(Mollusca, Vermetidae) to the Brazilian coast.

Recent introduction of non-indigenous vermetid species (Mollusca, Vermetidae) to the Brazilian coast. Paula Spotorno-Oliveira, Ricardo Coutinho & Frederico Tapajós de Souza Tâmega Marine Biodiversity ISSN 1867-1616 Mar Biodiv DOI 10.1007/s12526-017-0702-7

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Author's personal copy Mar Biodiv DOI 10.1007/s12526-017-0702-7

ORIGINAL PAPER

Recent introduction of non-indigenous vermetid species (Mollusca, Vermetidae) to the Brazilian coast. Paula Spotorno-Oliveira 1 & Ricardo Coutinho 1 & Frederico Tapajós de Souza Tâmega

1,2

Received: 10 June 2016 / Revised: 20 March 2017 / Accepted: 5 April 2017 # Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017

Abstract The present study describes the bioinvasion of the vermetid gastropod Eualetes tulipa of the Brazilian coast. The species was first reported in the Pacific Ocean, off the coast of Panama (since the 1840s); however, the type locality was not specified in the original species description. Since then, E. tulipa has been introduced to Hawaii, the Caribbean Sea, southeastern Florida and India. In Brazil, the first documented occurrence was in 2005, at Ceará State, northeast Brazil, and later in 2009 it was registered at Rio de Janeiro State, southeast Brazil, 3000 km from the previous location. Nowadays, they are not only found growing on artificial substrates but also along sandstone fringing reefs and rocky reefs coexisting with the native species Petaloconchus varians. The impact on the native benthic community is unknown; however, studies have suggested impacts such as competing for space with fouling communities (E. tulipa, Venezuela), and causing deleterious effects on corals (Ceraesignum maximum, French Polynesia). The possibility of spread through Brazilian endemic areas (e.g. Abrolhos Marine National Park), is a legitimate cause for concern as a result of oil industry shipping further distributing this non-indigenous species. E. tulipa has a continuous year-long reproduction and fast settlement, within 24 h of hatching. This reproductive mode allows for the highly successful invasion and establishment to new areas following Communicated by V. Urgorri * Frederico Tapajós de Souza Tâmega [email protected] 1

Departamento de Biotecnologia Marinha, Instituto de Estudos do Mar Almirante Paulo Moreira, Rua Kioto, n° 253, Praia dos Anjos, Arraial do Cabo, Rio de Janeiro 28930-000, Brazil

2

Laboratório de Geologia e Paleontologia, Instituto de Oceanografia, Universidade Federal do Rio Grande, Av. Itália Km 8, Rio Grande, Rio Grande do Sul 96203-900, Brazil

maritime transport or natural rafting, predicting a rapidly widespread distribution and invasion of Brazilian and International waters. Keywords Vermetidae . Eualetes tulipa . Introduction . Bioinvasion . Brazilian coast

Introduction Eualetes tulipa (Rousseau in Chenu 1843) is a large vermetid gastropod that inhabits shallow waters in warm temperate and tropical seas. The species was originally described as Vermetus tulipa by Chenu (1843-1845) and no type locality was stated in the original description. Due to the type specimen being lost, the species was placed in a different genus, Trypsicha (Eualetes) tulipa, by Keen (1971a) after comparing illustrations of type material matched with specimens from Panama Bay. However, the first record in Panama was based on the assumed synonym Vermetus panamensis Rosseau in Chenu, 1844 (Bieler 2015). Although the type locality of V. panamensis was not stated, one might assume that the species had been known in the Panama region since the 1840s, by nominal inference (Bieler and Petit 2011: 51). E. tulipa has been registered in Verra Cruz (Hughes 1985), and also in Veraguas Province (Vega and González 2002), both in the Panama area, east Pacific Ocean. Vermetus alii Hadfield and Kay was described in 1972 (Hadfield et al. 1972) as a species thought to be native to the Hawaiian Islands. Because of the likely Panamic origin of this species, V. alii became tagged as a potential invasive in Hawaiian waters (Bieler in Carlton 1999: 449), and the name was eventually replaced by E. tulipa in both the western Atlantic (e.g., Miloslavich 1996; Miloslavich et al. 2010) and Hawaiian (e.g., Coles and Eldredge 2002; Coles et al.

Author's personal copy Mar Biodiv

2006) literature. After realizing that the synonymy was widely accepted but never formally justified, Golding et al. (2014) considered V. alii Hadfield and Kay 1972 (Hadfield et al. 1972) from Hawaii and Vermetus sp. (Miloslavich and Penchaszadeh 1992) from Venezuela, as synonymy to E. tulipa, based on detailed morphological and molecular comparisons. In Hawaii, E. tulipa has been reported as a non-indigenous, introduced species in 32 localities including Kane‘ohe Bay, Hilo Harbour, O’ahu Waikiki and O’ahu Honolulu (as V. alii, Hadfield et al. 1972; Coles and Eldredge 2002). In these locations, individuals were mainly found attached to both artificial (e.g., concrete pilings and walls, metal and wood) and natural substrates (e.g., reefs and mangrove roots) (Coles and Eldredge 2002; Coles et al. 2002; Schluker 2003; Carlton and Eldredge 2009). In the Venezuelan Caribbean, this species (as Vermetus sp.; Miloslavich and Penchaszadeh 1992) has been observed in the central west coast near Puerto Cabello colonizing the walls of a intake-cooling sea water channel of a thermoelectric power plant (Miloslavich and Penchaszadeh 1992); on the concrete pilings at the deck of El Palito oil refinery; and also on the metal remains of a World War II shipwreck (BSesostris^) at Isla Larga (Miloslavich and Penchaszadeh 1992; Osman and Shirley 2007). The species has been registered in southeastern Florida based on museum records (FMNH 318223) at Peanut Island, Palm Beach County (Rawlings et al. 2010; Golding et al. 2014). Other Florida records are at Port Canaveral, Brevard County, Fort Pierce Inlet, St. Lucie County (R. Bieler, personal communication) and at Phil Foster Park, Riviera Beach (C. Marshall, personal communication). Cortés (2012) recorded the species occurrence in Isla Del Coco National Park, an oceanic island in the Eastern Tropical Pacific of Costa Rica. On the southeast coast of India (Bay of Bengal), in the northeastern part of the Indian Ocean, E. tulipa has recently been registered in the Royapuram fishing harbour, located near the port of Chennai, on submerged boulders of a breakwater at depths of 0.5–1.0 m (Jebakumar et al. 2015). As the knowledge of the distribution of this species is scarce, the present study aims to describe the bioinvasion of the vermetid gastropod E. tulipa of the Brazilian coast. In addition, this is the first report describing the arrival of the species in 2005 in the Central and South Atlantic Ocean and consequent spread along the coastline, providing some morphological and ecological accounts of the species and notes on its invasive behaviour.

Material and methods The specimens described in this study were based on 21 lots deposited in museum collections, 3 new samplings deposited

in the IEAPM collection, and four additional collections not catalogued/deposited in the following locations along the Brazilian coast, from northeast to southeast Brazil (Table 1; Fig. 1). The voucher material was deposited in seven Brazilian Institutions. For detailed examination, the shell, radulae and operculum of E tulipa (MORG49597 and IEAPM1001) were observed using a scanning electron microscope (SEM). Institutional abbreviations CMPHRM – A: Coleção Malacológica Prof. Henry Ramos Matthews - Série A, Universidade Federal do Ceará (UFC), Brazil; CMPHRM – B: Coleção Malacológica Prof. Henry Ramos Matthews Série B, Universidade Federal do Ceará (UFC), Brazil; IEAPM: Marinha do Brasil, Instituto de Estudos do Mar Almirante Paulo Moreira (IEAPM), Brazil; LABIPE: Laboratório de Biologia Pesqueira, Departamento de Oceanografia e Limnologia, Universidade Federal do Rio Grande do Norte (UFRN), Brazil; MORG: Museu Oceanográfico Prof. Eliézer de Carvalho Rios, Universidade Federal do Rio Grande (FURG), Brazil; MNRJ: Museu Nacional, Universidade Federal do Rio de Janeiro (UFRJ), Brazil; MZSP: Museu de Zoologia da Universidade de São Paulo (USP), Brazil.

Results and discussion Systematics Class Gastropoda Cuvier 1795 Order Littorinimorpha Golikov and Starobogatov 1975 Family Vermetidae Rafinesque 1815 Genus Eualetes Keen 1971 Eualetes tulipa (Rousseau in Chenu 1843) Figures 2, 3, 4, 5 Description Shell. Protoconch (Fig. 2a): Globose and inflated, with one and a half whorls, buried by the teleoconch whorls. Mean length 1 mm, globular apex, aperture circular. The suture between the first and second whorl thickened. Teleoconch (Figs. 2b−f, 3a, b): Relatively mediumlarge size, sturdy, with about 6–10 whorls laterally piled up, extending to one side, growth flat to the surface; mean length 37.74 mm (range 15–57 mm). Tube margins compressed to the substrate, non-circular. Emergent tube (or feeding tube) range 9–30 mm. Feeding tube scars, i.e., remnants of earlier feeding tubes, present. Aperture with a mean diameter of 9.03 mm (range 5.22–14.07 mm), compressed to the substrate (planar growth) or circular (generally projecting above its own teleoconch, sometimes slightly erect). Early post-larval

Author's personal copy Mar Biodiv Table 1 Region

Data of the specimens studied along the Brazilian coast (see Fig. 1 for site locations) Site

Northeast Fortaleza, Ceará State, Brazil (NE) Port oAmarante (Fig. 1a)

Fortaleza, Ceará State, Mucuripe Port (Fig. 1b)

Coordinates

Date

03°31′53.3″S, i − iii/2005 38°47′36.6″W i/2009

Depth Range Substrate (m)

Museum deposit number

1–16

A (port pillar)

a

1

A (port pillar)

CMPHRM4001A

i/2009 i/2009

2 3

A (port pillar) A (port pillar)

CMPHRM4002A CMPHRM4003A

i/2009

4

A (port pillar)

CMPHRM4004A

i/2009 29/v/2009

5 15


CMPHRM4005A CMPHRM4816B

13/x/2010

5–8

MORG49597

13/x/2010

5–8

2011 2011

3 2

A (recruitment panels - port pillar) A (recruitment panels port pillar) A (port pillar) A (port pillar)

3m 3


MORG52487 MORG52489

12–16/ii/2009 1 ii/2009 1 ii/2009 2

A (port pillar) A (port pillar) A (port pillar)

MORG52488 CMPHRM3996A CMPHRM3997A

ii/2009 ii/2009


CMPHRM3998A CMPHRM3999A

03°41′58.5″S, 2–5/ii/2009 38°28′54.8″W 2–5/ii/2009

3 4

ii/2009 06°00′25.2″S, 25/v/2016 Natal, Rio Grande do Norte 35°06′23.6″W State, Nísia Floresta, Ponta de Ilha Verde Reefs (Fig. 1c) Southeast Arraial do Cabo, Rio de Janeiro 22°58′19.7″S, vii/2009 Brazil (SE) State, Forno Port (Fig. 1d) 42°00′49.5″W 20/vii/2011 2013 13/ii/2017 22°58′44.4″S, 20/viii/2015 Arraial do Cabo, Rio de 42°00′55.1″W 16/v/2016 Janeiro State, Anjos Beach (Fig. 1e)

5 A (port pillar) Intertidal N rock pools 5 2–8 2–8 Intertidal 1–2 5

A (buoy hull) A (port pillar) A (breakwater) A (breakwater) N (rocky reefs) N (rocky reefs)

CMPHRM3221B MZSP 107786 MZSP 107787

CMPHRM4000A a

a

MNRJ19373 a

IEAPM1773 IEAPM930 IEAPM1001

A Artificial, N natural a

specimens not deposited

sculpture of axial growth lines, and subsequent sculpture with longitudinal ribs, producing a slightly reticulated appearance, especially along the top of the shells; reddish-brown to greyish coloration, darker at the top, lightening along the sides, creamy-white along the bottom edge. Head-foot (Fig. 4a, b): Head greatly protruding, approximately half of foot length. Snout large and cylindrical, as an extension of the head. Mouth ample, semicircle shape, with a horizontal slit in anterior-ventral snout region. Cephalic tentacles emerging laterally from snout base, sturdy and cylindrical, longer than snout. Eyes small, black, immersed in ventral-basal region of tentacles. Dorsal region containing a pair of well-

developed pedal tentacles, extending beyond the foot, and dorsoventrally flat propodial pad. Columellar muscle well developed and robust, and occupying approximately 40–50% of total body length. Head-foot overall burgundy or red wine in colour; mouth, the cephalic and pedal tentacles darkened; light yellow spots around the mouth and on the cephalic tentacles. Operculum (Fig. 4a−c): thin, shallowly concave, corneous and bright, with an internal spiral keel of 1.5 coils, smooth downward. Average diameter of 5.11 mm (range 3–6.85 mm), approximately 60% of the aperture diameter, slightly overlapping the dorsal surface of foot. Mantle organs (Fig. 4b): Mantle border thin and smooth, colour light orange. Pallial cavity about 1/3 of


Fig. 1 Study locations of Eualetes tulipa along the Brazilian coast: Ceará State, CE (a, b); Rio Grande do Norte State, RN (c); Rio de Janeiro State, RJ (d, e)

soft parts length. Visceral mass: Yellowish-white in colour. Adult average length of 86.67 mm (rang 60– 100 mm). Visceral mass occupying about 2/3 of total length, filling all available shell space up to posterior end. Posterior lobe of digestive gland long, occupying most of visceral mass, pale green to light brown. Posterior end forming slender tail, comprising gonadal tissue. Gonad along ventral surface of visceral mass, compressing digestive gland of about same length, yellowish-white, yellow or orange colour. Radula (Fig. 4d): Taenioglossate radula typical of Vermetidae, consisting of approximately 45 rows of seven teeth (a central one, a pair of lateral and two pairs of marginal teeth). Rachidian (central) tooth trapezoidal, with strong main cusp and six to eight additional cusps on each side. Lateral tooth with a stout main cusp and five to six cusps on each side. Marginal teeth similar to lateral, hook-like, long, slender, with a long and strong main cusp. Inner marginal tooth with up to three cusps on each side. Outer marginal tooth smooth, without cusp outside, and up to two inner cusps.

Brood protection and early ontogeny (Fig. 4e, f): Mantle border entire in brooding females, without longitudinal mantle slit, accommodating free spherical and elongated egg capsules inside. Egg capsules at different stages, containing discernible nurse eggs and developing veligers; all embryos in a given capsule are at the same stage of development. Broods comprised from 2 to 34 capsules interleaved. Average dimensions of capsules (stage IV, late veliger larvae) 5.04 mm in length (range 4.61–5.39 mm) and 3.39 mm in width (range 3.14–3.9 mm). Up to 277 small veligers within a single egg capsule (average of 213). Signs of abnormality (absence of shell coiling) were observed in some veligers. Juvenile shells with postmetamorphosis averages 0.43 mm in length (0.34–0.49); globose, translucent, about one and a half whorls, deeply marked brown suture, light-brown coloration. Soft parts light yellow colour with two black eyes like dark spots through shells. Habitat (Figs. 2f, 3a, b, 5a, b): Solitary specimens or groups can be found attached to artificial (monobuoys, breakwaters, pillars and offshore port) or natural (rocky reefs) substrates. The specimens are frequently found attached to vertical surfaces on rocky shores, associated with a diverse fauna.

Author's personal copy Mar Biodiv Fig. 2 Eualetes tulipa: settled protoconch (a) and initial whorls of teleoconch (b), IEAPM1001; entire shell, piled up whorls laterally extending to one side and detail of the emergent tube (ft), MORG49597 (c), MNRJ19373 (d); entire shell, lateral view (e), MORG49597; in situ surface sculpture of the teleoconch and colour pattern of a specimen from rocky reef at Arraial do Cabo, Southeast Brazil (f). Scale bars (a, c–f) 1 cm; (b) 100 μm. ft feeding tube

The associated fauna registered include: the native vermetid Petaloconchus varians (d’Orbigny 1839); the oyster Crassostrea brasiliana (Lamarck 1819); the mussel Perna perna (Linnaeus 1758); the invasive bivalves Isognomon bicolor (C. B. Adams 1845) and Myoforceps aristatus (Dillwyn 1817); the ascidian Didemnum sp.; the sponge

Darwinella sp.; the balanid Tetraclita stalactifera (Lamarck 1818); the sea urchin Paracentrotus gaimardi (Blainville 1825); the corals Millepora alcicornis Linnaeus 1758; Palythoa caribaeorum (Duchassaing and Michelotti 1860); the invasive encrusting bryozoan Schizoporella errata (Waters 1878); crustose coralline algae; the sea anemone

Fig. 3 Eualetes tulipa: in situ detail of shell aperture compressed to the substrate in planar growth (a) and circular, projecting above the teleoconch (b) of specimens from rocky reefs of Arraial do Cabo, Southeast Brazil. Scale bars 1 cm. ap aperture

Author's personal copy Mar Biodiv Fig. 4 Eualetes tulipa: headfoot, detail of anterior region (a), animal removed from the shell, headfoot, detail of anterior region, lateral-left view (b), IEAPM930; operculum, SEM, external view (c), radula, SEM (d), MORG49597; two spherical and one elongated egg capsules at different stages, detail of developing veligers (ve) (e), IEAPM1001; shells of intracapsular juveniles, after metamorphosis (f, MORG49597. Scale bars (a, b) 1 cm; (c, e, f) 1 mm; (d) 100 μm. ct cephalic tentacles, he head, mb mantle border, mo mouth, op, operculum, pp propodial pad, sn snout. Photo credits: Luís Felipe Skinner (a)

Bunodosoma caissarum Corrêa in Belém, 1987; the algae Colpomenia sinuosa (Mertens ex Roth) Derbès and Solier; Spiridia sp., Codium intertextum Collins and Hervey; Codium spongiosum Harvey, and others. Population densities of E. tulipa were estimated as follows: up to 24 specimens per 100 cm−2 attached to artificial substrate (Arraial do Cabo,

breakwater of Forno Port) and up to 10 specimens per 100 cm−2 attached to natural substrate (Arraial do Cabo, rocky reefs at Anjos Beach). Distribution: From the intertidal to 16 m depth. Occurring from the northeast coast (Ceará State) to the southeast coast of Brazil (Rio de Janeiro State).

Fig. 5 Eualetes tulipa: in situ detail of a monospecific group of specimens (a) and association with the native vermetid Petaloconchus varians (b) from rocky reefs of Arraial do Cabo, southeast Brazil. Scale bars (a) 5 cm; (b) 1 cm. eu E. tulipa, pe P. varians


Taxonomic remarks E. tulipa registered from the Brazilian coast shows similarities to specimens from the Pacific, Caribbean and Indian Oceans. There were no available data on specimens from the Eastern Tropical Pacific (Costa Rica). However, in Panama Bay and the Caribbean, the shells attain a maximum length of 60 and 70 mm, respectively, which is slightly larger than the specimens recorded from the Brazilian coast (mean length 34.74 mm, range 15–57 mm). The Hawaiian specimens (as Vermetus alii Hadfield and Kay in Hadfield et al. 1972) had the same shell sculpture, similar length (up to 35 mm) and aperture diameter (8 mm). The Brazilian specimens also share a similar maximum aperture diameter (14.07 mm) with the Panama Bay (16 mm; Keen 1971b) and Caribbean specimens (12 mm; Miloslavich and Penchaszadeh 1992). The same comparison was observed for the operculum diameter: Indian, Caribbean and Brazilian specimens had the same operculum diameter (mean 5 mm; Miloslavich and Penchaszadeh 1992; Jebakumar et al. 2015; present study). Another remarkable feature of the shell of E. tulipa from the Brazilian coast is the emergent tube (or feeding tube) which ranges from 9 to 30 mm, in comparison to the Caribbean specimens in which it ranges from 10 to 120 mm in length (Miloslavich and Penchaszadeh 1992). However, a noticeable difference among the Indian, Caribbean and Brazilian specimens is the respective measurements of the elongated body. Although they have the same red-wine colour in the head-foot, the maximum body length recorded in the Caribbean was 141 mm (Miloslavich and Penchaszadeh 1992), in comparison to 100 mm in Brazilian specimens and 72 mm in Indian specimens (Jebakumar et al. 2015). The head-foot coloration is the same as registered by Hadfield et al. (1972) for the Hawaiian specimens, and Miloslavich and Penchaszadeh (1992) for Caribbean specimens, highlighting the same light spots also detected in Brazilian specimens. Regarding brood protection, females of E. tulipa can brood their egg capsules freely inside the mantle cavity. Each capsule contains the same stage of embryo development; however, the stages of development vary between capsules, evidence of a continuous reproduction (Hadfield 1989; Miloslavich and Penchaszadeh 1992; Phillips and Shima 2009). The number of egg capsules brooded per E. tulipa females as well as the number of embryos per capsule may be related to female size, as the Brazilian specimens seem to brood fewer eggs capsules (between 2 and 34), when compared to Caribbean (up to 54; Miloslavich and Penchaszadeh 1992) and Hawaiian specimens (up to 50; Hadfield et al. 1972). Despite E. tulipa from Brazil producing apparently fewer egg capsules, these capsules in stage IV (late veliger larvae) are larger in length

(5.04 mm; present study) than the Caribbean specimens (3.42 mm; Miloslavich and Penchaszadeh 1992), while Brazilian specimens produce up to 277 small veligers within a single egg capsule versus 80–200 (Hawaii) and 188 (Caribbean). However, the reproductive cycle and embryonic development of E. tulipa from Brazil are currently under study. Several physical factors (water temperature, salinity, water pollution, maternal size and condition at reproduction) have been investigated for their correlation with egg size in an attempt to understand the various effects of the environment on per offspring investment (Thatje and Hall 2016). In this context, temperature-driven latitudinal shifts in energy provisioning to eggs has long been suggested for several mollusks (Thorson 1950; Hadfield 1989; Honkoop and Van Der Meer 1998; Collin and Salazar 2010). Therefore, one might suggest that temperature (see discussion below) may dictate E. tulipa egg size with a production of smaller eggs/less embryos or bigger eggs/more embryos, depending on the geographic region. The absence of shell coiling in some of the veligers registered by Miloslavich and Penchaszadeh (1992) was also observed in the Brazilian specimens (present study) with normal structures. E. tulipa have obligatory planktonic phases (Hadfield et al. 1972), and the positively phototropic veliger larva settles within 24 h (Miloslavich and Penchaszadeh 1992). The feeding method of Brazilian specimens presents a number of unusual features when compared to Hawaiian specimens. According to Hadfield et al. (1972), E. tulipa feeds mainly by means of cilia on the ctenidial filaments, as opposed to the other Hawaiian species which feed by mucous web. In contrast, specimens from Panama Bay (Hughes 1985) and Brazil (present study) confirm the mucous web feeding behaviour by E. tulipa. Similarity in feeding behaviour among species of genera Eualetes, Dendropoma and Thylacodes indicates that trapping of particles by a mucous web is the major method of obtaining food in all vermetids (Hughes 1985). According to Hughes (1985), the branchial filtering by vermetids is an auxiliary method of capturing food particles, most of which are trapped in the mucous web spun by the pedal tentacles. Species introduction and distribution along the Brazilian coast E. tulipa was first reported in the Pacific Ocean, off the coast of Panama (since the 1840s) and later in Costa Rica (1992). Since then, E. tulipa has been reported as a non-indigenous, introduced species to Hawaii, the Caribbean Sea, southeastern Florida, southeast India andthe Brazilian coast (Fig. 6). In Brazil, the first documented occurrence was in January 2005, at the offshore Port of Pecém (03°31′53.3″S, 38°47′ 36.6″W), Ceará, (NE), and later in February 2009 in


Fig. 6 Updated distribution map of Eualetes tulipa: (1) Panama, 1971; (2) Hawaii, 1972; (3) Venezuelan Caribbean, 1986; (4) southeastern Florida; (5) Costa Rica, 2012; (6) India, 2015. Species introduction

along the Brazilian coast: (7) Ceará State (NE), 2005 and 2008; (8) Rio Grande do Norte State (NE), 2016; (9) Rio de Janeiro State (SE), 2009

Mucuripe Port (03°41′58.5″S, 38°28′54.8″W), approximately 80 km from the previous location (Fig. 6). They remained colonizing this region, being collected from annual recruitment panels placed at the Port of Pecém, from October 2009 to November 2011 (Rabay et al. 2012). In the State of Ceará (NE), a number of surveys of benthic macroinvertebrates associated with port terminal structures have been performed (Monteiro 2003; Franklin-Junior et al. 2005; Mota 2006; Bezerra 2010). Miranda et al. (2013) listed the occurrence and distribution of 7 species of marine benthic invertebrates introduced to the coast of the State of Ceará, including the marine jetty of Port of Pecém. Previous studies had only reported the native vermetid species Petaloconchus varians in that region (Furtado-Ogawa 1970; SpotornoOliveira, personal observation). Recently (May 2016), in the same region (NE), specimens were detected living on rock pools in the sandstone fringing reefs at Ponta de Ilha Verde Reefs (06°00′25.2″S, 35°06′23.6″ W), Natal, Rio Grande do Norte State, 600 km from the previous location. Although the main occurrence area of sandstone reefs in Brazil is in the Northeast State, the knowledge of molluscan fauna, composition and distribution in the sandstone fringing reefs are scarce (Matthews 1967; Matthews and Rios 1969, 1974; Furtado-Ogawa 1970; Oliveira 1971; Matthews-Cascon et al. 1989; Martinez et al. 2012). Oliveira (1971) registered the vermetid Petaloconchus cf. varians as commonly distributed along the sandstone fringing reefs at Natal, Rio Grande do Norte State (NE), whereas Martinez et al. (2012) recorded unidentified Vermetidae specimens in the reef habitat of Maracajaú sandstone reef, a Coral Reef Protected Area (APARC), located 7 km away from the

Maracajaú beach, Maxaranguape City, in the State of Rio Grande do Norte (NE). In March 2009, a population of E. tulipa was detected encrusting an oil company monobuoy at the Forno Port (22°58′19.7″S, 42°00′49.5″W), Arraial do Cabo (SE), 3000 km from the initial location (Port of Pecém, Ceará, NE) (Fig. 6). This region has unique features regarding its marine ecosystems—an upwelling area that exposes the rocky shores with cold water, enriching primary production and consequently the local food web, and may also be considered a hot spot for biodiversity conservation (Ferreira et al. 2006). Arraial do Cabo has unique features related to its marine environment, being a Marine Extractive Reserve (RESEXMAR Arraial do Cabo) since 1997. In this region, many nonindigenous species have been detected since the 2000s (Ferreira et al. 2006; López et al. 2010, 2014), and many of these introductions have been associated with the increase in ship traffic to Forno Port. This harbour previously contained operations related to salt transfer to Rio Grande do Norte state, on the northeast coast of Brazil. Since the late 1990s, support activities for the oil industry, ship traffic and the number of platforms have increased in this region. In 2009, the Forno Port received only 0.02% of the total annual shipping tonnage of all Brazilian ports, increasing to 0.4% in 2010 (ANTAQ 2016). Nowadays, E. tulipa are not only situated in the Forno Port but also along the rocky reefs of Anjos Beach, coexisting with the native species (P. varians) (Fig. b5). In the Caribbean (Planta Centro power plant channel), E. tulipa also cohabits with two morphotypes of genus Petaloconchus, and their shells form dense multispecies colonies (Weinberger et al. 2010).


The impact on the native benthic community is unknown (in both northeast and southeast Brazil), and there is limited knowledge on the distribution of this species in other locations along the Brazilian coast. However, studies have suggested impacts such as competing for space with fouling communities (E. tulipa, Venezuela; Losada et al. 1988; Miloslavich et al. 2010), and deleterious effects on corals (Ceraesignum maximum (G.B. Sowerby I 1825), French Polynesia; Shima et al. 2013). Miloslavich et al. (2010) observed that the increase in the abundance of E. tulipa in the Venezuela coast, which has more than doubled in the last 20 years, may be related to an increase in organic suspended matter or nutrient supply (Birkeland 1977, 1987). This is mainly due to human activities including discharge of untreated wastewater and sediment from upstream and coastal sources (Penchaszadeh et al. 2000). As a result of urban growth in Arraial do Cabo (SE), an outfall was built which discharges a combination of municipal wastewater, storm water, and sewer overflows into the centre of the Arraial do Cabo Bay at the Anjos Beach (Coelho-Souza et al. 2013). This may act as a potential source of nutrient overload to the marine environment where a population of E.tulipa has been observed (since 2009, present study). According to Rogers et al. (2014), shipping traffic to the local harbour can also be a prospective source of sediment resuspension for the nearby rocky reefs of Anjos Beach. Additionally, the introduction of one species to a new habitat is a risk to the environment, as free of predators, parasites and natural competitors and, in a good environmental conditions, these organisms can reach high-density populations (Carlton 1996). Little is known about the Brazilian vermetids ecology, particularly their interactions with predators. The possibility of spread through Brazilian endemic areas (e.g. Abrolhos Marine National Park, the south Atlantic largest coral reef complex), is a legitimate cause for concern as a result of oil industry shipping further distributing this nonindigenous species. E. tulipa has continuous year-long reproduction and fast settlement, within 24 h of hatching (Miloslavich and Penchaszadeh 1992). This reproductive mode allows for the highly successful invasion and establishment to new areas following maritime transport or natural rafting, predicting a rapid widespread distribution and invasion of Brazilian and International waters. Furthermore, the fact that the same female may brood egg capsules at different stages of development (present study) indicates that these species has continuous spawning, also confirmed by Miloslavich et al. (2010) for the Venezuelan Caribbean specimens. Vermetids are considered of great interest because they possess traits that confer a high potential for invasion (Bieler 1995; Strathmann and Strathmann 2006). Besides their high tolerance of adverse conditions such as lack of food and turbid water (Schiaparelli and Cattaneo-Vietti 1999; Strathmann and Strathmann 2006), they also have the ability to attach to

different natural (to other organisms such as barnacles and oysters) and artificial substrates (ship hulls, oil platforms, anthropogenic floating marine debris) (Miloslavich and Penchaszadeh 1992; Bieler 1996; Schiaparelli et al. 2002; Breves and Skinner 2014). For these reasons, it has been proposed that they can passively travel long distances as fouling attached to ships and vessels, providing subsequent establishment of populations (Bieler 1996; Strathmann and Strathmann 2006; Molnar et al. 2008). Although vermetids do not normally settle on wood, they attach to organisms that do, such as barnacles and oysters (Bieler 1995). In the case of the Arraial do Cabo area (SE), specimens of E. tulipa are dispersing from the Forno Port and arriving at the rocky reefs of Arraial do Cabo Bay probably by Brafting^ or similar means of transport, attached to natural or artificial substrates, like marine debris or pieces of wood, which are commonly found floating in this area. Nevertheless, the possibility of natural dispersion of larvae (within 24 h) is not discarded. E. tulipa was reported in Brazil at depths of up to 16 m, attached to natural and artificial substrates, while specimens from the Caribbean range from 0 to 5 m depth, attached to submerged artificial substrates (Miloslavich and Penchaszadeh 1992). Beyond this batimetric difference, the species also seems to tolerate wider temperatures limits, inhabiting different water temperatures conditions along the Brazilian coast. While in northeast Brazil the average temperature is 28.4 °C, along the southeast coast, the marine systems in the Cabo Frio region (Arraial do Cabo, RJ) are subject to an annual upwelling season with the lowest temperatures ranging from 18 to 12 °C at certain sites (Valentin et al. 1987; Carbonel 1998), although the mean water temperature at Arraial do Cabo Bay is 22.5 °C (Guimaraens and Coutinho 2000). According to Hughes (1985) and Miloslavich and Penchaszadeh (1992), E. tulipa from the previous records inhabits warmer water temperatures like those in the Venezuelan Caribbean, and the coasts of India, Costa Rica and Hawaii where temperatures vary from 26 to 30 °C. Based on the present records along the Brazilian coast, we conclude that E. tulipa represents a recent introduction of a non-indigenous vermetid species to the Brazilian coast. However, further studies are needed to understand the impact to the native benthic community, interactions with predators and dispersal processes from this region. Acknowledgements We are grateful to the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro-FAPERJ and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES for providing post-doc fellowships (PSO and FTST); the Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq for providing the productivity fellowship (RC) and the Instituto Chico Mendes de Conservação da Biodiversidade for research licence SISBIO no 44575– 3. We thank the Instituto de Estudos do Mar Almirante Paulo MoreiraIEAPM for field and laboratory support. We are also grateful to Cristina

Author's personal copy Mar Biodiv de Almeida Rocha-Barreira (CMPHRM – A), Helena Matthews Cascon and Cristiane Xerez Barroso (CMPHRM – B), Sérgio Mendonça Almeida and Luiz Ricardo L. Simone (MZSP), Luís Felipe Skinner (UERJ), Sula Salani Mota (MNRJ), Alina Rocha Pires Barboza and Tatiana Leite (LABECE, UFRN) for kindly assisting with the examined material in this study; to Daniel Souza dos Santos for the artwork in Fig. 1, to Gabriela Perna for kindly reviewing the English version; to Rudiger Bieler, an anonymous reviewer and the associated editor Victoriano Urgorri for improving this paper with useful comments. Rudmar Krumreick and Caroline Ruas (Centro de Microscopia Eletrônica do Sul, CEME-SUL, Universidade Federal do Rio Grande, FURG) are thanked for the SEM images.

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