While exploring the presence of non-indigenous fouling species colonizing settlement plates deployed in local marinas in Madeira Island (north-eastern Atlantic Ocean), two non-indigenous species (NIS) of free-swimming crustaceans, Paracerceis sculpta (Holmes, 1904) and Sphaeroma walkeri Stebbing, 1905 (Isopoda: Sphaeromatidae), were detected. Paracerceis sculpta is native to the Pacific Coast of North and Central America and has been introduced into many other regions worldwide. Sphaeroma walkeri is native to the northern Indian Ocean and nowadays is considered one of the most widely ship-transported species globally. Both species were collected in the marina of Funchal, Madeira Island, Portugal, during monitoring surveys in 2015. Moreover, several specimens of S. walkeri were also found in a foreign recreational yacht hull, during a dry dock inspection. These findings suggest that hull fouling is a significant vector for the introductions of marine invertebrates into the Madeira island system.
Today, the introduction of non-indigenous species (NIS) into new areas is still an inevitable phenomenon, representing a major environmental and economic threat to biodiversity in coastal marine ecosystems (Nentwig, 2007; Canning-Clode, 2015). This fact is even more disturbing in the case of island ecosystems due to the relatively poor biological communities which are integrated by a great number of endemic species (Cronk, 1997). One of the most relevant vectors contributing to the spread and establishment of marine NIS in the world is commercial shipping, which facilitates the unintentional transport of species in ships ballast water tanks and via hull fouling across seas and oceans (Ruiz et al., 2000; Clarke Murray et al., 2014). Consequently, it is of crucial importance that early detections of NIS in new ecosystems and areas are promptly reported, including the potential pathways and vectors of introduction, spread rates and life histories. As a result, these records have the potential to contribute to future checklists, reviews, impact assessment and ecosystems management (Zenetos et al., 2005; Galil et al., 2016). In addition, this recent data would support the implementation of new marine strategies and monitoring programs (Olenin et al., 2010). In this context, a comprehensive study by Chainho et al. (2015) has listed a total of 133 NIS for the Portuguese coastal areas, including estuaries, coastal lagoons and islands. The lowest number of NIS was recorded for the Portuguese mainland territory, with a total of 68 different species recorded for both marine and brackish waters. In contrast, a total of 85 different species were recorded for the island systems, with 64 and 39 species recorded for the Azores and Madeira archipelagos, respectively (Chainho et al., 2015).
The Madeira archipelago is comprised of two inhabited volcanic islands (Madeira and Porto Santo) located southwest of continental Europe and 700 km from the Moroccan coast. Due to its strategic geographic position in the north-eastern Atlantic Ocean, the Madeira Island has historically provided an important maritime route for many ships between Europe, the Americas and Africa. Nowadays, most of the maritime traffic comes from tourist cruise ships and sailing yachts for refuelling, and rest stops from different parts of the world (APRAM, 2016). In recent years, the number of marine NIS detections in Madeira archipelago has increased significantly due to on-going monitoring surveys, particularly in marinas on the southern coast of the islands. Consequently, several records of different taxa have been detected (Canning-Clode et al., 2013), such as Annelida (Ramalhosa et al., 2014), Crustacea (Ramalhosa & Canning-Clode, 2015) Bryozoa (Wirtz & Canning-Clode, 2009; Ramalhosa et al., 2016; Souto et al., 2016), including bryozoan species previously undescribed for science in Madeira Island (Souto et al., 2015) and Porto Island (Souto et al., 2016).
Peracarid crustaceans (mainly amphipods, isopods, tanaids, mysids and cumaceans) constitute a species rich and abundant group of small crustaceans (usually less than 20 mm) from all types of marine, freshwater and terrestrial habitats (Melic, 2015). There are approximately 4500 described species of marine isopods, which can be found at different depths and marine habitats in the world (Kensley, 1998). However, research on peracarid crustaceans in the Madeira Archipelago has been scarce or rather unknown, with only a few studies conducted in freshwater and brackish waters (Dahl, 1958; Kaim-Malka, 1970; Stock & Abreu, 1992; Stock 1993, 1994), and marine waters (Jacobs, 1987; Fonseca et al., 1995; Castelló & Junoy, 2007). To the best of our knowledge, only 4 isopod species were recorded for the Madeira Island from which three species are endemic to the Macaronesia region: Eisothistos adcentralis Knight-Jones & Knight-Jones, 2002, Ceratothoa parallela (Otto, 1828), Lekanesphaera glabella Jacobs, 1987, while the last one, Sphaeroma serratum (Fabricius, 1787), is considered to have a worldwide distribution (Castelló & Junoy, 2007).
In the present paper, we report the presence of two additional species of isopods, Paracerceis sculpta (Holmes, 1904) and Sphaeroma walkeri Stebbing, 1905 (Isopoda: Sphaeromatidae), for Madeira Island, north-eastern Atlantic Ocean. Both species were found in the Funchal marina. Also, we identified a potential key vector of introduction of these invaders in the island by finding specimens of S. walkeri on the hull of a foreign yacht, while performing dry dock inspections at a local shipyard along the south coast of Madeira island.
MATERIAL AND METHODS
In 2006 we initiated a NIS monitoring program of sessile communities in a local marina located along the South-eastern coast of Madeira Island (Canning-Clode et al., 2009, 2013). In more recent years, we have expanded this monitoring programme to all marinas of the Madeira archipelago (Ramalhosa et al., 2014; Ramalhosa & Canning-Clode, 2015) with four main study sites: Calheta (32°43′N 17°10′W), Funchal (32°38′N 16°54′W), Quinta do Lorde, Caniçal (32°44′N 16°42′W) and Porto Santo Island (33°03′N 16°18′W) (fig. 1a-d, respectively). Following the methods used by Canning-Clode et al. (2013) and Ramalhosa et al. (2016), 10 polyvinylchloride (PVC) settlement plates (14 × 14 × 0.3 cm) were individually attached to a brick in a horizontal orientation facing downwards and hung at about 1 m depth, from pontoons in four local marinas. Every 3 months, plates were retrieved from the field and examined to determine species composition. During each sampling event, plates were carefully examined using a stereo microscope (Leica Wild-M3 Heerbrugg). Moreover, specimens from settling plates were photographed using a Sony DSC-W55 camera. Unknown taxa were collected and preserved in 95% ethanol for later identification. For the purpose of this analysis, however, we are only reporting the presence of free-swimming Sphaeromatidae species collected during a sampling event in Funchal marina in October 2015.
In addition to the settling plate deployment, we have also initiated in 2013 dry dock inspections (DDI) on foreign yacht hulls at a local shipyard (REPMaritima, http://www.repmaritima.com, 32°42′N 16°46′W; fig. 1e) for monitoring NIS arrivals via hull fouling (for a detailed sampling procedure see Ramalhosa et al., 2016). To complement the information related to the taxa found on vessel hulls, questionnaires were given to yacht owners to collect data concerning vessel identification, hull maintenance history and last mooring ports. Specimens collected from the Funchal marina and DDI were preserved in 95% ethanol and later examined with a StereoZoom Leica S8 APO and digital photographs were taken with an Olympus Stylus TG-4. Selected specimens were deposited in the collections of the Museu Municipal (História Natural) in Funchal (MMF), Madeira, Portugal.
In this study we report the presence of two isopod species: Paracerceis sculpta (fig. 2A, B, C, 3 ♂ specimens) and Sphaeroma walkeri (fig. 3A, B, 1 ♂ specimen) that were both collected on PVC settling plates from the marina of Funchal, Madeira Island on October 2015. The P. sculpta ‘α-male’ morph specimens had a mean body length of 5.3 ± 0.3 mm (, mean ± SD), whereas the S. walkeri male specimen measured 12.6 mm total length; both species were deposited at the Museu Municipal (História Natural) in Funchal as vouchers MMF 46513 and MMF 46514, respectively. Additionally, 17 individuals of S. walkeri (13 ♀, 4 ♂, fig. 3C) were found two weeks later during a DDI performed in November 2015 on the hull of a foreign yacht having La Gomera, Canary Islands, as a registered last port of call. These specimens were difficult to find as they were inhabiting holes and cavities along the stern, rudder and propeller of the vessel, thus collection from hidden spaces was only possible when using tweezers. The mean body length for the females of S. walkeri was 6.7 ± 1.4 mm (, mean ± SD), males had a slightly larger mean body length (7.6 ± 1.3 mm, , mean ± SD). These specimens were deposited as voucher MMF 46515. Thus, Paracerceis sculpta and Sphaeroma walkeri are recorded for the first time from Madeira Island, Portugal (north-eastern Atlantic Ocean). Following this, we describe the two isopod species detected in artificial substrates in the Madeira Island from 2015:
Order ISOPODA Latreille, 1817 Family Sphaeromatidae Latreille, 1825 Genus Paracerceis Hansen, 1805 Paracerceis sculpta (Holmes, 1904) (fig. 2A, B, C)
Dynamene sculpta Holmes, 1904: 300-302, pl. 34, figs. 1-7.
Cilicaea sculpta Richardson, 1905: 318-319, fig. 349.
Paracerceis sculpta Menzies, 1962: 340-341, fig. 2; Miller, 1968: 14, fig. 3; Schultz, 1969: 120, fig. 167; Pires, 1981: 219-220; Pires, 1982: 54, figs. 26-27; Harrison & Holdich, 1982: 440-441, fig. 10; Forniz & Sconfietti, 1983: 197-203, figs. 1-2; Forniz & Maggiore, 1985: 780; Bruce, 1986: 552; Rodriguez et al., 1992: 94-97, figs. 1-2; Loyola e Silva et al., 1999: 109-124, figs. 1-18; Yasmeen & Javed, 2001: 43-48, figs. 1-3; Hewitt & Campbell, 2001: 925-936, figs. 1-3; Yu & Li, 2001: 48-49; Espinosa-Pérez & Hendrickx, 2001: 1172-1176, fig. 2C; Yu & Li, 2003: 246-249, fig. 6; Marchini et al., 2017: 3, fig. 2.
Material examined.— MMF 46513 (15/10/2015, Funchal).
Species description.— Adult body size ranging between 5.0 and 5.7 mm; males with sexual polymorphism, three different morphs named α-, β- and γ-males (for further information see Shuster, 1987); α-males slightly larger than females. Species with marked sexual dimorphism, females with cephalon and pereon (i.e., head and thoracic segments including their appendages) similar to males, morphological differences especially at pleon level, α-males with enlarged and rugose pleotelson, with elongated forceps-like uropods, these structures are unmodified in females; body habitus relatively slender with a length/width ratio of 2-2.1; increasing in width posteriorly. Head narrow and scarcely longer than the first segment of the pereon. Eyes large, oval and very prominent, posterior-laterally situated. Dorsal surfaces of cephalosome and pereonites almost smooth, except for a posterior rugose micro-sculptured pattern. First pereonite larger than the others, pereonites bearing 5 to 7 tufts of setae situated in the posterior margin. Pleon and anterior part of pleotelson granulose. Posterior margin of pleon and middle part of pleotelson each with 3 setose tubercles. α-males with apex of pleotelson deeply cleft, with three pairs of notches, anterior and middle notches deep and posterior shallow. Regarding appendages, antennula shorter than the antenna, the peduncle article 1 enlarged, oval and emarginated at the distal end, peduncle article 2 subquadrate; flagella 9-11 articled, longer than the peduncle. Antenna scarcely reaching the middle of the thorax, peduncle slender, with articles 2-3 articles much longer than the preceding ones; flagellum a little longer than the peduncle, articles bearing tufts of short setae. As in all members of the subfamily Dynameninae, pereopods 1 and 2 are ambulatory, not prehensile. Pereopods increasing slightly in length posteriorly, bearing pads of short setae; propodus inferior margin armed with spines; dactylus transformed in a curved and strong spine. α-male uropods with endopod flattened, reduced, not reaching the level of pleotelson apex; exopod greatly elongated, gradually incurved, extending considerably beyond; pleotelsonic apex and bearing many bundles of setae, apex acute and directed obliquely upwards.
Remarks.— The β-male morph shows a body size and habitus very similar to mature females; however, this male morph presents well-developed and functional male genitalia (for a detailed description of masculine appendices see Shuster, 1987); the presence of these appendices allows for distinguishing this morph from females. Regarding γ-males, this morph mimics immature stages but as occurring in the previous case, the male genitalia is well-developed too, allowing for separating γ-males from immature stages.
Genus Sphaeroma Latreille, 1802 Sphaeroma walkeri Stebbing, 1905 (fig. 3A, B, C)
Sphaeroma walkeri Stebbing, 1905: 31-33, 61, pl. VII; 1910: 220; 1917: 444; Barnard, 1920: 360; 1936: 178; 1940: 405; Omer-Cooper, 1927: 240; Baker, 1928: 49; Nierstrasz, 1931: 192; Monod, 1931: 36; Monod, 1933: 198; Larwood, 1940: 28; Pillai, 1955: 132, pl. VI; Loyola e Silva, 1960: 41, figs. 6-7; Joshi & Ball, 1959: 61-62; Menzies & Glynn, 1968: 56, fig. 23; Miller, 1968: 8-11, fig. 3; Glynn 1972: 286, fig. 5; Carlton & Iverson, 1981: 31-48; Estevez & Simon, 1976: 288; Harrison & Holdich, 1984: 279-282, fig. 1; Jacobs, 1987: 22-24, fig. 6; Mak et al., 1985: 75; Kensley & Schotte, 1989: 235, fig. 101; Kussakin & Malyutina, 1993: 1170; Bruce, 1993: 156, fig. 1; Ghani & Qadeer, 2001: 871-872; Galil, 2008: 443-444; Khalaji-Pirbalouty & Wägele, 2010: 9-16, figs. 6-10.
Material examined.— MMF 46514 (15/10/2015, Funchal), MMF 46515 (3/11/2015, DDI).
Species description.— Adult body size ranging between 7.0 and 8.8 mm; males slightly bigger than females; no evident sexual dimorphism, females similar to males apart from sexual appendages and a slightly shorter pleotelson; body habitus relatively slender with a length/width ratio: 2; maximum width at the level of pereonites 5-6. Dorsal surface of cephalosome uneven. Pereonites 1 and 2 smooth, sometimes pereonite 2 with sparse low tubercles or with an irregular row of short tubercles. Pereonites 3 and 4 each one bearing two irregular transverse rows of low tubercles. Pereonites 5-7 and pleon each bearing one transverse row of prominent, round, blunt tubercles, with presence of sparse low tubercles too. Pleon with posterior margin bearing an additional row of small round tubercles. Dorsal surface of pleotelson granulose with four long, parallel and longitudinal rows of prominent tubercles, two on either side of midline; the inner one usually with six tubercles and the outer one with three tubercles. In lateral view pleotelson is relatively long, subapically concave and slightly upturned (laterally and apically raised); apex of telson with entire margin, lacking a notch or foramen but distinctly crenulated.
Regarding appendages, antennular penduncle article 1 subequal to article 3; article 2 reduced; article 3 slender and cylindrical; 13-16 articled flagellum extending to level of pereonite, flagellum articles bearing aesthetascs. Antenna, peduncle moderately slender; 14-20 articled flagella extending to article 3. Articles of flagellum bearing tufts of fine setae. As all the members of subfamily Sphaeromatinae, the pereopods 1 and 2 are ambulatory, not prehensile. All pereopods with inferior margins of merus, carpus and propodus bearing dense pads of long setae. Uropod rami broad, reaching pleotelsonic apex. Endopod with prominent dorsal tubercles, not reduced but showing almost the same length as exopod. Exopod without tubercles, with five to seven large, triangular, teeth along the external margin.
Remarks.— Some minor variation in the ornamentation of cephalosome, pereonites, telson as well as for some appendages, e.g., uropod exopod is pointed by several authors. For an exhaustive description of mouthparts, appendages and sexual organs see Harrison & Holdich (1984) and Khalaji-Pirbalouty & Wägele (2010).
In recent years, the marinas on the south coast of the Madeira archipelago islands have been a site of constant monitoring surveys for marine NIS (Canning-Clode et al., 2013; Ramalhosa et al., 2016; Souto et al., 2016). As a result, the number of NIS detections has been increasing, thus contributing in this way to a better knowledge of the marine invertebrate fauna of the Madeira archipelago. Here, we report for the first time the non-indigenous isopods Paracerceis sculpta (Holmes, 1904) and Sphaeroma walkeri Stebbing, 1905 (Isopoda: Sphaeromatidae) for the Madeira Island coast. It is difficult to determine when P. sculpta and S. walkeri arrived to Madeira island, because of the absence of studies and routine monitoring along the coastal waters and thus until recently.
Paracerceis sculpta is a species native to the northeastern Pacific, where it was first described by Holmes (1904) from San Clemente Island, in August 1893 and San Diego, CA, USA in July, 1895. The native distribution of this species is from southern California (Miller, 1968), San Quintin Bay, Southern Baja California (Menzies, 1962), northern and central Gulf of California (Brusca, 1980) down to San Juan de Alima, Michoacan, Mexico (Espinosa-Pérez & Hendrickx, 2001). P. sculpta has been introduced to many localities in the world including Hawaii (Miller, 1968), Brazil (Pires, 1980; Loyola et al., 1999), Cadiz, Spain, Europe (Rodriguez et al., 1992), Gibraltar (Castelló & Carballo, 2001); Venice, Italy, Mediterranean (Forniz & Maggiore, 1985; Forniz & Sconfietti, 1985) Queensland, Australia (Harrison & Holdich, 1982; Hewitt & Campbell, 2001), Hong Kong, China (Bruce, 1990), Osaka Bay, Japan (Ariyama & Otani, 2004), Arabian Sea, Pakistan (Yasmeen & Yousuf, 2006) and Greece (Fryganiotis & Chintoroglou, 2014) (see fig. 4 for world map distribution). The most recent report is for the Macaronesia biogeographic region of Azores Archipelago (Portugal) for the island of São Miguel (Marchini et al., 2017). In this latter study 29 specimens (8 males, 16 females and 5 juveniles) of P. sculpta were collected in 2014 and only α-males morphs were captured. Our study also reports the finding of only α-males specimens with average body lengths of 5.3 mm, these specimens being slightly smaller than the one reported for the Azores with 6.9 mm (Marchini et al., 2017, fig. 2a). However, both studies confirm the absence of the two smaller morphs (β- and γ-males) most likely because these have a shorter lifespan (Shuster & Wade, 1991) and consequently cannot survive longer voyages and reach to new colonizing regions.
Sphaeroma walkeri is a native species to the northern Indian Ocean where it was first described in 1905 from Sri Lanka based upon material examined by Thomas Stebbing collected in 1902 in the context of pearl oyster fisheries studies (Stebbing, 1905; Carlton & Iverson, 1981). This species was later recorded in the Arabian Sea, in the west of India as far north as Bombay and also in the east coast of India, Bay of Bengal (Pillai, 1955; Carlton & Iverson, 1981 and references therein). The earliest records of S. walkeri are for Port of Suez (Stebbing, 1910b), Suez Canal (Omer-Cooper, 1927; Monod, 1933) and in the Mediterranean for Israel (Glynn, 1972), Port Said and Alexandria, Egypt (Omer-Cooper, 1927; Larwood, 1940), where samples were collected from ship hulls dating back to 1924 and 1933, respectively. Consequently, it has spread throughout the Mediterranean as it was found in the Gulf of Izmir, Turkey in 1976 (Kocataş, 1978), Toulon, France in 1977 (Zibrowius, 1992), Alicante, Spain in 1981 (Jacobs, 1987), Port of Radès, Tunisia in 2003 (Ben Souissi et al., 2004), La Spezia harbour, Italy (Lodola et al., 2012). Additionally, it has been reported in many other locations of the world like Durban, South Africa (Stebbing, 1917), Australia (Baker, 1928), Brazil (Loyola e Silva, 1960; Pires, 1982; Loyola et al., 1999), Florida (Miller, 1968), San Diego Bay, CA (Carlton & Iverson, 1981) and Hawaii (Miller, 1968) (see fig. 5 for world map distribution). The present finding constitutes the first record of this non-indigenous species for the NW Atlantic region. In fact, the review from Carlton & Iverson (1981) effectively explains and summarizes the worldwide distribution of S. walkeri and its possible routes of dispersal from its Indian Ocean origin, throughout the Gulf of Suez, Mediterranean, Australia, South Africa, Brazil, Puerto Rico, Florida, Hawaii and California that was greatly facilitated through shipping across the oceans (see table 2 and fig. 2 in Carlton & Iverson, 1981).
As for this study, the most likely vector for the introduction of both isopod species in Madeiran waters is “shipping” through hull fouling on recreational vessels an hypothesis also supported by other studies (Hewitt & Campbell, 2001; Galil, 2008) including the recent finding of P. sculpta in the Azores (Marchini et al., 2017). The occurrence of both species inside the marina Funchal is not surprising, since marinas are considered to be “hotspots” for NIS settlement due to high levels of propagule pressure and are therefore considered ideal study sites for rapid NIS detecting surveys (Arenas et al., 2006; Minchin, 2012).
The two isopod species reported here occurred cohabiting with other non-indigenous fouling bryozoans, such as Amathia verticillata (delle Chiaje, 1882), Bugula neritina (Linnaeus, 1758), Bugulina simplex (Hincks, 1886), Cradoscrupocellaria bertholletii (Audouin, 1826) and Schizoporella pungens Canu & Bassler, 1928, in a salinity range from 35-36 psu, while sea surface temperature in Funchal Bay ranges from 17 to 22.5°C over the year (Alves et al., 2001). According to the information taken from the questionnaire given to the foreign yacht owner, the vessel in question was a British yacht from Guernsey, UK. It appears that the last journeys made by this vessel were Algarve in the south of Portugal, Morocco, Canary islands: Lanzarote, Gran Canary and lastly La Gomera, before arriving to the marina of Quinta do Lorde, Caniçal, Madeira Island on October 2015 (see fig. 6 for map-diagram of this journey). More important, the last dry-dock used was in Gran Canaria Island in June 2015 from which the actual antifouling paint was renewed. Furthermore, with only four months passed since the last renewal, we noticed that this antifouling coating was in decent conditions, yet still, we found other fouling taxa groups (i.e., polychaetes, bryozoans, platyhelminthes and crustaceans) throughout the hull area. Amongst these were the isopod S. walkeri, known to be one of the most widely ship-transported species in the world (Galil, 2008). Thus, it is difficult to determine where exactly S. walkeri was “picked up” from either the last journeys made from the Canary Islands or even from its last mooring at Quinta do Lorde marina from where it was docked for six days, before going to the DDI on 3 November 2015. Interestingly, S. walkeri has not been reported (yet) from any of the localities above (compare with fig. 6). However, we do not exclude the fact that these species could have already been established in other marinas along the south coast of Madeira Island, as domestic voyages often contribute to the spread of species amongst marinas. To date, we have not yet found or collected P. sculpta and S. walkeri in the neighbouring marinas in Madeira. Further monitoring programs should evaluate their spatial distribution and spread along the coastline of the island. Consequently, in our subsequent monitoring surveys we will be more alert for the presence and establishment status of P. sculpta and S. walkeri in adjacent marinas of Madeira and Porto Santo islands, beside the marina of Funchal. In parallel, research should also focus on evaluating their potential impact on resident ecosystem with the aim to understand the risk and relevance of non-indigenous species introduction process. Nevertheless, future studies should consider better methods to trap and collect more individuals of free swimming fauna like artificial sponges and/or PVC pipes as used in Shuster (1992) and/or Munguia & Shuster (2013) respectively, instead of plain settling plates which are not ideal to collect a fair number of mobile individuals and do not offer refuge from predators.
We wish to thank the administration of all marinas (Porto Recreio da Calheta, Marina do Funchal, Marina da Quinta do Lorde, and Marina do Porto Santo) and also RepMarítima for allowing us to survey NIS diversity along the south coast of Madeira archipelago since 2013 to present date. P. Ramalhosa was partially funded by the Project Observatório Oceânico da Madeira-OOM (M1420-01-0145-FEDER-000001), co-financed by the Madeira Regional Operational Programme (Madeira 14-20), under the Portugal 2020 strategy, through the European Regional Development Fund (ERDF). I. Gestoso was supported by a postdoctoral grant in the framework of the 2015 ARDITI Grant Programme Madeira 14-20 (Project 002458/2015/132). J. Canning-Clode was supported by a starting grant in the framework of the 2014 FCT Investigator Programme (IF/01606/2014/CP1230/CT0001). This study had the support of Fundação para a Ciência e Tecnologia (FCT), through the strategic project UID/MAR/04292/2013 granted to MARE. This work was partially funded by project MIMAR (MAC/ 4.6.d/066) INTERREG MAC 2014-2020 Programme.
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