The spaghetti bryozoan Amathia verticillata, formerly known as Zoobotryon verticillatum, was first described in 1822 from Naples, Italy, although this species was already present in 1807 at Cadiz, Spain. This ctenostome has long been considered a native species in the Mediterranean Sea but it has recently been suggested to be of Caribbean origin. It is most likely to have been introduced by vessels as hull fouling. This pseudo-indigenous species, i.e. a non-indigenous species (NIS) having been perceived to be native, has been found in several marinas and harbours within the Mediterranean Sea. In November 2014, this bryozoan species was abundant in the La Grande Motte marina on the south coast of France. Several thousand colonies were estimated to be present within this marina attached to the floating pontoon units that supported a floating boardwalk. Of the berthed craft examined, 31% were fouled with this species, and it was occasionally a prominent fouling species. Several macroinvertebrate species were associated with A. verticillata colonies, including some NIS, Paracerceis sculpta, Paranthura japonica and Caprella scaura, that are recorded for the first time from the Mediterranean coast of France. A. verticillata might support their transfer elsewhere by providing a habitat and substrate when attached to vessel hulls.
RESUMEN
El briozoo espagueti Amathia verticillata, anteriormente conocido como Zoobotryon verticillatum, fue descrito por primera vez en 1822 en Nápoles, Italia, aunque esta especie ya estaba presente en 1807 en Cádiz, España. Este ctenostomado ha sido considerado por mucho tiempo como una especie nativa del Mar Mediterráneo, pero se ha sugerido recientemente que es originario del Caribe. Es probable que haya sido introducido incrustado en los cascos de los barcos. Esta especie pseudoindígena, es decir, una especie introducida que ha sido percibida como nativa, se ha encontrado en varios puertos comerciales y deportivos del Mar Mediterráneo. En noviembre de 2014, esta especie de briozoo era abundante en el puerto deportivo de La Grande Motte en la costa sur de Francia. Se estimaron varios miles de colonias presentes en este puerto, adheridas a las unidades de pontones flotantes que sostienen el paseo marítimo flotante. El treinta y uno por ciento de los barcos atracados, examinados en el puerto deportivo, estaban incrustados con esta especie, cuyo aspecto algunas veces fue una sola incrustación prominente. Varias especies de macroinvertebrados se asociaron con las colonias del A. verticillata, incluyendo algunas especies introducidas que se registran por primera vez en la costa Mediterránea de Francia: Paracerceis sculpta, Paranthura japonica y Caprella scaura. Este briozoo podría ayudar a la transferencia de diferentes macroinvertebrados a otros lugares, pues proporciona un hábitat y un substrato cuando está adherido a los cascos de los barcos.
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 1807), Malaga and Algiers (Mediterranean Sea), the Red Sea, the Antilles and Trinidad (Atlantic Ocean), Mauritius (Indian Ocean) and Mariana Island (Pacific Ocean; Agardh 1823, Kützing 1843, Durieu de Maisonneuve 1848, Zanardini 1858, Reichert 1870). 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. 2015), 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 2009, Wirtz and Canning-Clode 2009, Minchin 2012). Such a cosmopolitan distribution has posed questions as to its real native origin: Winston (1995) suggested an origin from the Caribbean region, whilst Floerl et al. (2009a) labelled it as being cryptogenic and Vieira et al. (2014) suggested that, since a wide range of habitats are occupied, A. verticillata may contain cryptic species. In a recent account, Galil and Gevili (2014) 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 2014). This bryozoan subsequently became introduced elsewhere, including Macaronesia and the Mediterranean Sea (Wirtz and Canning-Clode 2009, Galil and Gevili 2014). Therefore, its status should now be considered to be pseudo-indigenous in the Mediterranean Sea (Ferrario et al. 2014), i.e. a non-indigenous species (NIS) having long been perceived to be native (Carlton 2009).
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 1888), Marseille Harbour (Gautier 1962) and Martigues Harbour (Chimenz et al. 1981). 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 2012) or shorter and bushy (Zirpolo 1933), and sometimes reaching a high biomass (Lenzi et al. 2009).
Due to its outstanding spreading capability, A. verticillata can have ecological and economic impacts (Gossett et al. 2004). 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 1965). Moreover, this effective suspension feeder can remove large volumes of planktonic material, affecting food web dynamics (Amat and Tempera 2009). 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 2007). 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. 2004). 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 2008).
This NIS should receive attention within the Mediterranean Sea as being a nuisance species, as has been suggested elsewhere (Coleman 1999, Farrapeira 2011, Minchin 2012, Nagy 2013). In particular, following the requirements of the European Marine Strategy Directive (EC 2008), 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. 2014).
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 METHODS
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.
La Grande Motte marina on the Mediterranean coast of southern France. The pontoons that were sampled lie beneath the boardwalk indicated with a star.
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), the method recommended for biological surveys elsewhere for port regions (Awad et al. 2014). 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.
Classes of abundance and distribution (ADR) according to Olenin et al. (2007). According to this scheme, Amathia verticillata should obtain level “C” (see text).
Abundance
Distribution scale
One locality
Several localities
Many localities
All localities
Low
A
A
B
C
Medium
B
B
C
D
High
B
C
D
E
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.
RESULTS
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 of Amathia verticillata attached to (A) a pontoon and (B) a leisure craft hull.
Colony number per pontoon examined.
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).
Non-indigenous peracarids associated with the spaghetti bryozoan in La Grande Motte: (A) Paracerceis sculpta; (B) Paranthura japonica; (C) Caprella scaura; (D) C. scaura specimens attached to Amathia verticillata branches.
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.
Known distribution of Amathia verticillata in the Mediterranean Sea and NE Atlantic. Records from harbours and marinas highlighted with circles. Numbers of records refer to Table 2.
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).
Records of Amathia verticillata in the Mediterranean Sea (Med) and NE Atlantic Ocean (Atl; record no. 63 refers to Suez Canal). The first column indicates the corresponding labels in Figure 5, where some records from the present Table have been merged; asterisks indicate years of publication, used whenever years of record were not available. Some early records were misidentifications of A. verticillata as macroalgae: record nos. 1, 25 and 71 under the name Ascothamnion intricatum; records no. 9 under the name Ulva intricata, nos. 10 and 37 under the names Valonia intricata and Hydra verticillata.
Labels in Fig. 5
Record no.
Country/Region
Year of record
Locality
Habitat
Reference
1
1
Africa (Eastern coast)
1889*
Unknown
Unknown
De Toni (1889)
2
2
Spain (Canary Islands)
2011
Lanzarote: Puerto del Carmen, Puerto Calera and
Marina Rubicon; Gran Canaria: Puerto del Morgan
Marinas
Minchin (2012)
3
3
Portugal (Madeira)
2009
Quinta do Lorde
Harbour
Wirtz and Canning-Clode (2009)
4
4
Portugal (Azores)
2008
Arcipelago of the Azores (Marina of Horta,
Pico Island, Sa Miguel Island)
Marinas and natural habitat
Amat and Tempera (2009)
5
5
Portugal
1937*
Unknown
Unknown
Nobre A. (1937)
6
Portugal
1942*
Berlengas Islands
Unknown
Nobre and Braga (1942)
6
7
Portugal
2001-2002
Ria Formosa
Lagoon
Curtis and Vincent (2005)
7
8
Spain (Atl)
2009
Chipiona
Harbour
Guerra-García et al. (2011)
9
Spain (Atl)
1807* (1st NE Atlantic record); 1823*
Cadiz
Unknown
De Roxas Clemente (1807); Agardh (1823)
8
10
Spain (Med)
1823*
Malaga
Unknown
Agardh (1823)
9
11
Spain (Med)
1982-86
Mar Menor lagoon islands
Lagoon
Pérez-Ruzafa et al. (1988)
12
Spain (Med)
1986*
Benidorm Island, València, Dénia
Unknown
Zabala (1986)
10
13
Spain (Med)
1921*
Mahon and Palma de Mallorca (Balearic Islands)
Unknown
Barroso (1922)
14
Spain (Med)
1956*
Mallorca (Balearic Islands)
Unknown
Prenant and Bobin (1956)
11
15
Spain (Med)
1986*
Catalan coasts: Sant Carles de la Ràpita,
Cases d’Alcanar
Unknown
Zabala (1986)
16
Spain (Med)
2005
Bay of Roses (Girona)
Artificial substrate
Martìnez and Adarraga (2008)
17
Spain (Med)
@ 2000
Blanes
Harbour
Xavier Turon (Pers. Comm.)
12
18
Spain (Med)
2008
Port de Llançà (Catalonia)
Harbour
Dan Minchin (Pers. Obs.)
13
19
France (Med)
2014
La Grande Motte
Marina
Present work
14
20
France (Med)
1962*
Marseilles
Harbour
Gautier (1962)
21
France (Med)
1981*
Martigues
Harbour
Chimenz et al. (1981)
15
22
France (Med)
1888*
Menton
Unknown
Joliet (1888)
23
France (Med)
1986*
Villefranche
Unknown
Zabala (1986)
24
Italy (Tyrrhenian)
1967-69
Vado Ligure
Artificial substrate
Geraci and Relini (1970)
16
25
Italy (Tyrrhenian)
1849*
Genoa
Unknown
Kützing (1849)
26
Italy (Tyrrhenian)
1959-60
Genoa
Harbour
Relini (1964)
27
Italy (Tyrrhenian)
2013
Santa Margherita Ligure
Marina
Jasmine Ferrario (Pers. Obs.)
17
28
Italy (Tyrrhenian)
2010-2011
Riomaggiore
Marina within an MPA
Lodola (2012)
29
Italy (Tyrrhenian)
2010-2011
La Spezia
Harbour
Ferrario et al. (2014)
30
Italy (Tyrrhenian)
2013
Lerici
Marina
Jasmine Ferrario (Pers. Obs.)
18
31
Italy (Tyrrhenian)
1849*
Leghorn
Unknown
Kützing (1849)
32
Italy (Tyrrhenian)
2013
Viareggio
Marina
Jasmine Ferrario (Pers. Obs.)
19
33
Italy (Tyrrhenian)
1970-1990
Orbetello
Lagoon
Lenzi et al. (2009)
20
34
Italy (Tyrrhenian)
1968-1971
Civitavecchia
Harbour
Chimenz Gusso and Rivosecchi Taramelli (1973)
21
35
Italy (Tyrrhenian)
1982-84
Caprolace, Monaci e Fogliano
Lagoons
Pieroni and Morgana (2003)
36
Italy (Tyrrhenian)
2010
Sabaudia
Lagoon
Armando Macali (Pers. Comm.)
22
37
Italy (Tyrrhenian)
1822* (1st Med record)
Naples
Unknown
Delle Chiaje (1822)
38
Italy (Tyrrhenian)
1963
Margellina (Naples)
Harbour
Ranzoli (1963)
39
Italy (Tyrrhenian)
1963
Fusaro
Lagoon
Carrada et al. (1965)
23
40
Italy (Tyrrhenian)
1975-76
Ischia
Harbour
Chimenz et al. (1981)
24
41
Italy (Tyrrhenian)
2010-2011
Olbia (Sardinia)
Harbour
Ferrario et al. (2014)
42
Italy (Tyrrhenian)
2014
Porto Torres (Sardinia)
Harbour
Jasmine Ferrario (Pers. Obs.)
25
43
Italy (Tyrrhenian)
1977*
Palermo (Sicily)
Harbour
Ardizzone et al. (1977)
26
44
Italy (Tyrrhenian)
1952
Santa Venere (Marsala, Sicily)
Lagoon
Gautier (1958)
27
45
Italy (Ionian)
1952; 1979-80
Catania (Sicily)
Harbour
Gautier (1958)
28
46
Italy (Ionian)
2010-2011
Lampedusa island
Harbour
Ferrario et al. (2014)
29
47
Italy (Ionian)
2008-2009
Capo Rizzuto MPA
Natural
Riolo (2009)
30
48
Italy (Ionian)
1972-82; 2003-2004
Mar Piccolo di Taranto
Artificial substrate
Montanaro (1983); Pierri et al. (2010)
49
Italy (Adriatic)
1898*
San Cataldo (Lecce)
Natural
Condorelli (1898)
31
50
Italy (Adriatic)
1987
Brindisi
Harbour
Chimenz and Faraglia (1993)
32
51
Italy (Adriatic)
1973-1974
Manfredonia
Harbour
Gherardi et al. (1974)
33
52
Italy (Adriatic)
1937*
Venice lagoon
Lagoon
Neviani (1937)
34
53
Italy (Adriatic)
1867*
Gulf of Trieste
Harbour
Reichert (1867)
35
54
Croatia
1907*; 1928*
Rovinj
Unknown
Zimmermann (1907); Vatova (1928)
55
Croatia
1973-99
Rijeka Bay
Natural
Zavodnik and Kovačić (2000)
36
56
Greece
1974-75
Chalkis
Unknown
Castritsi-Cathrios and Kiortsis (1984)
57
Greece
1970;1980
Corinthe Gulf
Natural
Castritsi-Cathrios and Kiortsis (1984)
58
Greece
1981
Gulf of Patras (Patraikos Bay)
Natural
Castritsi-Cathrios and Ganias (1989)
37
59
Greece
1969; 1977; 1978
Pirèe
Harbour
Castritsi-Cathrios and Kiortsis (1984)
38
60
Greece
1974-75
Rhodes Island
Unknown
Castritsi-Cathrios and Kiortsis (1984)
39
61
Syria
1954
Latakia
Natural
Gautier (1956)
40
62
Israel
From 1930s
Israel coast
Natural
Fishelson (2000)
63
Israel
1960
Mikhmoret
Harbour
Lipkin and Safriel (1971)
41
64
Israel
2013
Ashdod
Marina
Galil and Gevili (2014)
42
65
Egypt
1828*
Suez Canal
Unknown
Ehrenberg (1828a)
43
66
Egypt
1828*
Alexandria
Natural
Ehrenberg (1828b)
67
Egypt
1990-91
Alexandria
Harbour
El-Komi (1992)
44
68
Tunisia
1934*
Gulf of Gabès
Natural
Seurat (1934)
45
69
Tunisia
1995-97
Tunisia North lagoon
Lagoon
Tlig-Zouari and Maamouri-Mokhtar (2008)
46
70
Tunisia
1981*
Bizerte
Harbour
Chimenz et al. (1981)
47
71
Algeria
1848*
Algiers
Artificial substrate
Durieu de Maisonneuve (1848)
DISCUSSION
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. 2014). These species may become distributed over a wide region, even across oceans (Minchin et al. 2006). 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 1933, Robinson 2004). Additionally, the basal stolon can resist low temperatures and strong currents (Zirpolo 1933), 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. 1993).
The preponderance of records of A. verticillata from marinas worldwide (Ryland 1965, Ganapathi and Satyanarayana Rao 1968, Ardizzone and Riggio 1981, Gordon and Mawatari 1992, Hewitt et al. 2004, Ramadan et al. 2006, Abdel-Salam and Ramadan 2008, Carlton and Eldredge 2009, Wirtz and Canning-Clode 2009, Farrapeira 2011, Minchin 2012, Galil and Gevili 2014, Tamsouri et al. 2014) 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 1933). A. verticillata produces vegetative fragments from a colony that can survive and attach to new substrates (Robinson 2004). 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. 1998, Barnes 2002) 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 1966, Galil and Gevili 2014), and they enter a senescent phase during the autumn (Zirpolo 1933). Along sheltered coasts A. verticillata has the ability to form overwintering stages from which new colonies can evolve (Geiger and Zimmer 2002) 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. 2014) 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. 2006). 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 1933). 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 2009), Italy (Riolo 2009) and Israel (Lipkin and Safriel 1971).
As reported by other authors (Farrapeira 2011, Ferrario et al. 2014) 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 2014). 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. 2014). It has been reported from the French Atlantic coast (Lavesque et al. 2013), and the Italian Adriatic and Tyrrhenian coasts (Marchini et al. 2014). 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. 2014). 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 2012, Ramalhosa et al. 2015). Recent molecular evidence suggests that its spread will have involved multiple introduction events of several sub-species (Cabezas et al. 2014). 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. 2014).
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. 2011), on the Balearic Islands (Ros et al. 2013), on the Canary islands (Minchin 2012), on Madeira Island (Ramalhosa et al. 2015), 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 2013); Polycerella emertoni A. E. Verrill, 1880 (in Agadir, Tunisia: Tamsouri et al. 2014); and Okenia spp. (Rudman 2004, Carlton and Eldredge 2009, Ortea et al. 2009).
CONCLUSION
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 1994, Carlton 1996, Floerl et al. 2009b). 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 2002, Savini et al. 2006) 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.
ACKNOWLEDGEMENTS
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.
REFERENCES Abdel-Salam K.H.M. Ramadan S.H.E. Fouling bryozoa from some Alexandria harbours, Egypt (I). Erect species 20089520http://dx.doi.org/10.12681/mms.129 Agardh C.A.1823 Lundae [Lund]: ex officina Berlingiana [vii-viii], [399]-531 Amat J.N. Tempera F.Zoobotryon verticillatum Delle Chiaje, 1822 (Bryozoa), a new occurrence in the archipelago of the Azores (North-Eastern Atlantic)200958761764http://dx.doi.org/10.1016/j.marpolbul.2009.02.019 Ardizzone G. Riggio S. Similitudine e diversitá nelle biocenosi bentoniche del Porto di Palermo in relazione al substrato di insediamento 19813587603 Ardizzone G.D. Mazzola A. Riggio S. Modificazioni nelle comunità incrostanti del porto di Palermo in relazione a diverse condizioni ambientali 1977151159 Awad A. Haag F. Anil A.C. GloBallast Monograph, 222014 London, UK GEF-UNDP-IMO GloBallast Partnerships Barnes D.K.A. Invasions by marine life on plastic debris 2002416808809http://dx.doi.org/10.1038/416808a Barroso M.G. Notas sobre briozoos marinos españoles. X. Especiés de Mahon, Baleares 19222288101 Cabezas M.P. Xavier R. Branco M. Invasion history of Caprella scaura Templeton, 1836 (Amphipoda: Caprellidae) in the Iberian Peninsula: multiple introductions revealed by mitochondrial sequence data 201416125http://dx.doi.org/10.1007/s10530-014-0660-y Carlton J.T. Pattern, process, and prediction in marine invasion ecology 19967897106http://dx.doi.org/10.1016/0006-3207(96)00020-1 Carlton J.T. Deep invasion ecology and the assembly of communities in historical time. Rilov G. Crooks J.A.2009 Berlin Heidelberg Springer-Verlag 1356http://dx.doi.org/10.1007/978-3-540-79236-9_2 Carlton J.T. Eldredge L.G. The introduced and cryptogenic marine and estuarine animals and plants of the Hawaiian Archipelago 200941203 Honolulu Bishop Museum Press Carrada G.C. Sacchi C.F. Rigillo M.T. Ricerche sulla valenza ecologica dei briozoi salmastri. I – Significato delle variazioni ritmiche dei fattori ambientali 196520153208 Castritsi-Catharios J. Kiortsis V. Bryozoaires côtiers de Grèce. Proposition d'une méthode automatisée de détermination systématique 1984118998 Castritsi-Catharios J. Ganias G. Bryozoaires épiphytes de l'herbier de Posidonies du Golfe de Patras (Greece). 19892157160 Chimenz C. Faraglia E. Biol. Mar. Mediterr. Supplemento al Notiziario S.I.B.M. 1 1993 Chimenz C. Fresi E. Cinelli F. Ricerche sui popolamenti bentonici di substrato dure del porto d'Ischia. Briozoi 19816187206 Chimenz Gusso C. Rivosecchi Taramelli E. Osservazioni sulle biocenosi incrostanti piastre di eternit immerse a diversa profondità nel porto di Civitavecchia.19732877100 Clarke-Murray C. Gartner H. Gregr E.J. Spatial distribution of marine invasive species: environmental, demographic and vector drivers.201420824836http://dx.doi.org/10.1111/ddi.12215 Coleman F.S. Note on Zoobotryon verticillatum (Bryozoa) in a solar saltfield 199987174http://dx.doi.org/10.1023/A:1009088401641 Condorelli M. Invertebrati raccolti dalla R. Nave "Scilla" nell'Adriatico e nel Jonio 189872549 Cornell J.2002 London McGraw Hill Curtis J.M.R. Vincent A.C.J. Distribution of sympatric seahorse species along a gradient of habitat complexity in a seagrass-dominated community 20052918191http://dx.doi.org/10.3354/meps291081 Delle Chiaje S. Vol. 1. dalla stamperia de 'Fratelli Fernandes'1822http://dx.doi.org/10.5962/bhl.title.46298 De Toni G.B. Vol. I. Sylloge chlorophycearum omnium hucusque cognitarum,1889http://dx.doi.org/10.5962/bhl.title.10544 De Roxas Clemente R.S.1807 Madrid Imp. de Villalpando Durieu de Maisonneuve M.C. Exploration scientifique de l'Algérie 18481361400 EC [European Commission] 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). 2008 L 1641940 Ehrenberg C.G.1828 Pars Zoologica Ehrenberg C.G.1828 El-Komi M.M. Field and laboratory studies on the ecology of marine fouling in Alexandria harbour, Egypt 199218115140 Farrapeira C.M.R. The introduction of the bryozoan Zoobotryon verticillatum (Delle Chiaje, 1822) in northeast of Brazil: a cause for concern. 2011131316http://dx.doi.org/10.1007/s10530-010-9788-6 Ferrario J. Marchini A. Lodola A. The pseudoindigenous bryozoan Zoobotryon verticillatum along the Mediterranean and Atlantic European coasts 201421117118 Fishelson L. Marine animal assemblages along the littoral of the Israeli Mediterranean seashore: the Red-Mediterranean Seas communities of species 200067393415http://dx.doi.org/10.1080/11250000009356345 Floerl O. Inglis G.J. Gordon D.P. Patterns of taxonomic diversity and relatedness among native and non-indigenous bryozoans 200915438449http://dx.doi.org/10.1111/j.1472-4642.2008.00553.x Floerl O. Inglis G.J. Dey K. The importance of transport hubs in stepping-stone invasions 2009463745http://dx.doi.org/10.1111/j.1365-2664.2008.01540.x Fryganiotis K. Chintoroglou Ch. New Mediterranean Biodiversity Records (October, 2014). Katsanevakis S. Acar Ü. Ammar I. First record of the isopod Paracerceis sculpta in the Aegean Sea: established populations in north Aegean marinas 201415667687 Galil B.S. Gevili R. Zoobotryon verticillatum (Bryozoa: Ctenostomatida: Vesiculariidae), a new occurrence on the Mediterranean coast of Israel. 20147e17http://dx.doi.org/10.1017/S1755267214000086 Galil B.S. Marchini A. Occhipinti-Ambrogi A. International arrivals: widespread bioinvasions in European Seas.201426152171http://dx.doi.org/10.1080/03949370.2014.897651 Ganapathi P.N. Satyanarayana Rao K. Fouling bryozoans in Visakhapatnam 1968378189 Gautier Y.V. Première faunule des bryozoaires des cotes syriennes 19567554561 Gautier Y.V. Bryozoaires marins actuels de Sicile 195844568 Gautier Y.V. Recherches écologiques sur les Bryozoaires Chilostomes en Méditerranée Occidentale 1962381434 Geiger D.L. Zimmer R.L. Anchoring rootlets in Bowerbankia imbricata (Bryozoa: Ctenostomata)200270791797 Geraci S. Relini G.. Insediamento su pannelli atossici immersi nella Rada di Vado Ligure: i Briozoi 1970381933 Gherardi M. Lepore E. Muscio A. Study on Manfredonia harbour's fouling communities 19744, 5, 6275287 Giacobbe S. De Matteo S. The potentially invasive opisthobranch Polycera hedgpethi Er. Marcus, 1964 (Gastropoda Nudibranchia), introduced in a Mediterranean coastal lagoon 20134359364 Gordon D.P. Mawatari S.F. Atlas of marine-fouling Bryozoa of New Zealand ports and harbours 1992107152 Gosset L. Lester J. Gonzales L.2004 Texas Texas Commission on Environmental Quality Guerra-García J.M. Ros M. Dugo-Cota A. Geographical expansion of the invader Caprella scaura (Crustacea: Amphipoda: Caprellidae) to the East Atlantic coast.201115826172622http://dx.doi.org/10.1007/s00227-011-1754-z Hewitt C.L. Campbell M.L. Thresher R.E. Introduced and cryptogenic species in Port Phillip Bay, Victoria, Australia.2004144183202http://dx.doi.org/10.1007/s00227-003-1173-x
Hopkins G.A. Forrest B.M. Management options for vessel hull fouling: an overview of risks posed by in-water cleaning 200865811815http://dx.doi.org/10.1093/icesjms/fsn026 Joliet L. Bryozoaries nouveaux de Roscoff et Bryozoaries de Menton 18882103109 Kützing F.T.1843 Leipzig F.A. Brockhaus Kützing F.T.1849 Leipzig F.A. Brockhaus Lavesque N. Sorbe J.C. Bachelet G. Recent discovery of Paranthura japonica Richardson, 1909 (Crustacea: Isopoda: Paranthuridae) in European marine waters (Arcachon Bay, Bay of Biscay)20132215219http://dx.doi.org/10.3391/bir.2013.2.3.07 Lenzi M. Birardi F. Boddi S. The lagoon of Orbetello Cecere E. Petrocelli A. Izzo G.2009 Venice Lagunet, CORILA, 111123 Lipkin Y. Safriel U.. Intertidal zonation on rocky shores at Mikhmoret (Mediterranean, Israel).197159130http://dx.doi.org/10.2307/2258448 Lodola A. Italy Univ. Pavia, 2012 Marchini A. Sorbe J.C. Torelli F. The non-indigenous Paranthura japonica Richardson, 1909 in the Mediterranean Sea: travelling with shellfish? 201415545553 Martìnez J. Adarraga I. First record of invasive caprellid Caprella scaura Templeton, 1836 sensu lato (Crustacea: Amphipoda: Caprellidae) from the Iberian Peninsula 20083165171http://dx.doi.org/10.3391/ai.2008.3.2.6 Minchin D. The transport and the spread of living aquatic species Davenport J. Davenport J.L.2006 Berlin Heidelberg New York, Springer 7797 Minchin D. Rapid assessment of the bryozoan, Zoobotryon verticillatum (Delle Chiaje, 1822) in marinas, Canary Islands. 20126421462150http://dx.doi.org/10.1016/j.marpolbul.2012.07.041 Montanaro C.Settlement of bryozoans in the Mar Piccolo of Taranto (Southern Italy) from 1972 to 1982.1983991103 Nagy L.2013 Jan 26, 2015 http://www.invasivespeciesinfo.gov/toolkit/detelk.shtml Neviani A. I briozoi della laguna veneta 193713382403 Nobre A.Fauna Marinha de Portugal. 1 aditamento 193793130 Nobre A. Braga S.M. Notas sôbre a Fauna das Ilhas Berlengas e Farilhôes 1942138166 O'Kelly M.E. Miller H.J. The hub network design problem: a review and synthesis 199423140http://dx.doi.org/10.1016/0966-6923(94)90032-9 Ojaveer H. Galil B.S. Minchin D. Ten recommendations for advancing the assessment and management of non-indigenous species in marine ecosystems 201444160165http://dx.doi.org/10.1016/j.marpol.2013.08.019 Olenin S. Minchin D. Daunys D. Assessment of biopollution in aquatic ecosystems.200755379394http://dx.doi.org/10.1016/j.marpolbul.2007.01.010 Ortea J. Moro L. Espinosa J. El género Okenia Menke, 1830 (Mollusca: Nudibranchia) en las islas Canarias con notas sobre Okenia zoobotryon (Smallwood, 1910), una especie en controversia permanente. 2009377583 Ortega M.J. Zubia E. Salva J. A new brominated indole-3-carbaldehyde from the marine bryozoan Zoobotryon verticillatum.199356633636http://dx.doi.org/10.1021/np50094a031 Pérez-Ruzafa À. Pérez-Ruzafa I.M. Marcos C. Cartografia bionómica del poblamiento bentónico de las islas del Mar Menor. Islas Perctiguera y del Barón.198892740 Pieroni A. Morgana J.G.2003 Casaccia ENEA Pierri C. Longo C. Giangrande A. Variability of fouling communities in the Mar Piccolo of Taranto (Northern Ionian Sea, Mediterranean Sea). 201090159167http://dx.doi.org/10.1017/S0025315409990798 Prenant M. Bobin G.60 1956 Faune de France, Ramadan S.E. Kheirallah A.M. Abdel-Salam K.M. Marine fouling community in the Eastern harbour of Alexandria, Egypt compared with four decades of previous studies 200671930http://dx.doi.org/10.12681/mms.167 Ramalhosa P. Canning-Clode J.. The invasive caprellid Caprella scaura Templeton, 1836 (Crustacea: Amphipoda: Caprellidae) arrives on Madeira Island, Portugal 2015497102http://dx.doi.org/10.3391/bir.2015.4.2.05
Ranzoli F. Studio quantitativo della sessualità in colonie di Zoobothryon verticillatum (Delle Chiaje). 196348227253 Reichert K.B.1867 Berlin Akademie der Wissenschaften zu Berlin. F. Dümmler, Reichert K.B.1870 Berlin Akademie der Wissenschaften zu Berlin F. Dümmler, Relini G. Andamento stagionale degli organismi sessili del Porto di Genova 196413281296 Relini G. Le comunita` dominanti nel 'fouling' portuale di Genova 196657136156 Riolo F.2009 Italy Capo Rizzuto MPA http://www.riservamarinacaporizzuto.it/dati/upload/files/RELAZIONE_MONITORAGGIO_CORALLI%281%29.pdf Robinson N.M. Orlando, Florida Univ. Central Florida 2004 Ros M. Vázquez-Luis M. Guerra-García J.M. The tropical caprellid amphipod Paracaprella pusilla a new alien crustacean in the Mediterranean Sea 201367675685http://dx.doi.org/10.1007/s10152-013-0353-4 Ros M. Guerra-García J.M. Navarro-Barranco C. The spreading of the non-native caprellid (Crustacea: Amphipoda) Caprella scaura Templeton, 1836 into southern Europe and northern Africa: a complicated taxonomic history 201415145155 Rudman W.B. Further species of the opisthobranch genus Okenia (Nudibranchia: Goniodorididae) from the Indo-West Pacific. 2004695170 Ryland J.S. Volume 2: Polyzoa 1965 OECD Savini D. Occhipinti-Ambrogi A. Minchin D. A concealed aspect in coastal water conservation: the diffusion of alien species by recreational craft.200613764772 Seurat L.G. Formations littorales et estuaires de la Syrte Mineure (Golfe de Gabès).193432165 Tamsouri N. Carmona L. Moukrim A.Polycerella emertoni and Favorinus ghanensis: two new alien sea slug molluscs from the Moroccan Atlantic coasts 20147 e13http://dx.doi.org/10.1017/S1755267214000050 Tlig-Zouari S. Maamouri-Mokhtar F. Macrozoobenthic species composition and distribution in the Northern lagoon of Tunis. 20082115 Vatova A. Compendio della Flora e della Fauna del. Mare Adriatico presso Rovigno 19281431614 Vieira L.M. Migotto A.E. Winston J.E. Ctenostomatous Bryozoa from São Paulo, Brazil, with descriptions of twelve new species 20143889485524http://dx.doi.org/10.11646/zootaxa.3889.4.2 Waeschenbach A. Vieira M. Reverter-Gil O. A phylogeny of Vesiculariidae (Bryozoa, Ctenostomata) supports synonymisation of three genera and reveals possible cryptic diversity 2015 in press http://dx.doi.org/10.1111/zsc.12130
Watts P.C. Thorpe J.P. Taylor P.D. Natural and anthropogenic dispersal mechanisms in the marine environment: a study using cheilostome Bryozoa 1998353453464http://dx.doi.org/10.1098/rstb.1998.0222 Williams S.L. Introduced species in seagrass ecosystems: status and concerns 200735089110http://dx.doi.org/10.1016/j.jembe.2007.05.032 Winston J.E. Ectoproct diversity of the Indian River coastal lagoon 1995578489 Wirtz P. Canning-Clode J. The invasive bryozoan Zoobotryon verticillatum has arrived at Madeira Island 20094669670http://dx.doi.org/10.3391/ai.2009.4.4.11 Zabala M.1986 Barcelona Institut d'Estudis Catalans, Zanardini G.1858 Venezia Reale Istituto veneto Zavodnik D. Kovačić M. Index of marine fauna in Rijeka bay (Adriatic Sea, Croatia)20009297379 Zimmermann H. Tierwelt am Strande der blauen Adria 190778293322 Zirpolo G.Zoobotryon verticillatum (Delle Chiaje). 193317190441