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The Non-Indigenous Bryozoan Triphyllozoon (Cheilostomata: Phidoloporidae) in the Atlantic: Morphology and Dispersion on the Brazilian Coast

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The Non-Indigenous Bryozoan Triphyllozoon (Cheilostomata: Phidoloporidae) in the Atlantic: Morphology and Dispersion on the Brazilian Coast ZOOLOGIA 32 (6): 476–484, December 2015 http://dx.doi.org/10.1590/S1984-46702015000600007 The non-indigenous bryozoan Triphyllozoon (Cheilostomata: Phidoloporidae) in the Atlantic: morphology and dispersion on the Brazilian coast Ana C.S. Almeida1,2,*, Facelucia B.C. Souza2, Dennis P. Gordon3 & Leandro M. Vieira1 1Laboratório de Estudos de Bryozoa, Departamento de Zoologia, Centro de Ciências Biológicas, Universidade Federal de Pernambuco. 50670-810 Recife, PE, Brazil. 2Museu de Zoologia, Universidade Federal da Bahia. 40170-290 Salvador, BA, Brazil. 3National Institute of Water and Atmospheric Research. Private Bag 14901, Kilbirnie, Wellington, New Zealand. *Corresponding author. E-mail: [email protected] ABSTRACT. Bryozoans constitute an important component of marine-fouling communities of anthropogenic substrata. Many species have been reported as exotic or widespread around the world, typically in ports and harbors of non-polar regions. Here we present the first record of a species of the bryozoan Triphyllozoon in the Atlantic Ocean. Triphyllozoon arcuatum (MacGillivray, 1889), described originally from Australia, is reported herein from natural substrata in Singapore and natural and artificial substrata in Brazil. Although easily recognizable, the species has not been previously reported from anywhere else in the Atlantic. In the latter instance, the species was collected during monitoring of the invasive scleractinian corals Tubastraea spp. on an oil platform originally from Singapore and now located at Todos os Santos Bay, northeastern Brazil. Colonies of T. arcuatum were also found associated with three species of sponges, giving evidence that it is also growing in the natural environment. Todos os Santos Bay is characterized by intense commercial shipping traffic and oil exploration and the finding of T. arcuatum on an oil platform provides strong evidence that it represents a non-indigenous species in the Atlantic. Owing to the possible impact of T. arcuatum in Brazil, further studies and monitoring of its bioinvasion are recommended. KEY WORDS. Bioinvasion; Brazil; Bryozoa; invasive species; oil platform. Marine bioinvasions have increased significantly during make them relatively adaptable to large scale disturbances and the last 40 years (MCCANN et al. 2007, IGNACIO et al. 2010). This therefore likely to invade and become established in non-na- is in part a consequence of anthropogenic transport of species tive habitats (GORDON & MAWATARI 1992, MCCANN et al. 2007). to areas beyond their native habitats and natural home ranges, Some species have long been recognized as invasive, being re- mainly by ballast water and fouling of hulls of ships and oce- ported worldwide, such as the common marine-fouling Bugula anic platforms (MARINS et al. 2010, BUMBEER & ROCHA 2012). Ship- neritina (Linnaeus, 1758) and Amathia verticillata (Delle Chiaje, ping activities are recognized as the main source of species’ 1831) (MACKIE et al. 2006, FARRAPEIRA 2011, WAESCHENBACH et al. introductions in marine habitats (MACKIE et al. 2006, IGNACIO et 2015), among others. al. 2010, BUMBEER & ROCHA 2012), and in the Atlantic, the num- The phidoloporid bryozoan genus Triphyllozoon Canu & ber of non-indigenous marine fouling species is increasing, Bassler, 1917 is one of several genera that form erect lace-like especially in ports and harbors (MCCANN et al. 2007, MARINS et colonies and are popularly referred to as ‘lace bryozoans’. These al. 2010). colonies show different degrees of architectural complexity, and Among the fouling fauna, bryozoans are colonial sessile may be calyciform, or scrolled, or widely open (e.g., HARMER animals that live attached to any type of natural and artificial 1934, HAYWARD 1999, 2000, 2004) and, since many of them may substrata and constitute an important component of such as- also be highly colored, they can be quite conspicuous. semblages (GORDON & MAWATARI 1992, MCCANN et al. 2007), some- Triphyllozoon species are commonly associated with living sub- times with higher species diversity than other encrusting strata like corals, hydrozoans and algae (GORDON 1989, O’HARA organisms (MARQUES et al. 2013). These animals have a suite of 2001, PUCE et al. 2007, WINSTON 1986) as well as rock and suit- traits (e.g., fast-growing, tolerance of different substrata) that able artificial substrata (BOCK 1982). 2015 | Sociedade Brasileira de Zoologia | www.sbzoologia.org.br | www.scielo.br/zool All content of the journal, except where identified, is licensed under a Creative Commons attribution-type BY. The non-indigenous bryozoan Triphyllozoon in the Atlantic 477 Phidoloporidae is a large family, comprising 22 genera and 324 species in all oceans (HAYWARD 2004, BOCK & GORDON 2013), but the greatest diversity is found in the Coral Tri- angle (CANU & BASSLER 1929, HARMER 1934), the wider tropical Southwest Pacific (e.g., TILBROOK 2006), and the seas around Australia (HAYWARD 1999, 2000, 2004). Triphyllozoon comprises 32 species, having a tropical to temperate distribution in the Indian and Western Pacific Oceans (HARMER 1934, HAYWARD 1999, 2000, 2004), with a single species reported from the Red Sea (AMUI & KASELOWSKI 2006). Some 16 genera and 60 phidoloporid species occur in the Atlantic Ocean, of which at least 15 species are found in Brazilian waters, but the vast majority of these are encrusting species of the genera Fodinella Tilbrook, Hayward & Gordon, 2001, Plesiocleidochasma Soule, Soule & Chaney, 1991, Rhynchozoon Hincks, 1895, Schizotheca Hincks, 1877 and Stephanollona Duvergier, 1920 (VIEIRA et al. 2008, WINSTON & VIEIRA 2013, WINSTON et al. 2014). Recent stud- ies, however, have shown that the full diversity of bryozoans from the Brazilian coast is yet to be described (e.g., ALMEIDA & SOUZA 2014, RAMALHO et al. 2011, VIEIRA et al. 2010) and species of Phidoloporidae continue to be discovered (e.g., WINSTON & VIEIRA 2013, WINSTON et al. 2014). Recently, colonies of a species of Triphyllozoon were col- lected in northeastern Brazil. Although easily recognizable, it Figure 1. Distribution map of Triphyllozoon arcuatum in Brazilian has not been previously reported from either Brazil (VIEIRA et coast. Legends: PE, Pernambuco State; BA, Bahia State; CIPS, In- al. 2008) or anywhere else in the Atlantic (BOCK 2015) and we dustrial Port Complex of Suape; TSB, Todos os Santos Bay; IT, Ituberá. are confident that this finding represents the first record of the genus in the Atlantic Ocean. In this paper we present the first record of Triphyllozoon TAXONOMY arcuatum (MacGillivray, 1889) from Brazil, describing and com- paring specimens from this locality and from Singapore. Also we Triphyllozoon arcuatum (MacGillivray, 1889) discuss the supposed introduction of the species in the Atlantic. Figs. 2-17 MATERIAL AND METHODS Retepora monilifera form arcuata MacGillivray, 1889: 29 [South Australia]. Specimens were collected from Ituberá and Todos os Triphyllozoon arcuatum (MacGillivray, 1889): Hayward, 1999: Santos Bay (TSB), in the state of Bahia, Brazil. Additional speci- 14, figs. 6d, 9 [Northern Territory and northeastern West- mens were collected at the Industrial Port Complex of Suape ern Australia]. (CIPS), in the state of Pernambuco, Brazil (sent by Farrapeira Description. Colony robust, thickly calcified, attached CMR, Lira SMA and Ferreira GFA) (Fig. 1). Colonies from Brazil to the substratum by a broad stalk. Growing edges irregularly were first examined under a stereomicroscope and selected frilled and anastomosing, forming open lobed cups of variable portions were mounted on stubs and coated with gold for ex- diameter (Figs. 2-7). Fenestrulae small, oval, ca. 0.33-0.42 mm amination by scanning electron microscopy (JEOL JSM-6390LV diameter; trabeculae larger than fenestrulae, about 0.31-0.50 and JSM-6460LV). Measurements were made from digital SEM mm wide, comprising 2-3 alternating longitudinal zooid series images using the software ImageJ®. Specimens are lodged in that face toward colony interior (Fig. 8). Autozooids at grow- the Bryozoa collection of Museu de Zoologia at Universidade ing edges elongate, longer than wide; frontal shield smooth, Federal da Bahia (UFBA) and Universidade Federal de Pernam- with 1-2 small marginal pores, bordered by thin raised sutures buco (UFPE). (Fig. 9). Primary orifice slightly wider than long, somewhat D- Material from Singapore (no precise locality), illustrated shaped; distal rim with irregular beading (small crenulations), here using a Hitachi TM3000 SEM, comprises a part of a larger condyles long, narrow, asymmetrical, obscured by proximal colony in the collection of the Raffles Museum of Biodiversity peristome. Oral spines 2-4, present in early astogeny, laterally Research (RMBR) and is lodged at NIWA Invertebrate Collec- placed; all stout, hollow, basally jointed. Peristome low, devel- tion, Wellington. oped as asymmetrical pair of lateral lobes, jointed, delimited ZOOLOGIA 32 (6): 476–484, December 2015 478 A.C.S. Almeida et al. 23 45 67 Figures 2-7. Triphyllozoon arcuatum. 2. Colonies associated with other encrusting organisms in natural environment at Todos os Santos Bay, Bahia, Brazil; 3. Close-up of colonies in natural environment at Todos os Santos Bay, Bahia, Brazil. Photos: Ricardo J. Miranda; 4. UFBA 560, Todos os Santos Bay, Bahia, Brazil, found attached to an oil platform; 5. UFBA 559, Ituberá, Brazil, associated with the sponges Tedania ignis and Clathrina sp. 6-7. UFBA 729. 6. Frontal view of the colony; 7. Abfrontal view of the colony showing broad
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