INTRODUCTIONTop

In the 19th century the ctenostome bryozoan Zoobotryon verticillatum (Delle Chiaje, 1822) was often misidentified as a macroalga and was reported under different names (Ulva intricata Clemente, Valonia intricata Agardh, Ascothamnion intricatum Kützing, Ascothamnion trinitatis Sonder) from different world regions: Cadiz (Spain, near the Gibraltar Strait, the first known record for this species; De Roxas Clemente 1807De Roxas Clemente R.S. 1807. Ensayo sobre las variedades de la vid comun que vegetan en Andalucía, con un índice etimológico y tres listas de plantas en que se caracterizan varias especies nuevas, por Don Simon de Roxas Clemente y Rubio. pp. [i]-xviii + [1]-324, 1 pl. Madrid (Imp. de Villalpando).), Malaga and Algiers (Mediterranean Sea), the Red Sea, the Antilles and Trinidad (Atlantic Ocean), Mauritius (Indian Ocean) and Mariana Island (Pacific Ocean; Agardh 1823Agardh C.A. 1823. Species algarum rite cognitae, cum synonymis, differentiis specificis et descriptionibus succinctis. Volumen primum pars posterior. pp. [vii-viii], [399]-531. Lundae [Lund]: ex officina Berlingiana., Kützing 1843Kützing F.T. 1849. Species algarum. F.A. Brockhaus, Leipzig, 922 pp., Durieu de Maisonneuve 1848Durieu de Maisonneuve M.C. 1848. Exploration scientifique de l’Algérie. Botany 1(10): 361-400., Zanardini 1858Zanardini G. 1858. Plantarum in mari rubro hucusque collectarum. Reale Istituto veneto, Venezia, 309 pp., Reichert 1870Reichert K.B. 1870. Vergleichende anatomische untersuchungen über Zoobotryon pellucidus (Ehrenberg). Buchdruckerei der königlichen Akademie der Wissenschaften zu Berlin, F. Dümmler, Berlin, 338 pp.). The first descriptions as an animal species occurred in Naples, Italy under the name Hydra verticillata Delle Chiaje, 1822, and later in Alexandria (Egypt, Mediterranean Sea) and the Red Sea under the name Zoobotryon pellucidus Ehrenberg, 1829. After a recent nomenclatural revision of ctenostome bryozoans (Waeschenbach et al. 2015Waeschenbach A., Vieira L.M., Reverter-Gil O., et al. 2015. A phylogeny of Vesiculariidae (Bryozoa, Ctenostomata) supports synonymisation of three genera and reveals possible cryptic diversity. Zool. Scripta, in press.), the genus Zoobotryon was concluded to be a junior subjective synonym of Amathia, and the name Z. verticillatum was changed to Amathia verticillata (Delle Chiaje, 1822) comb. n., which has now to be intended as its valid name.

It is because of those widespread early records that its occurrence within the Mediterranean has led to the presumption that this species is native to this region. It is currently known from tropical to subtropical localities in the Atlantic and Indo-Pacific region, and recently it has expanded its range within Macaronesia (Amat and Tempera 2009Amat J.N., Tempera F. 2009. Zoobotryon verticillatum Delle Chiaje, 1822 (Bryozoa), a new occurrence in the archipelago of the Azores (North-Eastern Atlantic). Mar. Pollut. Bull. 58(5): 761-764., Wirtz and Canning-Clode 2009Wirtz P., Canning-Clode J. 2009. The invasive bryozoan Zoobotryon verticillatum has arrived at Madeira Island. Aq. Inv. 4: 669-670., Minchin 2012Minchin D. 2012. Rapid assessment of the bryozoan, Zoobotryon verticillatum (Delle Chiaje, 1822) in marinas, Canary Islands. Mar. Pollut. Bull. 64(10): 2146-2150.). Such a cosmopolitan distribution has posed questions as to its real native origin: Winston (1995)Winston J.E. 1995. Ectoproct diversity of the Indian River coastal lagoon. Bull. Mar. Sci. 57: 84-89. suggested an origin from the Caribbean region, whilst Floerl et al. (2009a)Floerl O., Inglis G.J., Gordon D.P. 2009a. Patterns of taxonomic diversity and relatedness among native and non-indigenous bryozoans. Divers. Distrib. 15: 438-449. labelled it as being cryptogenic and Vieira et al. (2014)Vieira L.M., Migotto A.E., Winston J.E. 2014. Ctenostomatous Bryozoa from São Paulo, Brazil, with descriptions of twelve new species. Zootaxa 3889(4): 485-524. suggested that, since a wide range of habitats are occupied, A. verticillata may contain cryptic species. In a recent account, Galil and Gevili (2014)Galil B.S., Gevili R. 2014. Zoobotryon verticillatum (Bryozoa: Ctenostomatida: Vesiculariidae), a new occurrence on the Mediterranean coast of Israel. Mar. Biodivers. Rec. 7: e17. suggested that it had properties and a history unlikely to have originated within the Mediterranean Sea because of its occurrence mainly on artificial habitats in harbours. It is now believed to be native to the Caribbean Sea, where it inhabits natural habitats such as sea-grass meadows, mangroves, oyster reefs and rocky shores and has apparently co-evolved with the goniodorid nudibranch Okenia zoobotryon (Smallwood, 1910), known to live, feed and reproduce exclusively on A. verticillata (Galil and Gevili 2014Galil B.S., Gevili R. 2014. Zoobotryon verticillatum (Bryozoa: Ctenostomatida: Vesiculariidae), a new occurrence on the Mediterranean coast of Israel. Mar. Biodivers. Rec. 7: e17.). This bryozoan subsequently became introduced elsewhere, including Macaronesia and the Mediterranean Sea (Wirtz and Canning-Clode 2009Wirtz P., Canning-Clode J. 2009. The invasive bryozoan Zoobotryon verticillatum has arrived at Madeira Island. Aq. Inv. 4: 669-670., Galil and Gevili 2014Galil B.S., Gevili R. 2014. Zoobotryon verticillatum (Bryozoa: Ctenostomatida: Vesiculariidae), a new occurrence on the Mediterranean coast of Israel. Mar. Biodivers. Rec. 7: e17.). Therefore, its status should now be considered to be pseudo-indigenous in the Mediterranean Sea (Ferrario et al. 2014Ferrario J., Marchini A., Lodola A., et al. 2014. The pseudoindigenous bryozoan Zoobotryon verticillatum along the Mediterranean and Atlantic European coasts. Biol. Mar. Mediterr. 21(1): 117-118.), i.e. a non-indigenous species (NIS) having long been perceived to be native (Carlton 2009Carlton J.T. 2009. Deep invasion ecology and the assembly of communities in historical time. In: Rilov G., Crooks J.A. (eds), Biological Invasions in Marine Ecosystems. Ecological Studies 204, Springer-Verlag Berlin Heidelberg, pp. 13-56.).

Amathia verticillata has been recorded mainly from enclosed habitats, such as coastal lagoons and embayments or their artificial equivalents, harbours and marinas. For example, in France A. verticillata was previously recorded in Menton (Joliet 1888Joliet L. 1888. Bryozoaries nouveaux de Roscoff et Bryozoaries de Menton. Arch. Zool. Exp. Gén. 2(6): 103-109.), Marseille Harbour (Gautier 1962Gautier Y.V. 1962. Recherches écologiques sur les Bryozoaires Chilostomes en Méditerranée Occidentale. Re. Trav. St. Mar. Endoume 38(24): 1-434.) and Martigues Harbour (Chimenz et al. 1981Chimenz C., Fresi E., Cinelli F., et al. 1981. Ricerche sui popolamenti bentonici di substrato dure del porto d’Ischia. Briozoi. Mem. Biol. Mar. Oceanogr. 6(4): 187-206.). In particular, its stolons are capable of attaching to different substrates, including smooth surfaces, and it can develop colonies by a process of budding. Colonies vary greatly in shape and size, being either elongated and hanging up to 2 m in length (Minchin 2012Minchin D. 2012. Rapid assessment of the bryozoan, Zoobotryon verticillatum (Delle Chiaje, 1822) in marinas, Canary Islands. Mar. Pollut. Bull. 64(10): 2146-2150.) or shorter and bushy (Zirpolo 1933Zirpolo G. 1933. Zoobotryon verticillatum (Delle Chiaje). Mem. Pont. Acc. Sci., Nuovi Lincei, Roma 17: 190-441.), and sometimes reaching a high biomass (Lenzi et al. 2009Lenzi M., Birardi F., Boddi S., et al. 2009. The lagoon of Orbetello. In: Cecere E., Petrocelli A., Izzo G. (eds), Flora and Vegetation of the Italian Transitional Water Systems. Lagunet, CORILA, Venice, pp. 111-123.).

Due to its outstanding spreading capability, A. verticillata can have ecological and economic impacts (Gossett et al. 2004Gosset L., Lester J., Gonzales L. 2004. Galveston Bay Invasive Species Risk Assessment - Final Report. Galveston Bay Estuary Program, Texas Commission on Environmental Quality, Texas, 57 pp.). It can form extensive fouling in harbours and marinas, on vessels and on fishing gear, and it has been known to clog the intake of abstraction pipework (Ryland 1965Ryland J.S. 1965. Catalogue of main fouling organisms (found on ships coming into European waters). Volume 2: Polyzoa. OECD, 84 pp.). Moreover, this effective suspension feeder can remove large volumes of planktonic material, affecting food web dynamics (Amat and Tempera 2009Amat J.N., Tempera F. 2009. Zoobotryon verticillatum Delle Chiaje, 1822 (Bryozoa), a new occurrence in the archipelago of the Azores (North-Eastern Atlantic). Mar. Pollut. Bull. 58(5): 761-764.). It has also been listed on the Global Invasive Species database as an impacting species (www.issg.org, Accessed Jan 17, 2015). Specifically, this bryozoan species causes extensive fouling on Zostera spp. in summer, contributing to its decline (Williams 2007Williams S.L. 2007. Introduced species in seagrass ecosystems: status and concerns. J. Exp. Mar. Biol. Ecol. 350(1): 89-110.). In the Galveston Bay (Texas, USA), A. verticillata was listed as having the highest ecological risk score and least feasibility for control and/or eradication (Gosset et al. 2004Gosset L., Lester J., Gonzales L. 2004. Galveston Bay Invasive Species Risk Assessment - Final Report. Galveston Bay Estuary Program, Texas Commission on Environmental Quality, Texas, 57 pp.). Although its soft colonies can be easily detached from hulls by mechanical removal, stolons are likely to persist and regenerate new colonies, whilst viable fragments dislodged during manual removal may survive and subsequently reattach once the environmental conditions become favourable (Hopkins and Forrest 2008Hopkins G.A., Forrest B.M. 2008. Management options for vessel hull fouling: an overview of risks posed by in-water cleaning. ICES J. Marine Sci. 65(5): 811-815.).

This NIS should receive attention within the Mediterranean Sea as being a nuisance species, as has been suggested elsewhere (Coleman 1999Coleman F.S. 1999. Note on Zoobotryon verticillatum (Bryozoa) in a solar saltfield. Int. J. Salt Lake Res. 8(1): 71-74., Farrapeira 2011Farrapeira C.M.R. 2011. The introduction of the bryozoan Zoobotryon verticillatum (Delle Chiaje, 1822) in northeast of Brazil: a cause for concern. Biol. Invasions 13(1): 13-16., Minchin 2012Minchin D. 2012. Rapid assessment of the bryozoa, Nagy 2013Nagy L. 2013. Early detection and rapid response. Managers Tool Kit. (Accessed Jan 26, 2015) ). In particular, following the requirements of the European Marine Strategy Directive (EC 2008EC [European Commission] 2008. Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). Official Journal of the European Union L 164: 19-40.), its “trends in abundance, temporal occurrence and spatial distribution in the wild [...] notably in high risk areas, in relation to the main vectors and pathways of spreading” should be assessed (MSFD Descriptor 2, Criterion 2.1, Indicator 2.1.1; see also Ojaveer et al. 2014Ojaveer H., Galil B.S., Minchin D., et al. 2014. Ten recommendations for advancing the assessment and management of non-indigenous species in marine ecosystems. Mar. Policy 44: 160-165.).

Unfortunately, due to its status of being a pseudo-indigenous species, A. verticillata has so far received little attention from Mediterranean researchers. Here, we present an updated account on the currently known distribution of A. verticillata in the Mediterranean Sea and NE Atlantic region. We also apply a rapid-assessment method to quantify the relative abundance of A. verticillata within La Grande Motte marina on the Mediterranean coast of France, a method which is easily replicable elsewhere. Furthermore, we describe some associated fauna new to the French coast associated with this bryozoan.

MATERIALS AND METHODSTop

La Grande Motte (Fig. 1) is a popular seaside resort and port, built in the 1960s-1970s in the region of Languedoc-Roussillon near the town of Montpellier (Southern France), located between the “Étang de l’or” lagoon and the Mediterranean Sea. It hosts a large marina providing 1374 berths. Many of the berthed recreational vessels have different registration ports ranging from the western Atlantic to the Indo-Pacific, and also including several regions within the Mediterranean Sea and Northern Europe.

The floating pontoons supporting a boardwalk in La Grande Motte marina (43°33’19.16”N, 4°04’53.78”E; Fig. 1) were sampled on 19 November 2014 using a rapid sampling method which was undertaken within a two-hour period. A single boardwalk was examined near to the sea entrance of the marina which is protected by a breakwater. The floating units, pontoons, each approximately 1 m in length, supported a boardwalk of 220 m in overall length. A sample of 30 pontoons were examined at spaced distances along each open pontoon side.

The abundance and distribution range (ADR) used in this study was based on the method within the bio-pollution assessment method of Olenin et al. (2007)Olenin S., Minchin D., Daunys D. 2007. Assessment of biopollution in aquatic ecosystems. Mar. Pollut. Bull. 55(7): 379-394., the method recommended for biological surveys elsewhere for port regions (Awad et al. 2014Awad A., Haag F., Anil A.C., et al. 2014. Guidance on port biological baseline surveys. GEF-UNDP-IMO GloBallast Partnerships, London, UK. GloBallast Monograph 22: 48 pp.). The size of the assessment unit, used in this case, was a single boardwalk within the marina for the period November 2014. This assessment is based on the abundance and frequency of A. verticillata colonies occurring on each individual pontoon supporting a single boardwalk. Abundance was considered ‘low’ with fewer than ten colonies per pontoon, ‘moderate’ with 10-50 colonies per pontoon and ‘high’ with more than 50 colonies per pontoon. The distribution scales for each assessment unit ranged from ‘local’, if present on one pontoon, ‘several localities’ if present in fewer than half the pontoons examined, ‘many localities’ if present on more than half of the pontoons, and ‘all localities’ if present on all the pontoons. Combinations of abundance and distribution provide a scale that ranges from ‘A’, few colonies present on one pontoon, to ‘E’, high numbers on all pontoons (Table 1). From the abundance of colonies on pontoons, an estimate of the total numbers beneath the boardwalk was possible. Additional observations were also made on the narrow gap sections between pontoon units.

The presence/absence of colonies attached to the hulls of berthed leisure craft was based on what could be observed from the boardwalk on the forward or stern sections of the craft, according to how these were berthed. From this a prevalence of A. verticillata was obtained.

Some colonies were selected from the pontoons and other structures associated with the marina such as ladders, fenders and submerged ropes, for examination of the biota associated with A. verticillata colonies. Samples were preserved in 4%-5% solution of formaldehyde in seawater and further submitted to taxonomic identification.

The distribution of A. verticillata from different countries and sea sectors within the Mediterranean Sea basin and NE Atlantic, including Macaronesia, were obtained from the literature and personal observations and communications.

RESULTSTop

The immersed sides of the pontoons were extensively populated with colonies of A. verticillata (Fig. 2A) with a prevalence of 96% and an estimated intensity of between >10 and <50 colonies per pontoon, providing an overall conservative estimate of colony numbers of >10000 beneath a single boardwalk (Fig. 3). Colonies on each pontoon ranged from none, for a short distance along a semi-exposed part of the boardwalk, to more than 50 colonies along a single pontoon side. Colonies were clearly recognized when they had attained a size of 2 cm or greater, and some extended to more than 20 cm in colony height at the time of the study. Colonies were present on more than half of the examined pontoons, which represented an occurrence at ‘many localities’, at a ‘moderate’ level of abundance to provide an ADR of ‘C’. A total of 114 berthed craft were visually examined and, of these, 35 were fouled with one or more A. verticillata colonies associated with their hulls to give a 31% prevalence. On many hulls the only fouling organism noted was A. verticillata (Fig. 2B), and on some boat hulls these were abundant. Although we did not perform estimates on the level of fouling on single boats, we could note from the boardwalk that fouling was greater on craft that did not appear to have been used recently and had “for sale” signs.

Colonies were attached to the sides, undersides and surfaces within the gaps between adjacent pontoons beneath the boardwalk; but were not present close to the surface water interface, where colonies of serpulids formed a distinctive horizon made up of Hydroides norvegicus Gunnerus, 1768, Spirobranchus lamarcki (Quatrefages, 1866), Janua sp. and the NIS Hydroides elegans (Haswell, 1883). Other prominent species of the fouling community included Bugula neritina (Linnaeus, 1758), Mytilus galloprovincialis Lamarck, 1819, and the cirripedes Amphibalanus amphitrite (Darwin, 1854) and the NIS Amphibalanus eburneus (Gould, 1841). The non-indigenous tunicate Styela plicata (Lesueur, 1823) was present on both pontoons and boat hulls. Elsewhere within the marina in the inner basin, other colonies of A. verticillata were present, suggesting that this bryozoan is extensively distributed throughout the marina.

Within the more sheltered conditions, diatomous films and sediment caused a dark green colouration on A. verticillata colonies, whereas in the more exposed conditions along the boardwalk these colonies were translucent. A. verticillata colonies sampled from both pontoons and boat hulls in the marina, especially those darker in colour, hosted a rich assemblage of small benthic species (polychaetes, nudibranchs, decapod and peracarid crustaceans, pycnogonids and ophiurids). Noteworthy was the presence of three non-indigenous peracarid species: the isopods Paracerceis sculpta (Holmes, 1904) (only one male specimen) and Paranthura japonica Richardson, 1909 (moderate abundance), and the caprellid amphipod Caprella scaura Templeton, 1836, which is the dominant species amongst the crustacean assemblage (Fig. 4 A-D).

Figure 5 shows the currently known distribution of A. verticillata in the Mediterranean Sea and NE Atlantic coasts, obtained from published and unpublished records. Most of these records were from the western Mediterranean (52%). For 18 records (Table 2), there was no information on the habitat where A. verticillata was found. Excluding those, in 64% of the records A. verticillata was found on man-made substrates in harbours and marinas, in 9% in lagoons and in 27% in natural habitats.

With only a few exceptions, the available records of A. verticillata in the Mediterranean Sea are limited to presence data. Because data on its distribution and temporal occurrence are widely scattered over two centuries, quantitative data on its abundance are almost completely absent (Table 2).

DISCUSSIONTop

In many aquatic environments throughout the world, the development of recreational berthing facilities has provided novel habitats for a wide range of species with a sessile life history stage and also for their associates (Clarke-Murray et al. 2014Clarke-Murray C., Gartner H., Gregr E.J., et al. 2014. Spatial distribution of marine invasive species: environmental, demographic and vector drivers. Divers. Distrib. 20: 824-836.). These species may become distributed over a wide region, even across oceans (Minchin 2006Minchin D. 2006. The transport and the spread of living aquatic species. In: Davenport J., Davenport J.L. (eds), The ecology of transportation: managing mobility for the environment. Springer, Berlin Heidelberg New York, pp. 77-97.). This may be the case of A. verticillata, which has biological traits that explain the success in its spread. In particular, its larvae and fragments can easily settle on a variety of natural and artificial substrates, including smooth and clean surfaces (Zirpolo 1933Zirpolo G. 1933. Zoobotryon verticillatum (Delle Chiaje). Mem. Pont. Acc. Sci., Nuovi Lincei, Roma 17: 190-441., Robinson 2004Robinson N.M. 2004. Interactions between the nudibranch Okenia zoobotryon and its bryozoan prey Zoobotryon verticillatum. Thesis, Master of Sciences. Univ. Central Florida, Orlando, Florida, 67 pp.). Additionally, the basal stolon can resist low temperatures and strong currents (Zirpolo 1933Zirpolo G. 1933. Zoobotryon verticillatum (Delle Chiaje). Mem. Pont. Acc. Sci., Nuovi Lincei, Roma 17: 190-441.), making this bryozoan well suited as a hull-fouling species. Moreover, A. verticillata produces active compounds (bromo-alkaloids), which probably provide protection by discouraging predation (e.g. Ortega et al. 1993Ortega M.J., Zubia E., Salva J. 1993. A new brominated indole-3-carbaldehyde from the marine bryozoan Zoobotryon verticillatum. J. Nat. Prod. 56(4): 633-636.).

The preponderance of records of A. verticillata from marinas worldwide (Ryland 1965Ryland J.S. 1965. Catalogue of main fouling organisms (found on ships coming into European waters). Volume 2: Polyzoa. OECD, 84 pp., Ganapathi and Satyanarayana Rao 1968Ganapathi P.N., Satyanarayana Rao K. 1968. Fouling bryozoans in Visakhapatnam Harbour. Curr. Sci. 37: 81-89., Ardizzone and Riggio 1981Ardizzone G., Riggio S. 1981. Similitudine e diversitá nelle biocenosi bentoniche del Porto di Palermo in relazione al substrato di insediamento. Quad. Lab. tecnol. pesca 3(1): 587-603., Gordon and Mawatari 1992Gordon D.P., Mawatari S.F. 1992. Atlas of marine-fouling Bryozoa of New Zealand ports and harbours. Misc. Publ. N. Z. Oceanogr. Inst. 107: 1-52., Hewitt et al. 2004Hewitt C.L., Campbell M.L., Thresher R.E., et al. 2004. Introduced and cryptogenic species in Port Phillip Bay, Victoria, Australia. Mar. Biol. 144(1): 183-202., Ramadan et al. 2006Ramadan S.E., Kheirallah A.M., Abdel-Salam K.M. 2006. Marine fouling community in the Eastern harbour of Alexandria, Egypt compared with four decades of previous studies. Mediterr. Mar. Sci. 7(2): 19-30., Abdel-Salam and Ramadan 2008Abdel-Salam K.H.M., Ramadan S.H.E. 2008. Fouling bryozoa from some Alexandria harbours, Egypt. (I) erect species. Mediterr. Mar. Sci. 9(2): 5-20., Carlton and Eldredge 2009Carlton J.T., Eldredge L.G. 2009. The introduced and cryptogenic marine and estuarine animals and plants of the Hawaiian Archipelago. Bishop Mus. Bull. Cultur. Environ. Stud. 4: 1-203., Wirtz and Canning-Clode 2009Wirtz P., Canning-Clode J. 2009. The invasive bryozoan Zoobotryon verticillatum has arrived at Madeira Island. Aq. Inv. 4: 669-670., Farrapeira 2011Farrapeira C.M.R. 2011. The introduction of the bryozoan Zoobotryon verticillatum (Delle Chiaje, 1822) in northeast of Brazil: a cause for concern. Biol. Invasions 13(1): 13-16., Minchin 2012Minchin D. 2012. Rapid assessment of the bryozoan, Zoobotryon verticillatum (Delle Chiaje, 1822) in marinas, Canary Islands. Mar. Pollut. Bull. 64(10): 2146-2150., Galil and Gevili 2014Galil B.S., Gevili R. 2014. Zoobotryon verticillatum (Bryozoa: Ctenostomatida: Vesiculariidae), a new occurrence on the Mediterranean coast of Israel. Mar. Biodivers. Rec. 7: e17., Tamsouri et al. 2014Tamsouri N., Carmona L., Moukrim A., et al. 2014. Polycerella emertoni and Favorinus ghanensis: two new alien sea slug molluscs from the Moroccan Atlantic coasts. Mar. Biodivers. Rec. 7: e13.) suggests that recreational craft may be involved in its spread. The arrival of A. verticillata to the NE Atlantic and Mediterranean Sea from the Caribbean region can only have been as ship hull fouling, as ballast water transmissions will not have taken place until more than 50 years after the time it was first described as an alga in Cadiz (Spain) and later as an animal in Naples (Italy). Even in modern times, the likelihood of transport by ballast water is low, since A. verticillata larvae remain only a few hours in the plankton (Zirpolo 1933Zirpolo G. 1933. Zoobotryon verticillatum (Delle Chiaje). Mem. Pont. Acc. Sci., Nuovi Lincei, Roma 17: 190-441.). A. verticillata produces vegetative fragments from a colony that can survive and attach to new substrates (Robinson 2004Robinson N.M. 2004. Interactions between the nudibranch Okenia zoobotryon and its bryozoan prey Zoobotryon verticillatum. Thesis, Master of Sciences. Univ. Central Florida, Orlando, Florida, 67 pp.). Although we cannot rule out the possibility that drifting fragments could survive in ballast waters, the transport of stolons, or full colonies, attached on vessel hulls provides a convincing hypothesis. Other transport mechanisms such as rafting on flotsam and drifting algae (Watts et al. 1998Watts P.C., Thorpe J.P., Taylor P.D. 1998. Natural and anthropogenic dispersal mechanisms in the marine environment: a study using cheilostome Bryozoa. Philos. Trans. R. Soc. Lond. B. 353: 453-464., Barnes 2002Barnes D.K.A. 2002. Invasions by marine life on plastic debris. Nature 416: 808-809.) may also increase the geographic range of bryozoan species. No such rafting was noted in the area of study.

The rapid-assessment method involving two workers was, within a two-hour period, sufficient to locate at least 7 NIS and undertake an ADR of A. verticillata in such a way that any significant change in abundance is likely to be measured during a re-visit. For a species such as this bryozoan, the method may even be suitable for measuring seasonal changes, especially if there is a winter decline. The ADR approach for a conspicuous species is effective when used on marinas, provided the same scoring system is used.

The occurrence of luxuriant colonies in November is noteworthy. Colonies are reported as occurring only during summer months in the Mediterranean Sea (Relini 1966Relini G. 1966. Le comunità dominanti nel ‘fouling’ portuale di Genova. Natura 57: 136-156., Galil and Gevili 2014Galil B.S., Gevili R. 2014. Zoobotryon verticillatum (Bryozoa: Ctenostomatida: Vesiculariidae), a new occurrence on the Mediterranean coast of Israel. Mar. Biodivers. Rec. 7: e17.), and they enter a senescent phase during the autumn (Zirpolo 1933Zirpolo G. 1933. Zoobotryon verticillatum (Delle Chiaje). Mem. Pont. Acc. Sci., Nuovi Lincei, Roma 17: 190-441.). Along sheltered coasts A. verticillata has the ability to form overwintering stages from which new colonies can evolve (Geiger and Zimmer 2002Geiger D.L., Zimmer R.L. 2002. Anchoring rootlets in Bowerbankia imbricata (Bryozoa: Ctenostomata). Bull. Mar. Sci. 70 (3): 791-797.) when temperatures become favourable. Therefore, an enclosed environment such as a Mediterranean marina could act as a suitable habitat during the winter. A eurytopic and euryecious species such as A. verticillata (Vieira et al. 2014Vieira L.M., Migotto A.E., Winston J.E. 2014. Ctenostomatous Bryozoa from São Paulo, Brazil, with descriptions of twelve new species. Zootaxa 3889(4): 485-524.) can endure the conditions within a marina on the south coast of France, where winter temperatures may descend to 11°C-14°C (http://www.surf-forecast.com/breaks/La-Grande-Motte/seatemp, accessed Jan 17, 2015).

A conservative estimate of the number of colonies of A. verticillata at La Grande Motte marina exceeded 10000 colonies. Colonies less than 2 cm in height were not easily distinguished along the pontoon sides, so the overall numbers of colonies are likely to have been greater than estimated. In addition, colonies that were abundant within the small gaps between adjacent pontoons and those attached to boat hulls and other structures were not scored. Overall, within this marina featuring ten boardwalks (Fig. 1) the numbers might have exceeded 100000 colonies. Such a sheltered environment provides suitable summer temperatures for reproduction and growth, suitable salinities and organic enrichment. Indeed, marinas provide extensive surfaces for sessile biota many times greater than would otherwise occur naturally (Minchin et al. 2006Minchin D. 2006. The transport and the spread of living aquatic species. In: Davenport J., Davenport J.L. (eds), The ecology of transportation: managing mobility for the environment. Springer, Berlin Heidelberg New York, pp. 77-97.). Moreover, the small tidal range in the Mediterranean involves a high retention of water, which makes the contention of propagules likely and explains the abundance on many different structures. Since the pelagic phase of the larvae is of the order of hours, retention of settling individuals is high (Zirpolo 1933Zirpolo G. 1933. Zoobotryon verticillatum (Delle Chiaje). Mem. Pont. Acc. Sci., Nuovi Lincei, Roma 17: 190-441.). Clearly, the abundance of the colonies of A. verticillata in La Grande Motte marina is sufficient to provide enough propagules to infest boat hulls. Recruitment onto boat hulls is extensive: some had little macrobiofouling, whereas others had a greater diversity of biofouling taxa. The numerous large colonies observed in La Grande Motte might also generate drifting fragments that could become established in surrounding natural habitats. The occurrence of the species on natural substrata has been observed in the Azores (Amat and Tempera 2009Amat J.N., Tempera F. 2009. Zoobotryon verticillatum Delle Chiaje, 1822 (Bryozoa), a new occurrence in the archipelago of the Azores (North-Eastern Atlantic). Mar. Pollut. Bull. 58(5): 761-764.), Italy (Riolo 2009Riolo F. 2009. Valutazione e monitoraggio della presenza e stato di salute dei coralli madreporari (scleractinia) nell’Area Marina Protetta Capo Rizzuto (anno 2009). Technical report, Capo Rizzuto MPA, Italy, 19 pp. Available at: http://www.riservamarinacaporizzuto.it/dati/upload/files/RELAZIONE_MONITORAGGIO_CORALLI%281%29.pdf. ) and Israel (Lipkin and Safriel 1971Lipkin Y., Safriel U. 1971. Intertidal zonation on rocky shores at Mikhmoret (Mediterranean, Israel). J. Ecol. 59: 1-30.).

As reported by other authors (Farrapeira 2011Farrapeira C.M.R. 2011. The introduction of the bryozoan Zoobotryon verticillatum (Delle Chiaje, 1822) in northeast of Brazil: a cause for concern. Biol. Invasions 13(1): 13-16., Ferrario et al. 2014Ferrario J., Marchini A., Lodola A., et al. 2014. The pseudoindigenous bryozoan Zoobotryon verticillatum along the Mediterranean and Atlantic European coasts. Biol. Mar. Mediterr. 21(1): 117-118.) and in this study, A. verticillata has a varied associated fauna, mainly other bryozoans, nudibranchs, amphipods and isopods. Their presence indicates that A. verticillata may act as a special niche for smaller NIS, thereby enhancing opportunities for their spread on vessel hulls. In this study A. verticillata acted as a substrate for three non-indigenous crustaceans, representing the first records from the Mediterranean coast of France: Paracerceis sculpta, Paranthura japonica and Caprella scaura.

The NE Pacific isopod Paracerceis sculpta was first reported from Tunisia in 1978, and subsequently from Italy, Spain (Gibraltar Strait) and Greece (Fryganiotis and Chintoroglou 2014Fryganiotis K., Chintoroglou Ch. 2014. First record of the isopod Paracerceis sculpta in the Aegean Sea: established populations in north Aegean marinas. In: Katsanevakis S., Acar Ü., Ammar I., et al., New Mediterranean Biodiversity Records (October, 2014). Mediterr. Mar. Sci. 15: 667-687.). Its occurrence in areas of shellfish farming as well as marinas indicate that it is polyvectic.

The NW Pacific isopod Paranthura japonica is again a likely pseudo-indigenous species, most probably introduced since the 1970s with shellfish transfers, but it has not previously been perceived to be an NIS as a result of earlier misidentifications (Marchini et al. 2014Marchini A., Sorbe J.-C., Torelli F., et al. 2014. The non-indigenous Paranthura japonica Richardson, 1909 in the Mediterranean Sea: travelling with shellfish? Mediterr. Mar. Sci. 15(3): 545-553.). It has been reported from the French Atlantic coast (Lavesque et al. 2013Lavesque N., Sorbe J.-C., Bachelet G., et al. 2013. Recent discovery of Paranthura japonica Richardson, 1909 (Crustacea: Isopoda: Paranthuridae) in European marine waters (Arcachon Bay, Bay of Biscay). BioInvasion Rec. 2(3): 215-219.), and the Italian Adriatic and Tyrrhenian coasts (Marchini et al. 2014Marchini A., Sorbe J.-C., Torelli F., et al. 2014. The non-indigenous Paranthura japonica Richardson, 1909 in the Mediterranean Sea: travelling with shellfish? Mediterr. Mar. Sci. 15(3): 545-553.). The current record indicates that this NIS, previously thought to be associated with aquaculture, might also be spread as hull fouling on leisure craft.

The Indo-Pacific amphipod Caprella scaura is one of the most widespread NIS in European marine waters (Galil et al. 2014Galil B.S., Marchini A., Occhipinti-Ambrogi A., et al. 2014. International arrivals: widespread bioinvasions in European Seas. Ethol. Ecol. Evol. 26: 152-171.). It was first reported from the Lagoon of Venice (Italy) in 1994, and then spread rapidly, being able to colonize lagoons, harbours and marinas in the Mediterranean Sea to include Macaronesia (Minchin 2012Minchin D. 2012. Rapid assessment of the bryozoan, Zoobotryon verticillatum (Delle Chiaje, 1822) in marinas, Canary Islands. Mar. Pollut. Bull. 64(10): 2146-2150., Ramalhosa et al. 2015Ramalhosa P., Canning-Clode J. 2015. The invasive caprellid Caprella scaura Templeton, 1836 (Crustacea: Amphipoda: Caprellidae) arrives on Madeira Island, Portugal. BioInvasion Rec. 4(2): 97-102.). Recent molecular evidence suggests that its spread will have involved multiple introduction events of several sub-species (Cabezas et al. 2014Cabezas M.P., Xavier R., Branco M., et al. 2014. Invasion history of Caprella scaura Templeton, 1836 (Amphipoda: Caprellidae) in the Iberian Peninsula: multiple introductions revealed by mitochondrial sequence data. Biol. Invasions 16(10): 1-25.). The present record of C. scaura in La Grande Motte represents the first record for continental France: the species was previously reported from the French island of Corsica (Ros et al. 2014Ros M., Guerra-García J.M., Navarro-Barranco C., et al. 2014. The spreading of the non-native caprellid (Crustacea: Amphipoda) Caprella scaura Templeton, 1836 into southern Europe and northern Africa: a complicated taxonomic history. Mediterr. Mar. Sci. 15: 145-155.).

The records from La Grande Motte (Fig. 3D), together with observations from the Mediterranean Sea and elsewhere, may have enabled the rapid spread of C. scaura, which has also been found firmly attached by means of its pereiopods to A. verticillata in other marinas in the Ligurian Sea (Jasmine Ferrario, personal observations), near Gibraltar (Guerra-García et al. 2011Guerra-García J.M., Ros M., Dugo-Cota A., et al. 2011. Geographical expansion of the invader Caprella scaura (Crustacea: Amphipoda: Caprellidae) to the East Atlantic coast. Mar. Biol. 158(11): 2617-2622.), on the Balearic Islands (Ros et al. 2013Ros M., Vázquez-Luis M., Guerra-García J.M. 2013. The tropical caprellid amphipod Paracaprella pusilla a new alien crustacean in the Mediterranean Sea. Helgoland Mar. Res. 67(4): 675-685.), on the Canary islands (Minchin 2012Minchin D. 2012. Rapid assessment of the bryozoan, Zoobotryon verticillatum (Delle Chiaje, 1822) in marinas, Canary Islands. Mar. Pollut. Bull. 64(10): 2146-2150.), on Madeira Island (Ramalhosa et al. 2015Ramalhosa P., Canning-Clode J. 2015. The invasive caprellid Caprella scaura Templeton, 1836 (Crustacea: Amphipoda: Caprellidae) arrives on Madeira Island, Portugal. BioInvasion Rec. 4(2): 97-102.), and in Hilary Marina, Australia (Dan Minchin, personal observation). The spaghetti bryozoan has also been shown to be a host for non-indigenous nudibranchs such as Polycera hedgpethi Er. Marcus, 1964 (in Sicily, Italy: Giacobbe and De Matteo 2013Giacobbe S., De Matteo S. 2013. The potentially invasive opisthobranch Polycera hedgpethi Er. Marcus, 1964 (Gastropoda Nudibranchia), introduced in a Mediterranean coastal lagoon. Biodiv. J. 4(2): 359-364.); Polycerella emertoni A. E. Verrill, 1880 (in Agadir, Tunisia: Tamsouri et al. 2014Tamsouri N., Carmona L., Moukrim A., et al. 2014. Polycerella emertoni and Favorinus ghanensis: two new alien sea slug molluscs from the Moroccan Atlantic coasts. Mar. Biodivers. Rec. 7: e13.); and Okenia spp. (Rudman 2004Rudman W.B. 2004. Further species of the opisthobranch genus Okenia (Nudibranchia: Goniodorididae) from the Indo-West Pacific. Zootaxa 695: 1-70., Carlton and Eldredge 2009Carlton J.T., Eldredge L.G. 2009. The introduced and cryptogenic marine and estuarine animals and plants of the Hawaiian Archipelago. Bishop Mus. Bull. Cultur. Environ. Stud. 4: 1-203., Ortea et al. 2009Ortea J., Moro L., Espinosa J. 2009. El género Okenia Menke, 1830 (Mollusca: Nudibranchia) en las islas Canarias con notas sobre Okenia zoobotryon (Smallwood, 1910), una especie en controversia permanente. Vieraea 37: 75-83.).

CONCLUSIONTop

It is very likely that marinas act as hubs for the dispersal of A. verticillata and its associates, particularly peracarids crustaceans and nudibranchs (O’Kelly and Miller 1994O’Kelly M.E., Miller H.J. 1994. The hub network design problem: a review and synthesis. J. Transp. Geogr. 2: 31-40., Carlton 1996Carlton J.T. 1996. Pattern, process, and prediction in marine invasion ecology. Biol. Conserv. 78: 97-106., Floerl et al. 2009bFloerl O., Inglis G.J., Dey K., et al. 2009b. The importance of transport hubs in stepping-stone invasions. J. Appl. Ecol. 46(1): 37-45.). The marina at La Grande Motte has a large number of berths with many visiting craft that have the capability of spreading these species to areas where they currently do not exist. This marina is recognized as serving many routes within the western Mediterranean Sea and with the continued development of marinas around the Mediterranean Sea (Cornell 2002Cornell J. 2002. World Cruising Routes. International Marine, McGraw Hill, London, 624 pp., Savini et al. 2006Savini D., Occhipinti-Ambrogi A., Minchin D., et al. 2006. A concealed aspect in coastal water conservation: the diffusion of alien species by recreational craft. Biol. Mar. Mediterr. 13(1): 764-772.) these species are likely to continue to expand. Because this NIS is able to regenerate from stolons as well as viable fragments, careful and conscientious hull maintenance routines are required. On account of the ability of A. verticillata to spread from fragments in water, hull-cleaning should be avoided. For this reason the boating industry must be made aware that there are NIS together with their associates, which require careful management to prevent their further spread.

ACKNOWLEDGEMENTSTop

This work was supported by the European Union’s Seventh Framework Programme for research, technological development and demonstration (FP7/2007-2013) within the Ocean of Tomorrow call under Grant Agreement No. 266445 for the project Vectors of Change in Oceans and Seas Marine Life, Impact on Economic Sectors (VECTORS); Jasmine Ferrario was supported by a PhD grant from the University of Pavia. The authors gratefully thank Armando Macali, Stefano Piraino and Xavier Turon for providing unpublished data and grey literature on A. verticillata distribution, and Anna Occhipinti for commenting on an earlier draft. We also thank two reviewers for their useful comments and literature suggestions.

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