tuscan Archipelago (NW Mediterranean Sea). Cryptogamie Algol. 32: 383-391.) seem to be facilitated by the presence of Cystoseira beds. This species is widespread in tropical and subtropical waters and was probably introduced into the Mediterranean Sea through the Suez Canal (Boudouresque and Verlaque 2002Boudouresque C.F., Verlaque M. 2002. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar. Pollut. Bull. 44: 32-38.). Until now, in the Mediterranean Sea, invasive events by L. lallemandii have only been described in the Balearic Islands (Patzner 1998Patzner R. 1998. The invasion of Lophocladia (Rhodomelaceae, Lophotaliae) at the northern coast of Ibiza (Western Mediterranean Sea). Boll. Soc. Hist. Nat. Balears 41: 75-80., Cebrian and Ballesteros 2010Cebrian E., Ballesteros E. 2010. Invasion of Mediterranean benthic assemblages by red alga Lophocladia lallemandii (Montagne) F. Schmitz: Depth-related temporal variability in biomass and phenology. Aquat. Bot. 92: 81-85., Marbà et al. 2014Marbà N., Arthur R., Alcoverro T. 2014. Getting turfed: The population and habitat impacts of Lophocladia lallemandii invasions on endemic Posidonia oceanica meadows Aq. Bot. 116: 76-82.) and in the Tuscan Archipelago (Bedini et al. 2011Bedini R., Bonechi L., Piazzi L. 2011. Spread of the introduced red alga Lophocladia lallemandii in the Tuscan Archipelago (NW Mediterranean Sea). Cryptogamie Algol. 32: 383-391.). In both areas, the alga is able to reach high values of percentage cover and biomass (Bedini et al. 2011Bedini R., Bonechi L., Piazzi L. 2011. Spread of the introduced red alga Lophocladia lallemandii in the Tuscan Archipelago (NW Mediterranean Sea). Cryptogamie Algol. 32: 383-391.) on rocky bottoms and in seagrass meadows (Ballesteros et al. 2007Ballesteros E., Cebrian E., Alcoverro T. 2007. Mortality of shoots of Posidonia oceanica following meadow invasion by the red alga Lophocladia lallemandii. Bot. Mar. 50: 8-13., Sureda et al. 2008Sureda A., Box A., Terrados J., et al. 2008. Antioxidant response of the seagrass Posidonia oceanica when epiphytized by the invasive macroalga Lophocladia lallemandii. Mar. Environ. Res. 66: 359-363., Marbà et al. 2014Marbà N., Arthur R., Alcoverro T. 2014. Getting turfed: The population and habitat impacts of Lophocladia lallemandii invasions on endemic Posidonia oceanica meadows Aq. Bot. 116: 76-82.). Cystoseira beds are particularly subjected to invasion (Cebrian and Ballesteros 2007Cebrian E., Ballesteros E. 2007. Invasion of the alien species Lophocladia lallemandii in Eivissa-Formentera (Balearic Islands). In: Pergent Martini C., El Asmi S. (eds), Proceed. 3rd Med. Symp. Mar. Vegetation, Marseilles, France. C. Le Ravallec Ed., RAC/SPA Publ., Tunis, pp. 34-41., Bedini et al. 2011Bedini R., Bonechi L., Piazzi L. 2011. Spread of the introduced red alga Lophocladia lallemandii in the Tuscan Archipelago (NW Mediterranean Sea). Cryptogamie Algol. 32: 383-391.), as thalli of these algae may offer a valuable substrate for L. lallemandii anchoring (Bedini et al. 2011Bedini R., Bonechi L., Piazzi L. 2011. Spread of the introduced red alga Lophocladia lallemandii in the Tuscan Archipelago (NW Mediterranean Sea). Cryptogamie Algol. 32: 383-391.). Negative effects of L. lallemandii invasion have been described for sessile invertebrates in meadows of the seagrass Posidonia oceanica (L.) Delile (Cabanellas-Reboredo et al. 2010Cabanellas-Reboredo M., Blanco A., Deudero S., et al. 2010. Effects of the invasive macroalga Lophocladia lallemandii on the diet and trophism of Pinna nobilis (Mollusca: Bivalvia) and its guests Pontonia pinnophylax and Nepinnotheres pinnotheres (Crustacea: Decapoda). Sci. Mar. 74: 101-110., Deudero et al. 2010Deudero S., Blanco A., Box A., et al. 2010. Interaction between the invasive macroalga Lophocladia lallemandii and the bryozoan Reteporella grimaldii at seagrass meadows: density and physiological responses. Biol. Inv. 12: 41-52.), while no information is available about effects of invasion on mobile macro-invertebrates.

The present study aimed to compare the structure of mobile epifaunal assemblages associated with Cystoseira beds between areas invaded and not invaded by Lophocladia lallemandii. The following hypotheses were tested: i) epifaunal assemblages associated with Cystoseira beds invaded by L. lallemandii differ in species composition and abundance from those colonizing non-invaded beds, ii) temporal patterns of assemblages vary between conditions, iii) differences between conditions are greater during the period of maximum vegetative growth of L. lallemandii.

MATERIALS AND METHODS

The study was carried out around the Island of Pianosa, in the Tuscan Archipelago National Park (northwestern Mediterranean Sea) at 5 m depth (Fig. 1). Lophocladia lallemandii started to spread around the island in 2008, and in 2010 it colonized with variable coverage a stretch of about 10 km between 2 and 10 m depth (Bedini et al. 2011Bedini R., Bonechi L., Piazzi L. 2011. Spread of the introduced red alga Lophocladia lallemandii in the Tuscan Archipelago (NW Mediterranean Sea). Cryptogamie Algol. 32: 383-391.). The alga begins to grow in July, reaches its maximum abundance in November and completely disappears between January and June (Bedini et al. 2011Bedini R., Bonechi L., Piazzi L. 2011. Spread of the introduced red alga Lophocladia lallemandii in the Tuscan Archipelago (NW Mediterranean Sea). Cryptogamie Algol. 32: 383-391.). All around the island, the rocky bottom between 4 m and 8 m of depth is colonized by Cystoseira spp. assemblages (mostly C. crinita Duby and C. brachycarpa var. balearica (Savageau) Giaccone). In invaded C. crinita beds, the biomass of L. lallemandii in November was about 0.2 kg dw m^–2 (Bedini et al. 2011Bedini R., Bonechi L., Piazzi L. 2011. Spread of the introduced red alga Lophocladia lallemandii in the Tuscan Archipelago (NW Mediterranean Sea). Cryptogamie Algol. 32: 383-391.).

Four areas of about 100 m² were selected in C. crinita beds along the southern coast of the island, two of them invaded by L. lallemandii and two non-invaded; areas were randomly chosen among those available for each condition (Fig. 1). On four dates during a one-year period (May 2010, August 2010, November 2010, May 2011), three samples were collected in each area. Samples were constituted by all organisms present within an area of 400 cm². All mobile macro-invertebrates present in each sample were identified and the abundance of each species was expressed as number of individuals m^–2. Epifaunal assemblages were analyzed by Permutational Analysis of Variances (PERMANOVA, Anderson 2001Anderson M.J. 2001. A new method for a non-parametric multivariate analysis of variance. Aust. Ecol. 26: 32-46.). A three-way model was used with Condition (Invaded vs. Non-invaded) as a fixed factor, Date (4 levels) as a random factor crossed with Condition and Area (2 levels) as a random factor nested in Condition. Data were log(x+1) transformed before calculation of the Bray-Curtis index of dissimilarity. The Monte-Carlo procedure was used when the number of permutations was low. A two-dimensional multidimensional scaling (n-MDS) was used for a graphical representation of results. The SIMPER routine was performed to establish which taxa most contributed to the dissimilarity between conditions and dates.

The number of taxa per sample and the abundance of organisms were detected by analyses of variance (ANOVA), with the same factors and levels used for multivariate analyses; Cochran’s C-test was utilised before each analysis to check for homogeneity of variance and data were transformed when necessary (Underwood 1997Underwood A.J. 1997. Experiments in ecology. Their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge.).

RESULTSTop

A total of 150 taxa were identified: 42 Polychaeta, 78 Arthropoda, 26 Mollusca and 4 Echinodermata (Table 1).

ANOVA analyses detected a significant difference among dates for the abundance of organisms (F=80.7, p=0.003) and the mean number of taxa per sample (F=20.6, p=0.001), while differences between conditions were not significant (F=2.6, p=0.120 and F=44.6, p=0.071 respectively). Both variables were higher on spring dates than on the others (Fig. 2).

PERMANOVA detected a significant interaction between Date and Condition (Table 2). The pairwise test showed that differences between conditions were significant in November 2010 but not on the other sampling dates (Table 2). In invaded condition, May 2010 and May 2011 differed from August and November 2010; in non-invaded condition, November 2010 differed from the other dates. MDS showed a greater disjunction between invaded and non-invaded assemblages in November 2010 than in the other sampling dates (Fig. 3).

The SIMPER test showed that the main differences between assemblages in November 2010 were the greater abundance of amphipods (Caprella acanthifera, Ampithoe ramondi, Dexamine spiniventris), isopods (Idotea granulosa) and polychaetes (Platynereis dumerilii) in invaded areas and the greater abundance of molluscs (Rissoa variabilis, Barleeia unifasciata) and decapods (Calcinus tubularis, Hippolyte longirostris, Cestopagurus timidus) in non-invaded areas (Table 3).

The main differences between spring sampling dates (May 2010 and May 2011) and autumn ones (November 2010) were a higher abundance of organisms in spring, especially the molluscs Barleeia unifasciata and Bittium latreillii and the amphipods Hyale schmidti, Ampithoe ramondi, Phtisica marina and Caprella spp.; only a few taxa were more abundant in autumn, including the decapods Cestopagurus timidus and Calcinus tubularis (Table 3).

DISCUSSIONTop

Results of the study described the structure of epifaunal assemblages associated with Cystoseira crinita beds and highlighted differences between areas invaded by Lophocladia lalemandii and non-invaded areas related to the vegetative cycle of Rhodophyta.

Epifaunal assemblages associated with C. crinita were characterized by high abundance and diversity, compared with those described for other seaweed habitats (Gestoso et al. 2012Gestoso I., Olabarria C., Troncoso J.S. 2012. Effects of macroalgal identity on epifaunal assemblages: native species versus the invasive species Sargassum muticum. Helgol. Mar. Res. 66: 159-166., Janiak et al. 2012Janiak D.S., Whitlatch R.B. 2012. Epifaunal and algal assemblages associated with the native Chondrus crispus (Stackhouse) and the non-native Grateloupia turuturu (Yamada) in eastern Long Island Sound. J. Exp. Mar. Biol. Ecol. 413: 38-44., Engelen et al. 2013Engelen A.H., Primo A.L., Cruz T., et al. 2013. Faunal differences between the invasive brown macroalga Sargassum muticum and competing native macroalgae. Biol. Inv. 15: 171-183.). Macroalgal assemblages associated with Mediterranean Cystoseira beds are well known (Boudouresque 1972Boudouresque C.F. 1972. Recherches de bionomie analytique structurale et expérimentale sur les peuplements benthiques sciaphiles de Méditerranée occidentale (fraction algale): la sous-strate sciaphile d’un peuplement photophile de mode calme, le peuplement à Cystoseira crinita. Bull. Mus. Hist. nat. Marseille 32: 253-263., Sales and Ballesteros 2010Sales M., Ballesteros E. 2010. Long-term comparison of algal assemblages dominated by Cystoseira crinita (Fucales, Heterokontophyta) from Cap Corse (Corsica, North Western Mediterranean). Eur. J. Phycol. 45: 404-412.), while epifaunal assemblages have been less investigated and knowledge is limited to particular taxa (Arrontes and Anadon 1990Arrontes J., Anadon R. 1990. Seasonal variation and population dynamics of isopods inhabiting intertidal macroalgae. Sci. Mar. 54: 231-240., Chemello and Milazzo 2002Chemello R., Milazzo M. 2002. Effect of algal architecture on associated fauna: some evidence from phytal molluscs. Mar. Biol. 140: 981-990., Fraschetti et al. 2002Fraschetti S., Giangrande A., Terlizzi A., et al. 2002. Spatio-temporal variation of hydroids and polychaetes associated with Cystoseira amentacea (Fucales: Phaeophyceae). Mar. Biol. 140: 949-957.). The present study, analysing the whole epifaunal assemblages, confirms the important ecological role of Cystoseira beds in Mediterranean coastal systems. Cystoseira thalli, like those of other structurally complex algae (Tanaka and Leite 2003Tanaka M.O., Leite F.P.P. 2003 Spatial scaling in the distribution of macrofauna associated with Sargassum stenophyllum (Mertens) Martius: analyses of faunal groups, gammarid life habits, and assemblage structure. J. Exp. Mar. Biol. Ecol. 293: 1-22., Wikström and Kautsky 2007Wikström S.A., Kautsky L. 2007. Structure and diversity of invertebrate communities in the presence and absence of canopy-forming Fucus vesiculosus in the Baltic Sea. Estuar. Coast. Shelf Sci. 72: 168-176.), may create a high number of microhabitats, hosting organisms with different requirements (Russo 1990Russo A.R. 1990. The role of seaweed complexity in structuring Hawaiian epiphytal amphipod communities. Hydrobiologia 194: 1-12., Gee and Warwick 1994Gee J.M., Warwick R.M. 1994. Metazoan community structure in relation to the fractal dimensions of marine macroalgae. Mar. Ecol. Progr. Ser. 103: 141-150., Taylor 1998Taylor R.B. 1998. Seasonal variation in assemblages of mobile epifauna inhabiting three subtidal brown seaweeds in northeastern New Zealand. Hydrobiologia 361: 25-35.). Moreover, Cystoseira beds may offer an effective refuge from predators and abundant food availability (Buschmann 1990Buschmann A.H. 1990. Intertidal macroalgae as refuge and food for amphipoda in Central Chile. Aq. Bot. 36: 237-245., Holmlund et al. 1990Holmlund M.B., Peterson C.H., Hay M.E. 1990. Does algal morphology affect amphipod susceptibility to fish predation? J. Exp. Mar. Biol. Ecol. 139: 65-83., Martin-Smith 1993Martin-Smith, K.M. 1993. Abundance of mobile epifauna: the role of habitat complexity and predation by fishes. J. Exp. Mar. Biol. Ecol. 174: 243-260.).

The sampling design of the study was not suitable for assessing the temporal dynamics of the assemblages. However, in non-invaded areas, epifaunal assemblages associated with C. crinita showed great differences between sampling dates, suggesting the occurrence of seasonal patterns which should be investigated through further studies. Seasonal variations in epifaunal assemblages associated with Cystoseira spp. as a consequence of taxa life cycles and modifications in seaweed structure have already been described (Fraschetti et al. 2002Fraschetti S., Giangrande A., Terlizzi A., et al. 2002. Spatio-temporal variation of hydroids and polychaetes associated with Cystoseira amentacea (Fucales: Phaeophyceae). Mar. Biol. 140: 949-957., Gozler et al. 2010Gozler A.M., Kopuz U., Agirbas E. 2010. Seasonal changes of invertebrate fauna associated with Cystoseira barbata facies of Southeastern Black Sea coast. Afr. J. Biotech. 9: 8852-8859.). In fact, Cystoseira are perennial species with seasonal cycles of vegetative growth: they reach their maximum size in spring-summer period, while in autumn they lose secondary branches, changing their habitus (Sales and Ballesteros 2012Sales M., Ballesteros E. 2012. Seasonal dynamics and annual production of Cystoseira crinita (Fucales: Ochrophyta)-dominated assemblages from the northwestern Mediterranean. Sci. Mar. 76: 403-408.). Temporal changes of epifaunal associated with Cystoseira spp. can also be caused by changes of macroalgal epiphyte assemblages. In fact, Cystoseira species host an abundant assemblage of macroalgae, mostly constituted by seasonal filamentous species (Ballesteros et al. 2009Ballesteros E., Garrabou J., Hereu B., et al. 2009. Deep-water stands of Cystoseira zosteroides C. Agardh (Fucales, Ochrophyta) in the Northwestern Mediterranean: insights into assemblage structure and population dynamics. Estuar. Coast. Shelf Sci. 82: 477-484., Sales and Ballesteros 2010Sales M., Ballesteros E. 2010. Long-term comparison of algal assemblages dominated by Cystoseira crinita (Fucales, Heterokontophyta) from Cap Corse (Corsica, North Western Mediterranean). Eur. J. Phycol. 45: 404-412.), which may change greatly throughout the year following the growth cycles of the main taxa.

The seasonal development of L. lallemandii overlaps this scenario. In fact, the study results showed that epifaunal assemblages associated with Cystoseira crinita beds differed between areas invaded and not invaded by Lophocladia lallemandii in November, when the invasive species reached maximum values of cover and biomass (Bedini et al. 2011Bedini R., Bonechi L., Piazzi L. 2011. Spread of the introduced red alga Lophocladia lallemandii in the Tuscan Archipelago (NW Mediterranean Sea). Cryptogamie Algol. 32: 383-391.), while assemblages showed no differences between conditions in other periods of the year.

The main effects of the presence of L. lallemandii were an increase in amphipods and polychaetes and a decrease in decapods and molluscs. Species more linked to the architecture of Cystoseira thalli may be damaged by substrate modification; in fact, many epifaunal organisms are related to particular macroalgae and may be strongly influenced by the presence of invasive species (Viejo 1999Viejo R.M. 1999. Mobile epifauna inhabiting the invasive Sargassum muticum and two local seaweeds on northern Spain. Aquat. Bot. 64: 131-149., Gestoso et al. 2010Gestoso I., Olabarria C., Troncoso J.S. 2010. Variability of epifaunal assemblages associated with native and invasive macroalgae. Mar. Freshwat. Res. 61: 724-731.). On the other hand, polychaetes are not specifically facilitated by the morphology of canopy seaweeds, and food preference and/or different substrate requirements may well cause their increase in invaded areas; in fact, several polychaete species may be facilitated by turfs created by L. lallemandii, where sediment and organic matter could be trapped. Caprellid amphipods need cylindrical substrates with a small diameter to be encircled by pereopods in order to avoid being dislodged by water movements (Aoki and Kikuchi 1990Aoki M., Kikuchi T. 1990. Habitat adaptations of caprellid amphipods and the importance of epiphytic secondary habitats in a Sargassum patens bed in Amakusa, southern Japan. Publ. Arnakusa Mar. Biol. Lab. Kyushu Univ. 10: 123-133. ), and the presence of L. lallemandii can increase the substrate available for anchoring. Moreover, herbivore amphipods, ampithoids in particular, may also be influenced by the increase in food availability in invaded areas (Duffy 1990Duffy J.E. 1990. Amphipods on seaweeds: partners or pests? Oecologia 83: 267-276., Duffy and Hay 2000Duffy J.E., Hay M.E. 2000. Strong impacts of grazing amphipods on the organization of a benthic community. Ecol. Monogr. 70: 237-263., Poore et al. 2008Poore A.G.B., Hill N.A., Sotka E.E. 2008. Phylogenetic and geographic variation in host breadth and composition by herbivorous amphipods in the family Ampithoidae. Evolution 62: 21-38.).

The results show that the effects of L. lallemandii colonization on mobile organisms are related more to changes in species composition than to changes in patterns of diversity. This finding agrees with those described for other introduced seaweeds, suggesting that, while macroalgal invasions strongly affect diversity of sessile assemblages (Ribera and Boudouresque 1995Ribera M.A., Boudouresque C.F. 1995. Introduced marine plants, with special reference to macroalgae: mechanisms and impact. Progr. Phycol. Res. 11: 187-268., Piazzi et al. 2001Piazzi L., Ceccherelli G., Cinelli F. 2001. Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Mar. Ecol. Progr. Ser. 210: 149-159., Schaffelke and Hewitt 2007Schaffelke B., Hewitt C.L. 2007. Impact of introduced seaweeds. Bot. Mar. 50: 397-417., Baldacconi and Corriero 2009Baldacconi R., Corriero G. 2009. Effects of the spread of the alga Caulerpa racemosa var. cylindracea on the sponge assemblage from coralligenous concretions of the Apulian coast (Ionian Sea, Italy). Mar. Ecol. 30: 337-345., Zuljevic and Nikolic 2008Zuljevic A., Nikolic V. 2008. The highly invasive alga Caulerpa racemosa var. cylindracea poses a new threat to the banks of the coral Cladocora caespitosa in the Adriatic Sea. Coral Reefs, 27: 441.), the effects of invasions on mobile organisms are more related to changes in the structure of assemblages (Vázquez-Luis et al. 2009Vázquez-Luis M., Sanchez-Jerez P., Bayle-Sempere J.T. 2009. Comparison between amphipod assemblages associated with Caulerpa racemosa var. cylindracea and those of other Mediterranean habitats on soft substrate. Estuar. Coast. Shelf Sci. 84: 161-170., Gestoso et al. 2012Gestoso I., Olabarria C., Troncoso J.S. 2012. Effects of macroalgal identity on epifaunal assemblages: native species versus the invasive species Sargassum muticum. Helgol. Mar. Res. 66: 159-166., Janiak et al. 2012Janiak D.S., Whitlatch R.B. 2012. Epifaunal and algal assemblages associated with the native Chondrus crispus (Stackhouse) and the non-native Grateloupia turuturu (Yamada) in eastern Long Island Sound. J. Exp. Mar. Biol. Ecol. 413: 38-44., Pacciardi et al. 2011Pacciardi, L., De Biasi A.M., Piazzi L. 2011. Effects of Caulerpa racemosa invasion on soft-bottom assemblages in the Western Mediterranean Sea. Biol. Inv. 13: 2677-2690., Engelen et al. 2013Engelen A.H., Primo A.L., Cruz T., et al. 2013. Faunal differences between the invasive brown macroalga Sargassum muticum and competing native macroalgae. Biol. Inv. 15: 171-183.).

Differences between invaded and non-invaded beds were not evident five months after the disappearance of L. lallemandii. The effects of invasion on Cystoseira-associated assemblages seem to be limited to the period of vegetative growth of the alga and reversible during the period of its vegetative rest. Recovery of assemblages could be related both to the intrinsic characteristics of organisms and to the lack of damage to C. crinita thalli. Macro-invertebrate assemblages are able to respond rapidly to various kinds of impacts (Teixeira et al. 2009Teixeira H., Neto M.J., Patricio J., et al. 2009. Quality assessment of benthic macroinvertebrates under the scope of WFD using BAT, the Benthic Assessment Tool. Mar. Pollut. Bull. 58: 1477-1486.), but they are also able to recover their original structure quickly after disturbance because of the short life cycles of the organisms (Lu and Shio-Sun Wu 2007Lu L., Shio-Sun Wu R. 2007. Seasonal effects of recolonization of macrobenthos in defaunated sediments: a series of field experiments. J. Exp. Mar. Biol. Ecol. 351: 199-210., Pacciardi et al. 2011Pacciardi, L., De Biasi A.M., Piazzi L. 2011. Effects of Caulerpa racemosa invasion on soft-bottom assemblages in the Western Mediterranean Sea. Biol. Inv. 13: 2677-2690.). Moreover, recovery followed the return of the habitat to its original structure. In fact, until now, no evidence of Cystoseira regression has been observed in invaded areas of Pianosa Island (Bedini et al. 2011Bedini R., Bonechi L., Piazzi L. 2011. Spread of the introduced red alga Lophocladia lallemandii in the Tuscan Archipelago (NW Mediterranean Sea). Cryptogamie Algol. 32: 383-391.). Although L. lallemandii completely cover Cystoseira thalli during the period of spread, several months without the invasive alga seem to be enough to avoid severe damage to Cystoseira beds.

The effects of L. lallemandii invasion at Pianosa Island seem to be less severe than those described in the Balearic Islands. However, the colonization of L. lallemandii in the Tuscan Archipelago has recently started and more severe effects could be hypothesized after longer periods of colonization on both Cystoseira beds and its associated assemblages, indicating the importance of monitoring the spread of the invasive alga.

ACKNOWLEDGEMENTSTop

We wish to thank the Italian National Research Council (CNR) for supporting the study and S. Oliva for the Spanish translation of the summary.

REFERENCESTop

Anderson M.J. 2001. A new method for a non-parametric multivariate analysis of variance. Aust. Ecol. 26: 32-46.
http://dx.doi.org/10.1111/j.1442-9993.2001.01070.pp.x

Aoki M., Kikuchi T. 1990. Habitat adaptations of caprellid amphipods and the importance of epiphytic secondary habitats in a Sargassum patens bed in Amakusa, southern Japan. Publ. Arnakusa Mar. Biol. Lab. Kyushu Univ. 10: 123-133.

Arrontes J., Anadon R. 1990. Seasonal variation and population dynamics of isopods inhabiting intertidal macroalgae. Sci. Mar. 54: 231-240.

Baldacconi R., Corriero G. 2009. Effects of the spread of the alga Caulerpa racemosa var. cylindracea on the sponge assemblage from coralligenous concretions of the Apulian coast (Ionian Sea, Italy). Mar. Ecol. 30: 337-345.
http://dx.doi.org/10.1111/j.1439-0485.2009.00282.x

Ballesteros E. 1990a. Structure and dynamics of the Cystoseira caespitosa Sauvageau (Fucales, Phaeophyceae) community in the North-Western Mediterranean. Sci. Mar. 54: 155-168.

Ballesteros E. 1990b. Structure and dynamics of the community of Cystoseira zosteroides (Turner) C. Agardh (Fucales, Phaeophyceae) in the northwestern Mediterranean. Sci. Mar. 54: 217-229.

Ballesteros E., Cebrian E., Alcoverro T. 2007. Mortality of shoots of Posidonia oceanica following meadow invasion by the red alga Lophocladia lallemandii. Bot. Mar. 50: 8-13.
http://dx.doi.org/10.1515/BOT.2007.002

Ballesteros E., Garrabou J., Hereu B., et al. 2009. Deep-water stands of Cystoseira zosteroides C. Agardh (Fucales, Ochrophyta) in the Northwestern Mediterranean: insights into assemblage structure and population dynamics. Estuar. Coast. Shelf Sci. 82: 477-484.
http://dx.doi.org/10.1016/j.ecss.2009.02.013

Bates C.R., Dewreede R.E. 2007. Do changes in seaweed biodiversity influence associated invertebrate epifauna? J. Exp. Mar. Biol. Ecol. 344: 206-214.
http://dx.doi.org/10.1016/j.jembe.2007.01.002

Bedini R., Bonechi L., Piazzi L. 2011. Spread of the introduced red alga Lophocladia lallemandii in the Tuscan Archipelago (NW Mediterranean Sea). Cryptogamie Algol. 32: 383-391.
http://dx.doi.org/10.7872/crya.v32.iss4.2011.383

Boudouresque C.F. 1972. Recherches de bionomie analytique structurale et expérimentale sur les peuplements benthiques sciaphiles de Méditerranée occidentale (fraction algale): la sous-strate sciaphile d’un peuplement photophile de mode calme, le peuplement à Cystoseira crinita. Bull. Mus. Hist. nat. Marseille 32: 253-263.

Boudouresque C.F., Verlaque M. 2002. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar. Pollut. Bull. 44: 32-38.
http://dx.doi.org/10.1016/S0025-326X(01)00150-3

Bulleri F., Balata D., Bertocci I., et al. 2010. The seaweed Caulerpa racemosa on Mediterranean rocky reefs: from passenger to driver of ecological change. Ecology 91: 2205-2212.
http://dx.doi.org/10.1890/09-1857.1

Buschmann A.H. 1990. Intertidal macroalgae as refuge and food for amphipoda in Central Chile. Aq. Bot. 36: 237-245.
http://dx.doi.org/10.1016/0304-3770(90)90037-L

Buschbaum C., Chapman A.S., Saier B. 2006. How an introduced seaweed can affect epibiota diversity in different coastal systems. Mar. Biol. 148: 743-754.
http://dx.doi.org/10.1007/s00227-005-0128-9

Byers J.E., Wright J.T., Gribben P.E. 2010. Variable direct and indirect effects of a habitat-modifying invasive species on mortality of native fauna. Ecology 91: 1787-1798.
http://dx.doi.org/10.1890/09-0712.1

Cabanellas-Reboredo M., Blanco A., Deudero S., et al. 2010. Effects of the invasive macroalga Lophocladia lallemandii on the diet and trophism of Pinna nobilis (Mollusca: Bivalvia) and its guests Pontonia pinnophylax and Nepinnotheres pinnotheres (Crustacea: Decapoda). Sci. Mar. 74: 101-110.
http://dx.doi.org/10.3989/scimar.2010.74n1101

Cacabelos E., Olabarria C., Incera M., et al. 2010. Effects of habitat structure and tidal height on epifaunal assemblages associated with macroalgae. Estuar. Coast. Shelf Sci. 89: 43-52.
http://dx.doi.org/10.1016/j.ecss.2010.05.012

Cebrian E., Ballesteros E. 2007. Invasion of the alien species Lophocladia lallemandii in Eivissa-Formentera (Balearic Islands). In: Pergent Martini C., El Asmi S. (eds), Proceed. 3rd Med. Symp. Mar. Vegetation, Marseilles, France. C. Le Ravallec Ed., RAC/SPA Publ., Tunis, pp. 34-41.

Cebrian E., Ballesteros E. 2010. Invasion of Mediterranean benthic assemblages by red alga Lophocladia lallemandii (Montagne) F. Schmitz: Depth-related temporal variability in biomass and phenology. Aquat. Bot. 92: 81-85.
http://dx.doi.org/10.1016/j.aquabot.2009.10.007

Chemello R., Milazzo M. 2002. Effect of algal architecture on associated fauna: some evidence from phytal molluscs. Mar. Biol. 140: 981-990.
http://dx.doi.org/10.1007/s00227-002-0777-x

Deudero S., Blanco A., Box A., et al. 2010. Interaction between the invasive macroalga Lophocladia lallemandii and the bryozoan Reteporella grimaldii at seagrass meadows: density and physiological responses. Biol. Inv. 12: 41-52.
http://dx.doi.org/10.1007/s10530-009-9428-1

Duffy J.E. 1990. Amphipods on seaweeds: partners or pests? Oecologia 83: 267-276.
http://dx.doi.org/10.1007/BF00317764

Duffy J.E., Hay M.E. 2000. Strong impacts of grazing amphipods on the organization of a benthic community. Ecol. Monogr. 70: 237-263.
http://dx.doi.org/10.1890/0012-9615(2000)070[0237:SIOGAO]2.0.CO;2

Edgar G.J., Moore P.G. 1986. Macro-algae as habitats for motile macrofauna. Monogr. Biol. 4: 255-277.

Engelen A.H., Primo A.L., Cruz T., et al. 2013. Faunal differences between the invasive brown macroalga Sargassum muticum and competing native macroalgae. Biol. Inv. 15: 171-183.
http://dx.doi.org/10.1007/s10530-012-0276-z

Fraschetti S., Giangrande A., Terlizzi A., et al. 2002. Spatio-temporal variation of hydroids and polychaetes associated with Cystoseira amentacea (Fucales: Phaeophyceae). Mar. Biol. 140: 949-957.
http://dx.doi.org/10.1007/s00227-001-0770-9

Gee J.M., Warwick R.M. 1994. Metazoan community structure in relation to the fractal dimensions of marine macroalgae. Mar. Ecol. Progr. Ser. 103: 141-150.
http://dx.doi.org/10.3354/meps103141

Gestoso I., Olabarria C., Troncoso J.S. 2010. Variability of epifaunal assemblages associated with native and invasive macroalgae. Mar. Freshwat. Res. 61: 724-731.
http://dx.doi.org/10.1071/MF09251

Gestoso I., Olabarria C., Troncoso J.S. 2012. Effects of macroalgal identity on epifaunal assemblages: native species versus the invasive species Sargassum muticum. Helgol. Mar. Res. 66: 159-166
http://dx.doi.org/10.1007/s10152-011-0257-0

Gozler A.M., Kopuz U., Agirbas E. 2010. Seasonal changes of invertebrate fauna associated with Cystoseira barbata facies of Southeastern Black Sea coast. Afr. J. Biotech. 9: 8852-8859.

Gribben P.E., Byers J.E., Clements M., et al. 2009. Behavioural interactions between ecosystem engineers control community species richness. Ecol. Lett. 12: 1127-1136.
http://dx.doi.org/10.1111/j.1461-0248.2009.01366.x

Holmlund M.B., Peterson C.H., Hay M.E. 1990. Does algal morphology affect amphipod susceptibility to fish predation? J. Exp. Mar. Biol. Ecol. 139: 65-83.
http://dx.doi.org/10.1016/0022-0981(90)90039-F

Janiak D.S., Whitlatch R.B. 2012. Epifaunal and algal assemblages associated with the native Chondrus crispus (Stackhouse) and the non-native Grateloupia turuturu (Yamada) in eastern Long Island Sound. J. Exp. Mar. Biol. Ecol. 413: 38-44.
http://dx.doi.org/10.1016/j.jembe.2011.11.016

Lu L., Shio-Sun Wu R. 2007. Seasonal effects of recolonization of macrobenthos in defaunated sediments: a series of field experiments. J. Exp. Mar. Biol. Ecol. 351: 199-210.
http://dx.doi.org/10.1016/j.jembe.2007.06.008

Marbà N., Arthur R., Alcoverro T. 2014. Getting turfed: The population and habitat impacts of Lophocladia lallemandii invasions on endemic Posidonia oceanica meadows Aq. Bot. 116: 76-82.

Martin-Smith, K.M. 1993. Abundance of mobile epifauna: the role of habitat complexity and predation by fishes. J. Exp. Mar. Biol. Ecol. 174: 243-260.
http://dx.doi.org/10.1016/0022-0981(93)90020-O

McKinnon J.G., Gribben P.E., Davis A.R., et al. 2009. Differences in soft-sediment macrobenthic assemblages invaded by Caulerpa taxifolia compared to uninvaded habitats. Mar. Ecol. Prog. Ser. 380: 59-71.
http://dx.doi.org/10.3354/meps07926

Pacciardi, L., De Biasi A.M., Piazzi L. 2011. Effects of Caulerpa racemosa invasion on soft-bottom assemblages in the Western Mediterranean Sea. Biol. Inv. 13: 2677-2690.
http://dx.doi.org/10.1007/s10530-011-9938-5

Patzner R. 1998. The invasion of Lophocladia (Rhodomelaceae, Lophotaliae) at the northern coast of Ibiza (Western Mediterranean Sea). Boll. Soc. Hist. Nat. Balears 41: 75-80.

Piazzi L., Ceccherelli G., Cinelli F. 2001. Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Mar. Ecol. Progr. Ser. 210: 149-159.
http://dx.doi.org/10.3354/meps210149

Poore A.G.B., Hill N.A., Sotka E.E. 2008. Phylogenetic and geographic variation in host breadth and composition by herbivorous amphipods in the family Ampithoidae. Evolution 62: 21-38.

Ribera M.A., Boudouresque C.F. 1995. Introduced marine plants, with special reference to macroalgae: mechanisms and impact. Progr. Phycol. Res. 11: 187-268.

Russo A.R. 1990. The role of seaweed complexity in structuring Hawaiian epiphytal amphipod communities. Hydrobiologia 194: 1-12.
http://dx.doi.org/10.1007/BF00012107

Sales M., Ballesteros E. 2009. Shallow Cystoseira (Fucales: Ochrophyta) assemblages thriving in sheltered areas from Menorca (NW Mediterranean): relationships with environmental factors and anthropogenic pressures. Estuar. Coast. Shelf Sci. 84: 476-482.
http://dx.doi.org/10.1016/j.ecss.2009.07.013

Sales M., Ballesteros E. 2010. Long-term comparison of algal assemblages dominated by Cystoseira crinita (Fucales, Heterokontophyta) from Cap Corse (Corsica, North Western Mediterranean). Eur. J. Phycol. 45: 404-412.
http://dx.doi.org/10.1080/09670262.2010.498585

Sales M., Ballesteros E. 2012. Seasonal dynamics and annual production of Cystoseira crinita (Fucales: Ochrophyta)-dominated assemblages from the northwestern Mediterranean. Sci. Mar. 76: 403-408.
http://dx.doi.org/10.3989/scimar.03465.16D

Schaffelke B., Hewitt C.L. 2007. Impact of introduced seaweeds. Bot. Mar. 50: 397-417.
http://dx.doi.org/10.1515/BOT.2007.044

Sureda A., Box A., Terrados J., et al. 2008. Antioxidant response of the seagrass Posidonia oceanica when epiphytized by the invasive macroalga Lophocladia lallemandii. Mar. Environ. Res. 66: 359-363.
http://dx.doi.org/10.1016/j.marenvres.2008.05.009

Tanaka M.O., Leite F.P.P. 2003 Spatial scaling in the distribution of macrofauna associated with Sargassum stenophyllum (Mertens) Martius: analyses of faunal groups, gammarid life habits, and assemblage structure. J. Exp. Mar. Biol. Ecol. 293: 1-22.
http://dx.doi.org/10.1016/S0022-0981(03)00233-8

Taylor R.B. 1998. Seasonal variation in assemblages of mobile epifauna inhabiting three subtidal brown seaweeds in northeastern New Zealand. Hydrobiologia 361: 25-35.
http://dx.doi.org/10.1023/A:1003182523274

Taylor R.B., Cole R.G. 1994. Mobile epifauna on subtidal brown seaweeds in northeastern New Zealand. Mar. Ecol. Progr. Ser. 115: 271-282.
http://dx.doi.org/10.3354/meps115271

Teixeira H., Neto M.J., Patricio J., et al. 2009. Quality assessment of benthic macroinvertebrates under the scope of WFD using BAT, the Benthic Assessment Tool. Mar. Pollut. Bull. 58: 1477-1486.
http://dx.doi.org/10.1016/j.marpolbul.2009.06.006

Underwood A.J. 1997. Experiments in ecology. Their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge.

Vázquez-Luis M., Sanchez-Jerez P., Bayle-Sempere J.T. 2009. Comparison between amphipod assemblages associated with Caulerpa racemosa var. cylindracea and those of other Mediterranean habitats on soft substrate. Estuar. Coast. Shelf Sci. 84: 161-170.
http://dx.doi.org/10.1016/j.ecss.2009.04.016

Viejo R.M. 1999. Mobile epifauna inhabiting the invasive Sargassum muticum and two local seaweeds on northern Spain. Aquat. Bot. 64: 131-149.
http://dx.doi.org/10.1016/S0304-3770(99)00011-X

Wikström S.A., Kautsky L. 2007. Structure and diversity of invertebrate communities in the presence and absence of canopy-forming Fucus vesiculosus in the Baltic Sea. Estuar. Coast. Shelf Sci. 72: 168-176.
http://dx.doi.org/10.1016/j.ecss.2006.10.009

Zuljevic A., Nikolic V. 2008. The highly invasive alga Caulerpa racemosa var. cylindracea poses a new threat to the banks of the coral Cladocora caespitosa in the Adriatic Sea. Coral Reefs, 27: 441.
http://dx.doi.org/10.1007/s00338-008-0358-7