Three non-indigenous species from Madeira harbors, including a new species of Parasmittina (Bryozoa)

Three non-indigenous species from Madeira harbors, including a new species of Parasmittina (Bryozoa) Mar Biodiv (2018) 48:977–986 DOI 10.1007/s12526-016-0592-0 ORIGINAL PAPER Three non-indigenous species from Madeira harbors, including a new species of Parasmittina (Bryozoa) 1,2 3 3,4,5 Javier Souto & Patrício Ramalhosa & João Canning-Clode Received: 17 February 2016 /Revised: 2 October 2016 /Accepted: 4 October 2016 /Published online: 22 October 2016 The Author(s) 2016. This article is published with open access at Springerlink.com . . Abstract During a study investigating the identity and Keywords Non-indigenous species Biological Invasions . . . abundance of fouling non-indigenous species in marinas Parasmittina New species Atlantic Ocean Celleporaria from the Madeira Archipelago, three species of bryo- zoans were detected on experimental settlement plates. These three species are described and figured. Introduction Celleporaria inaudita was previously only known from Vanuatu (South Pacific Ocean) and Safaga Bay (Red The introduction of non-indigenous species (NIS) into new Sea). Parasmittina alba was previously only known ecosystems is now considered a major environmental and from the Brazilian coast. The origin of Parasmitina economic threat and, along with habitat destruction, a leading multiaviculata sp. nov. is unknown. Secondary introduc- cause of biodiversity loss at a global scale (Nentwig 2007; tion by anthropogenic vectors (via hull fouling of rec- Canning-Clode 2015). In the marine system, the most signif- reational vessels) seems the most plausible explanation icant vector contributing to new biological invasions is com- for the presence of these species in the Madeira Islands. mercial shipping, particularly through the unintentional trans- fer of large numbers of organisms in ballast water and hull fouling (Ruiz et al. 2000). Every hard substratum in the marine environment (e.g., Communicated by A. Waeschenbach artificial structures such as ship hulls, piers, pontoons, pilings, This article is registered in ZooBank under urn:lsid:zoobank.org:pub:036799 seawalls, and buoys) is subject to a process known as biofoul- F4-D0D9-463B-BE6D-971692E3EDF7 ing — the accumulation of unwanted biological material at an interface (Dobretsov et al. 2014). The organisms forming this * Javier Souto biofouling community may vary in size from microorganisms javier.souto-derungs@univie.ac.at and propagules of sessile macroorganisms to complex multi- species and multidimensional assemblages including mobile Institut für Paläontologie, Geozentrum, Universität Wien, associated fauna and large macroalgae (Wahl 1997;Dürr and Althanstrasse 14, A-1090 Wien, Austria Thomason 2010; Dobretsov et al. 2014). In fact, one of the Departamento de Zoología, Genética y Antropología Física, most ancient vectors of introduction of NIS is the transfer of Universidad de Santiago de Compostela, Santiago de fouling species such as sponges, hydrozoans, barnacles, bryo- Compostela, Spain zoans, mollusks, tunicates and macroalgae on ship hulls MARE — Marine and Environmental Sciences Centre, Quinta do (Carlton and Hodder 1995). In this context, several new re- Lorde Marina, Sítio da Piedade, 9200 - 044, Caniçal, Madeira, cords of these groups have been found globally, particularly in Portugal marinas and harbors (e.g., Piola and Johnston 2008;Canning- Department of Oceanography and Fisheries, Centre of IMAR of the Clode et al. 2013a, b; Zabin et al. 2014). University of the Azores, Rua Prof. Dr Frederico Machado, 4, PT-9901-862 Horta, Azores, Portugal The Madeira Archipelago is composed of two inhabited volcanic islands — Madeira and Porto Santo — and is located Smithsonian Environmental Research Center, Edgewater, MD 21037, USA southwest of continental Europe and ∼700 km off the 978 Mar Biodiv (2018) 48:977–986 Moroccan coast in the Atlantic Ocean. Historically, the main fragments were dried, and scanning electron microscope island of Madeira has offered an important port for re-fuel and (SEM) photographs of uncoated material were taken using rest stops for merchant and passenger ships between Europe an FEI Inspect S50 SEM at the University of Vienna, and the Caribbean, and the American and African continents. Austria. Some samples were treated in an ultrasound bath Nowadays, most shipping can be attributed to tourist cruise and bleached with sodium hypochlorite prior to SEM exami- ships and sailing yachts from different parts of the world nation. The SEM was used with a back-scattered electron (APRAM 2014). In recent years, the Madeira Archipelago detector in low vacuum mode. Zooidal measurements were has been the site of a comprehensive monitoring survey of taken from the SEM images using the software ImageJ® marine NIS. As a result, several new species have been de- (http://rsbweb.nih.gov/ij). Specimens were deposited in the tected (e.g., Wirtz and Canning-Clode 2009; Canning-Clode collections of the Museu Municipal de História Natural et al. 2013a; Ramalhosa et al. 2014; Ramalhosa and Canning- (MMF), in Funchal, Madeira Island, Portugal. Clode 2015) including previously un-described species (Souto et al. 2015). The knowledge about bryozoans from Systematics Madeira Island is far from complete, but several papers record approximately 150 species from this phylum in this area. The Phylum Bryozoa Ehrenberg, 1831 first papers about bryozoans from these islands date back to Class Gymnolaemata Allman, 1856 the end of the past century (Busk 1858a, b, 1859, 1860, 1861; Order Cheilostomata Busk, 1852 Hincks 1880; Johnson 1897; Waters 1899;Norman 1909)but Family Lepraliellidae Vigneaux, 1947 in recent years new records, including undescribed species Genus Celleporaria Lamouroux, 1821 and NIS, have been added (d’Hondt 1985; Alves and Cocito Celleporaria inaudita Tilbrook, Hayward and Gordon, 2002; Berning and Kukliński 2008; Berning et al. 2008; Wirtz 2001 and Canning-Clode 2009;Berning 2012; Souto et al. 2014, (Fig. 2, Table 1) 2015; Ramalhosa et al. 2016). In the present paper, we de- Celleporaria inaudita Tilbrook, Hayward and Gordon, scribe one new species and two new records of Bryozoa col- 2001: 72, Figs 13D-F lected from artificial settlement plates as part of an ongoing Material examined: MMF44608 and MMF44609 from monitoring survey of NIS conducted in several marinas in the Funchal, MMF44610 from Calheta and MMF44611 from Madeira Archipelago. Caniçal. Description Irregular encrusting colony, multilaminar or developing Material and methods nodules. Irregular autozooids with an irregular disposition. Frontal wall finely granular, with only a few rounded, margin- Since July 2013, we have been investigating the species com- al pores. Primary orifice slightly wider than long, anter semi- position and abundance of fouling assemblages in four ma- circular, poster with sides slightly concave and indented by rinas of the Archipelago: Calheta (32°43′ N, 17°10′ W), two asymmetrical sinuses, separated by one cusp; two more Funchal (32°38′ N, 16°54′ W), Caniçal (32°44′ N, 16°42′ cusps can appear in the lateral part of the sinus. Development W) and Porto Santo Island (33°3′ N, 16°18′ W) (Fig. 1)as and size of the orifice, the sinuses, and the cusps are very part of an ongoing survey of NIS in Madeira. Following the variable between autozooids, in some cases dependent on methods used by Canning-Clode et al. (2013a) and most re- the degree of the calcification. Condyles lacking. No oral cently by Ramalhosa et al. (2014), ten polyvinylchloride spines. Avicularia suboral on an umbo, present in some zo- (PVC) settlement plates (14 × 14 × 0.3 cm) were individually oids, rostrum elliptical, with the distal portion denticulate. attached to a brick in a horizontal orientation facing down- Large vicarious avicularia, cystid with rounded marginal wards and hung at about 1 meter depth, from pontoons in all pores similar to the ones present in the autozooid; rostrum four marinas. Settlement plates were collected every 3 months raised, with rounded and serrated tip, sometimes externally (starting in July 2013; finishing in August 2014) for fouling cover by secondary calcification. Cross-bar complete, thin, species identification, a duration after which fully developed without columella, palate with very large foramen. Ooecium colonies could be observed. Fouling communities were first non-cleithral, widely open; covered by granular secondary observed with the aid of a stereomicroscope (Leica Wild-M3 calcification. Heerbrugg), and digital photographs were taken of specimens Distribution from settlement plates using a Sony DSC-W55 camera. For Known from Vanuatu (South Pacific Ocean) and Safaga the purpose of this analysis, only bryozoan samples were col- Bay (Red Sea). This paper reports its first record for lected from the plate in the different marina sites, and pre- Madeira Island. To date, our monitoring surveys did not detect served in 95 % ethanol. Bryozoan specimens were later ex- Celleporaria inaudita in Porto Santo Island. Remarks amined with a stereomicroscopy Leica MZ12. Colony Mar Biodiv (2018) 48:977–986 979 Fig. 1 Location of the four study sites where samples were collected in the Madeira archipelago Celleporaria inaudita was described from Vanuatu as this new record confirms its identification, and its presence forming nodules on corals and anthropogenic structures, across the marinas of Madeira island. e.g., Port Vila harbor on Efate Island (Tilbrook et al. 2001). Family Smittinidae Levinsen, 1909 Ostrovsky et al. (2011) also included this species in a checklist Genus Parasmittina Osburn, 1952 of bryozoans from Safaga Bay (Red Sea); see figures in Parasmittina alba Ramalho, Muricy and Taylor, 2011 Ostrovsky et al. (2015). According to Tilbrook et al. (2001), (Fig. 3, Table 2) C. inaudita is similar to C. aperta, but the latter species has Parasmittina alba Ramalho, Muricy and Taylor, 2011: oral spines and a lanceolate rostrum in the spatulate 769, Fig. 2. avicularium, which is absent in C. inaudita. The specimens Material examined: MMF44612 from Caniçal, collected in Madeira, as well as the specimens described by MMF44613 and MMF44614 from Calheta, MMF44615 from Tilbrook et al. (2001) and the Safaga Bay specimens, indicate Porto Santo. that there is variability in several characters, not only between Description colonies, but also between zooids in the same colony. The Colony encrusting, unilaminar or multilaminar, pale white morphology of the orifice is very variable, and although the in color. Autozooids mainly rectangular, in some cases hex- presence of the two asymmetrical sinuses is constant, their agonal, longer than wide, disposed initially in linear series; morphology is very variable and the smaller sinus can be very linear pattern in old colonies lost. Frontal wall coarse, imper- reduced. Here we figured the denticulation of the rostrum of forate centrally, and with large marginal pores. Primary orifice the spatulate avicularia, not visible in the Safaga Bay collec- wider than long, surrounded by a proximo-lateral peristome, tion, was probably due to erosion of the specimens. Similarly, incomplete proximally, with a proximal fissure usually qua- the lyrula is very variable and not a good taxonomic character drangular. Distal edge round, with two curved, thin, and point- (see, for example, Kuklinski et al. 2013; Berning et al. 2014). ed condyles, curved and directed to the lyrula. In ovicellate The morphology of the orifice in general, and the sinus in zooids, the distal margin of the orifice has two symmetrical particular can be very variable in some species of notches that could be more or less developed. Wide lyrula in Celleporaria, both between colonies and within the same col- the proximal border. One or two spines in the distal margin of ony; see the case of Celleporaria brunnea (Hincks, 1884) the orifice. Three kinds of adventitious avicularia. In most (Canning-Clode et al. 2013b;Harmelin 2014;Lodola etal. cases only one per zooid (although two in some cases), located 2015). Therefore, orifice morphology is not a very useful tax- latero-proximal to the orifice. Although, there are large areas onomic character for this genus. In 2006 and 2007, Canning- in the colony without avicularia. Avicularia are small oval, Clode et al. (2013a) collected specimens at Quinta do Lorde very abundant, variable in size and form, generally longer than Marina that were identified as Celleporaria cf. inaudita;thus, wide and with the distal margin rounded and wider than the 980 Mar Biodiv (2018) 48:977–986 Fig. 2 Celleporaria inaudita. a General aspect of the colony surface, with vicarious avicularia. b Autozooid orifices, vicarious avicularia and ooecia. c Ooecia in unbleached specimen. d Vicarious avicularia. e, f, g, h Morphological variability between orifices and suboral avicularia proximal portion. Small triangular avicularia directed to the elongated and spatulate of variable morphology, covering al- margin of the zooid, lightly raised, and with the margins most the whole frontal wall of the zooid. Ovicell slightly serrated. Large, spatulate avicularia not common, sit- hyperstomial, ooecium formed by the distal autozooid, glob- uated close to the orifice and directed proximally, rostrum ular, about as wide as long, ectooecium perforated by Table 1 Measurements (in mm) Mean SD Minimum Maximum N of Celleporaria inaudita Zooidal orifice length 0.147 0.0107 0.126 0.169 19 Zooidal orifice width 0.169 0.0168 0.147 0.204 19 Spatulate avicularia length 0.430 0.0148 0.411 0.448 6 Spatulate avicularia width 0.192 0.0110 0.175 0.204 6 Ooecium length 0.130 0,0186 0,094 0,175 11 Ooecium width 0.275 0.0191 0.228 0.299 11 SD standard deviation, N number of measurements Mar Biodiv (2018) 48:977–986 981 Fig. 3 Parasmittina alba. a General view of the colony margin. b Autozooid orifice, with condiles and the base of oral spines. c Autozooids with lateral small triangular avicularia. d Autozooids with latero-suboral oval avicularia. e Spatulate avicularia. f, g Ovicellate zooids with variability in the morphology of the ooecia. h Detail of ovicell; arrows indicate symmetrical notches in the distal margin of the orifice numerous, although variable in number, irregularly-shaped and had not been recorded elsewhere until now. Some pseudopores. Secondary calcification very variable in devel- differences are noted between the original material and opment, covering the distal and lateral portions of the ovicell, our specimens; mainly in the figured ovicells the ectooecium visible only in the circular frontal–proximal (Ramalho et al. 2011:Fig. 2b, h), which have large area. pores in the ectooecium, but are smaller in our speci- Distribution mens. This difference could be attributed to the vari- Only known previously from Arraial do Cabo, Rio de ability of this structure and difference in level of cal- Janeiro, Brazil. Now present in Porto Santo and Madeira cification, as was observed by us between colonies Island (Calheta and Caniçal), Portugal. and even between ovicells in the same colony Remarks (Fig. 3f, g, h). Madeira specimens have two symmet- The specimens found in Madeira fully match the rical notches in the distal margin of the orifice in morphological characteristics given for Parasmittina ovicellate zooids (Fig. 3h); this structure was also not- alba. This species was described from Arraial do ed in P. alba from Arraial do Cabo (Fig. 2g and h in Cabo in Rio de Janeiro, Brazil (Ramalho et al. 2011) Ramalho et al. 2011), although comments about this 982 Mar Biodiv (2018) 48:977–986 Table 2 Measurements (in mm) Mean SD Minimum Maximum N of Parasmittina alba Zooidal length 0.488 0.0697 0.390 0.670 24 Zooidal width 0.340 0.0580 0.240 0.460 24 Primary orifice length 0.082 0.0056 0.076 0.101 20 Primary orifice width 0.125 0.0102 0.103 0.143 20 Oval avicularia length 0.092 0.0095 0.074 0.104 9 Oval avicularia width 0.056 0.0037 0.051 0.063 9 Pointed avicularia length 0.078 0.0067 0.068 0.089 10 Pointed avicularia width 0.047 0.0050 0.037 0.054 10 Ooecium length 0.265 0.0177 0.235 0.297 20 Ooecium width 0.267 0.0184 0.233 0.300 20 SD standard deviation, N number of measurements were not included in the original description. Only one peristome, laterally more developed, proximally poorly devel- avicularium per autozooid is indicated in the original oped and distally interrupted by one (in some cases two) distal description, while two triangular avicularia were ob- spines. This peristome is not visible when the secondary cal- served in one ovicellate zooid, but this seems very cification is more developed. Proximal border of the orifice infrequent. In addition, the adventitious avicularia with a variable lyrula, usually short and occupying from one were not seen in our specimens. quarter to two third of the proximal border. Condyles stout, This species is very similar to Parasmittina betamorphaea sharply pointed. Avicularia monomorphic, oval (lightly point- Winston 2005, distributed in the Gulf of Mexico and Brazil. ed when is in direct contact with the margin of the zooid), very But according to Ramalho et al. (2011) Parasmittina alba is numerous in some parts of the colony, but always two or more differentiated by the presence of more than one avicularium per zooid. The avicularia occur on the margins of the zooids. per zooid in P. betamorphaea, lacking the serrated rostrum in Rostrum is slightly spatulate. Ovicell subimmersed, and be- small avicularia, possessing the giant avicularia with a more coming endozooidal because of the strong secondary calcifi- rounded rostrum, and by the different positioning and shape of cation. Ooecium formed by the distal autozooid. Ectooecium the pores in the ovicell. Much of the difference between these almost flat frontally, with several irregularly-shaped species, in the ovicell and avicularia morphology, is attributed pseudopores. The secondary calcification covers the distal, to characters that are very variable between colonies or even lateral and, in some cases, the proximal part of the ectooecium, between zooids in the same colony. In the figures of the orig- leaving only a central area with exposed pseudopores. In some inal description of P. betamorphaea, it is not possible to see ovicells only the peripheral area of the secondary calcification more than one avicularium per zooid. Both species, P. alba is truly calcified, whereas the rest is membraneous, in cleaned and P. betamorphaea, were described from only two colonies, specimens showing the ectooecium with pseudopores which indicates that more specimens should be studied more underneath. carefully, particularly to examine the intra-colonial variability Distribution and to evaluate the possibility of the two species being Currently only known from Porto Santo Island, Madeira, synonyms. Portugal. Parasmittina multiaviculata sp. nov. Remarks (Fig. 4, Table 3) According to the literature, only two species of this Material examined: Holotype: MMF44616 from Porto genus were previously recorded in Madeira, Santo; Paratype: MMF44617 from Porto Santo. Parasmittina trispinosa (Johnston, 1825) by Waters Etymology: In reference to the numerous avicularia per (1899)and Norman (1909)and Parasmittina protecta zooid. (Thornely, 1905) by Canning-Clode et al. (2013a). The Description two colonies reported in the current study show signif- Colony encrusting, unilaminar or multilaminar, initially icant differences from these two species and from the translucent. Rectangular to hexagonal autozooids in the first previously described species, P. alba. According to layer and more irregular in the second layers. Frontal wall Harmelin et al. (2009), P. protecta presents a peristome nodular, with marginal large pores. Orifice longer than wide, interrupted distally, and raised proximally; the orifice is surrounded by a normally rectangular (but very variable in broader than high, and the avicularia are infrequent and when present, they occur in two morphologies and are morphology, and more rounded in ovicellated zooids) Mar Biodiv (2018) 48:977–986 983 Fig. 4 Parasmittina multiaviculata sp. nov. a General view of the autozooids and ooecia in an unbleached specimen. b Bleached specimen, showing ooecia and abundant frontal avicularia. c Ovicellate zooids and frontal avicularia. d, e Primary orifice with variations in the lyrula morphology. f Condile. g Bleached ovicellate and non ovicellate zooids. h Ovicellate zooid in unbleached specimen large. According to the descriptions by Hayward and specimens are similar to Parasmittina inalienata Tilbrook Ryland (1999) and Soule and Soule (2002), 2006, described from the Solomon and Fiji Islands; but differ P. trispinosa presents an orbicular orifice with a big from that species by having a slightly bigger orifice with a triangular avicularium lateral to the orifice, which is, wider lyrula, (Fig. 35D in Tilbrook 2006), less globular in some cases, replaced by a smaller avicularium. ovicells which are almost flat in the frontal plane, and by Furthermore, the ovicells in P. trispinosa are character- lacking a round peristome in the ovicellate zooids. The ized by having few, irregular large pores. avicularia of P. inalienata seem to be numerous with a slightly The genus Parasmittina is very specious with currently spatulate rostrum which is always directed proximo-medially 122 known species (Bock 2015a; WoRMS 2015), distributed or medially, while in the Madeira specimens, the direction of around all oceans, but with a high number of species in the the rostrum is disordered, without a clear pattern, and the Pacific and Indian Oceans. Among this diversity, there are few rostrum in some cases is slightly pointed. species that have an orifice that is longer than wide, mono- Most species of this genus (c. 99 species) seem to be morphic avicularia, and one or two distal oral spines. Madeira natives from the Pacific and Indian Oceans (e.g., 984 Mar Biodiv (2018) 48:977–986 Table 3 Measurements (in mm) Mean SD Minimum Maximum N of Parasmittina multiaviculata sp nov Zooidal length 0.576 0.0719 0.464 0.720 14 Zooidal width 0.366 0.0392 0.307 0.429 14 Primary orifice length 0.110 0.0076 0.093 0.124 14 Primary orifice width 0.081 0.0081 0.079 0.109 14 Avicularia length 0.103 0.0161 0.065 0.130 18 Avicularia width 0.050 0.0082 0.036 0.062 18 Ooecium length 0.218 0.0125 0.198 0.241 18 Ooecium width 0.275 0.0158 0.249 0.297 18 SD standard deviation, N number of measurements Tilbrook et al. 2001;Tilbrook 2006; Soule and Soule the extent by which these species have established themselves 1973, 2002;Gordon 1984, 1989;Hayward 1988;Bock in the natural environment. 2015a;Seo 2002; Hayward and Parker 1994), and are The natural fauna of Madeira shows close affinities with particularly abundant in coral reef habitats (Hayward the fauna of Lusitania, Mediterranean, and Mauritanian re- and Parker 1994). Several other Parasmittina species gions (Wirtz 1998); nevertheless, the three species of bryo- identified or recorded from other oceans and seas are zoans found here show closer affinities with species from the considered non-indigenous (e.g., Harmelin et al. 2009). Pacific (C. inaudita, P. multiaviculata sp. nov.) and the The exclusive presence of Parasmittina multiaviculata Caribbean (P.alba). Several Brazilian and Caribbean species sp. nov. on artificial plates deployed in harbors in of macroinvertebrates were detected in recent years in Madeira, and the fact that there are no previous records Madeiran waters (e.g., Wirtz and Canning-Clode 2009; of similar species in the area, suggests this could be a Canning-Clode et al. 2013a, b; Ramalhosa et al. 2014; Souto new introduction. The presence of this species in only et al. 2015). Beania maxilladentata Ramalho, Muricy and one locality may indicate a recent introduction. Its mor- Taylor 2008, a bryozoan only previously known from Brazil phological proximity to P. inalienata could indicate (Ramalho et al. 2008; Vieira et al. 2010), was also found in Parasmittina multiaviculata sp. nov. may have a Madeiran waters (Souto et al. 2015), but in this case, only on Pacific origin. natural substrates. In addition, several other species with West Atlantic distributions, mainly from the Gulf of Mexico, were also recently found in Madeira (Canning-Clode et al. 2013a; Discussion Ramalhosa et al. 2014) such as the bryozoans Schizoporella pungens (Canu and Bassler 1928), Cradoscrupocellaria Knowledge of the Madeira marine invertebrate fauna is scarce bertholetti (Audouin 1826), Amathia verticillata (Delle and in the case of bryozoans, very limited (Busk 1858a, b, Chiaje 1822), the ascidian Distaplia corolla Monniot F. 1859, 1860, 1861;Hincks 1880; Johnson 1897; Waters 1899; 1974 and the sabellid polychaete Branchiomma bairdi Norman 1909). However, in recent years, monitoring surveys (McIntosh 1885). Also a few species from the Indo-Pacific for non-indigenous species in the archipelago has resulted in region were detected (Norman 1909; Canning-Clode et al. new records and undescribed species in the islands (d’Hondt 2013a; Ramalhosa et al. 2014; Ramalhosa and Canning- 1985; Alves and Cocito 2002; Berning and Kukliński 2008; Clode 2015), but most of these species appeared first in Berning et al. 2008; Wirtz and Canning-Clode 2009; Berning European waters (e.g., Cabezas et al. 2015; Arias et al. 2012;Souto etal. 2014, 2015; Ramalhosa et al. 2016). 2013;Cinar 2009; Giangrande et al. 2013; Garcia Raso Nevertheless, the lack of a comprehensive checklist of bryo- 1981; Turon et al. 2005;Rylandetal. 2009, 2011). zoans in Madeira makes the detection and dating of new an- Nevertheless, none of the three species reported in the current thropogenic introductions a complex challenge. Due to the paper were recorded in other areas close to Madeira. Of them, sessile mode of life of their adults and the estimated short- only Celleporaria inaudita was recently found in the Red Sea, lived non-feeding pelagic phase of their larvae, the presence after its original description in the Pacific Ocean. The direct of the three species reported here in Madeiran waters is diffi- introduction of these species from their original localities to cult to explain by natural dispersion methods, so anthropogen- Madeira seems not very plausible. It is possible that these ic vectors seem more reasonable. The presence in other sub- species have a broader distribution than currently known, par- strates different from the settlement panels (natural or artifi- ticularly in European and North African waters, and have been cial) was not checked, so no inferences can be made regarding probably introduced to Madeira via hull fouling (recreational Mar Biodiv (2018) 48:977–986 985 Arias A, Giangrande A, Gambi MC, Anadon N (2013) Biology and new and/or cruise vessels). Currently, most shipping can be attrib- records of the invasive species Branchiomma bairdi (Annelida: uted to tourist cruise ships and sailing yachts visiting for re- Sabellidae) in the Mediterranean Sea. Mediterr Mar Sci 14:162–171 fuel and rest stops from different parts of the world (APRAM Berning B (2012) Taxonomic notes on some Cheilostomata (Bryozoa) 2014). Furthermore, recent findings by Ramalhosa et al. from Madeira. Zootaxa 3236:36–54 Berning B, Kukliński P (2008) North-east Atlantic and Mediterranean (2016) have shown that dry dock inspections on local and species of the genus Buffonellaria (Bryozoa, Cheilostomata): impli- foreign recreational vessels support the hypothesis from other cations for biodiversity and biogeography. Zool J Linn Soc 152: studies, that emphasize hull fouling as the key introduction 537–566. doi:10.1111/j.1096-3642.2007.00379.x vector that contribute to the arrival and spread of NIS to Berning B, Tilbrook KJ, Rosso A (2008) Revision of the north-eastern Atlantic and Mediterranean species of the genera Herentia and neighbouring islands. Moreover, the genus Parasmittina is a Therenia (Bryozoa: Cheilostomata). J Nat Hist 42:1509–1547 very specious genus with currently 122 known species (Bock Berning B, Tilbrook KJ, Ostrovsky AN (2014) What, if anything, is a 2015a; WoRMS 2015) and 17 fossil species. Similar diversity lyrula? In: Rosso A, Wyse Jackson PN, Porter JS (eds) Bryozoan is present in the Celleporaria genus, with 90 species (Bock Studies, Museo delle Scienze, Trento pp 21–28 2015b). This large number of species in these genera makes Bock P (2015) Recent and fossil Bryozoa: Parasmittina Osburn, 1952. Available from: http://www.bryozoa.net/cheilostomata/smittinidae/parasmittina.html. correct identification challenging, possibly resulting in some Accessed 16 September 2015) species being misidentified and lumped together. So records in Bock P (2015) Celleporaria Lamouroux, 1821. In: Bock P, Gordon D other parts of the world of these species could go unnoticed. (2015) World List of Bryozoa. Accessed through: World Register of Here, three species of bryozoans are added to the nine other Marine Species at http://www.marinespecies.org/aphia.php?p= taxdetails&id=205020. Accessed16June2016 non-indigenous bryozoan species known from the Madeira Busk G (1858a) Zoophytology. On some Madeiran Polyzoa. Quart J archipelago (Wirtz and Canning-Clode 2009; Canning-Clode Micros Sci 6:124–130 et al. 2013a; Ramalhosa et al. 2016). Currently, the Busk G (1858b) Zoophytology. On some Madeiran Polyzoa. Quart J xenodiversity in Madeira Island is probably underestimated, Micros Sci 6:261–263 and therefore this number is likely to increase in the next Busk G (1859) Zoophytology. On some Madeiran Polyzoa. Quart J Micros Sci 7:65–67 years. Busk G (1860) Zoophytology. Catalogue of the Polyzoa collected by J.Y. Johnson, Esq., at Madeira, in the years 1859 and 1860, with descrip- tions of new species. Quart J Micros Sci 8(213–214):280–285 Acknowledgments Open access funding provided by Univeristy of Busk G (1861) Description of new Polyzoa collected by J.Y.Johnston Vienna. Esq., at Madeira. Quart J Micros Sci New Ser 1:77–80 We are grateful to Oscar Reverter-Gil and Linda McCann for the Cabezas MP, Xavier R, Branco M, Santos AM, Guerra-García JM (2015) valuable revision of an earlier version of this manuscript. Thanks also Invasion history of Caprella scaura Templeton, 1836 (Amphipoda: to Kevin Tilbrook and Andrew Ostrovsky for their comments that helped Caprellidae) in the Iberian Peninsula: multiple introductions re- to improve this paper. The work of J.S. was supported by the Austrian vealed by mitochondrial sequence data. Biol Invasions 16:2221– Science Fund (FWF, Lise Meitner Program M1444-B25 and Project Number AP28954-B29). P. Ramalhosa holds a research fellowship in the Project M1420-01-0145-FEDER-000001 — project Observatório Canning-Clode J (2015) General introduction: aquatic and terrestrial bi- Oceânico da Madeira (OOM). J. Canning-Clode was supported by a ological invasions in the 21st century. In: Canning-Clode J (ed) starting grant in the framework of the 2014 FCT Investigator Biological invasions in changing ecosystems: vectors, ecological Programme (IF/01606/2014/CP1230/CT0001). We thank Porto Santo impacts, management and predictions. De Gruyter Open, Berlin, Line for their travel aid to the Island of Porto Santo, and the administra- pp 13–20 tion of the four marinas monitored in this study (Porto Recreio da Calheta, Canning-Clode J, Fofonoff P, McCann L, Carlton JT, Ruiz G (2013a) Marina do Funchal, Marina da Quinta do Lorde and Marina do Porto Marine invasions on a subtropical island: fouling studies and new Santo). This is contribution number 32 of the Marine Biology Station records in a recent marina on Madeira Island (East Atlantic Ocean). of Funchal. Finally, we are grateful to the anonymous reviewers and Dr Aquat Invasion 8:261–270 A. Waeschenbach for their valuable revision and comments. Canning-Clode J, Souto J, McCann L (2013b) First record of Celleporaria brunnea (Bryozoa: Lepraliellidae) in Portugal and in Open Access This article is distributed under the terms of the Creative he East Atlantic. Mar Biodivers Rec 6, e108 Commons Attribution 4.0 International License (http:// Carlton JT, Hodder J (1995) Biogeography and dispersal of coastal ma- creativecommons.org/licenses/by/4.0/), which permits unrestricted use, rine organisms: experimental studies on a replica of a 16th-century distribution, and reproduction in any medium, provided you give appro- sailing vessel. Mar Biol 121:721–730 priate credit to the original author(s) and the source, provide a link to the Cinar ME (2009) Alien polychaete species (Annelida: Polychaeta) on the Creative Commons license, and indicate if changes were made. southern coast of Turkey (Levantine SEA, eastern Mediterranean), with 13 new records for Mediterranean Sea. 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Three non-indigenous species from Madeira harbors, including a new species of Parasmittina (Bryozoa)

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Mar Biodiv (2018) 48:977–986 DOI 10.1007/s12526-016-0592-0 ORIGINAL PAPER Three non-indigenous species from Madeira harbors, including a new species of Parasmittina (Bryozoa) 1,2 3 3,4,5 Javier Souto & Patrício Ramalhosa & João Canning-Clode Received: 17 February 2016 /Revised: 2 October 2016 /Accepted: 4 October 2016 /Published online: 22 October 2016 The Author(s) 2016. This article is published with open access at Springerlink.com . . Abstract During a study investigating the identity and Keywords Non-indigenous species Biological Invasions . . . abundance of fouling non-indigenous species in marinas Parasmittina New species Atlantic Ocean Celleporaria from the Madeira Archipelago, three species of bryo- zoans were detected on experimental settlement plates. These three species are described and figured. Introduction Celleporaria inaudita was previously only known from Vanuatu (South Pacific Ocean) and Safaga Bay (Red The introduction of non-indigenous species (NIS) into new Sea). Parasmittina alba was previously only known ecosystems is now considered a major environmental and from the Brazilian coast. The origin of Parasmitina economic threat and, along with habitat destruction, a leading multiaviculata sp. nov. is unknown. Secondary introduc- cause of biodiversity loss at a global scale (Nentwig 2007; tion by anthropogenic vectors (via hull fouling of rec- Canning-Clode 2015). In the marine system, the most signif- reational vessels) seems the most plausible explanation icant vector contributing to new biological invasions is com- for the presence of these species in the Madeira Islands. mercial shipping, particularly through the unintentional trans- fer of large numbers of organisms in ballast water and hull fouling (Ruiz et al. 2000). Every hard substratum in the marine environment (e.g., Communicated by A. Waeschenbach artificial structures such as ship hulls, piers, pontoons, pilings, This article is registered in ZooBank under urn:lsid:zoobank.org:pub:036799 seawalls, and buoys) is subject to a process known as biofoul- F4-D0D9-463B-BE6D-971692E3EDF7 ing — the accumulation of unwanted biological material at an interface (Dobretsov et al. 2014). The organisms forming this * Javier Souto biofouling community may vary in size from microorganisms javier.souto-derungs@univie.ac.at and propagules of sessile macroorganisms to complex multi- species and multidimensional assemblages including mobile Institut für Paläontologie, Geozentrum, Universität Wien, associated fauna and large macroalgae (Wahl 1997;Dürr and Althanstrasse 14, A-1090 Wien, Austria Thomason 2010; Dobretsov et al. 2014). In fact, one of the Departamento de Zoología, Genética y Antropología Física, most ancient vectors of introduction of NIS is the transfer of Universidad de Santiago de Compostela, Santiago de fouling species such as sponges, hydrozoans, barnacles, bryo- Compostela, Spain zoans, mollusks, tunicates and macroalgae on ship hulls MARE — Marine and Environmental Sciences Centre, Quinta do (Carlton and Hodder 1995). In this context, several new re- Lorde Marina, Sítio da Piedade, 9200 - 044, Caniçal, Madeira, cords of these groups have been found globally, particularly in Portugal marinas and harbors (e.g., Piola and Johnston 2008;Canning- Department of Oceanography and Fisheries, Centre of IMAR of the Clode et al. 2013a, b; Zabin et al. 2014). University of the Azores, Rua Prof. Dr Frederico Machado, 4, PT-9901-862 Horta, Azores, Portugal The Madeira Archipelago is composed of two inhabited volcanic islands — Madeira and Porto Santo — and is located Smithsonian Environmental Research Center, Edgewater, MD 21037, USA southwest of continental Europe and ∼700 km off the 978 Mar Biodiv (2018) 48:977–986 Moroccan coast in the Atlantic Ocean. Historically, the main fragments were dried, and scanning electron microscope island of Madeira has offered an important port for re-fuel and (SEM) photographs of uncoated material were taken using rest stops for merchant and passenger ships between Europe an FEI Inspect S50 SEM at the University of Vienna, and the Caribbean, and the American and African continents. Austria. Some samples were treated in an ultrasound bath Nowadays, most shipping can be attributed to tourist cruise and bleached with sodium hypochlorite prior to SEM exami- ships and sailing yachts from different parts of the world nation. The SEM was used with a back-scattered electron (APRAM 2014). In recent years, the Madeira Archipelago detector in low vacuum mode. Zooidal measurements were has been the site of a comprehensive monitoring survey of taken from the SEM images using the software ImageJ® marine NIS. As a result, several new species have been de- (http://rsbweb.nih.gov/ij). Specimens were deposited in the tected (e.g., Wirtz and Canning-Clode 2009; Canning-Clode collections of the Museu Municipal de História Natural et al. 2013a; Ramalhosa et al. 2014; Ramalhosa and Canning- (MMF), in Funchal, Madeira Island, Portugal. Clode 2015) including previously un-described species (Souto et al. 2015). The knowledge about bryozoans from Systematics Madeira Island is far from complete, but several papers record approximately 150 species from this phylum in this area. The Phylum Bryozoa Ehrenberg, 1831 first papers about bryozoans from these islands date back to Class Gymnolaemata Allman, 1856 the end of the past century (Busk 1858a, b, 1859, 1860, 1861; Order Cheilostomata Busk, 1852 Hincks 1880; Johnson 1897; Waters 1899;Norman 1909)but Family Lepraliellidae Vigneaux, 1947 in recent years new records, including undescribed species Genus Celleporaria Lamouroux, 1821 and NIS, have been added (d’Hondt 1985; Alves and Cocito Celleporaria inaudita Tilbrook, Hayward and Gordon, 2002; Berning and Kukliński 2008; Berning et al. 2008; Wirtz 2001 and Canning-Clode 2009;Berning 2012; Souto et al. 2014, (Fig. 2, Table 1) 2015; Ramalhosa et al. 2016). In the present paper, we de- Celleporaria inaudita Tilbrook, Hayward and Gordon, scribe one new species and two new records of Bryozoa col- 2001: 72, Figs 13D-F lected from artificial settlement plates as part of an ongoing Material examined: MMF44608 and MMF44609 from monitoring survey of NIS conducted in several marinas in the Funchal, MMF44610 from Calheta and MMF44611 from Madeira Archipelago. Caniçal. Description Irregular encrusting colony, multilaminar or developing Material and methods nodules. Irregular autozooids with an irregular disposition. Frontal wall finely granular, with only a few rounded, margin- Since July 2013, we have been investigating the species com- al pores. Primary orifice slightly wider than long, anter semi- position and abundance of fouling assemblages in four ma- circular, poster with sides slightly concave and indented by rinas of the Archipelago: Calheta (32°43′ N, 17°10′ W), two asymmetrical sinuses, separated by one cusp; two more Funchal (32°38′ N, 16°54′ W), Caniçal (32°44′ N, 16°42′ cusps can appear in the lateral part of the sinus. Development W) and Porto Santo Island (33°3′ N, 16°18′ W) (Fig. 1)as and size of the orifice, the sinuses, and the cusps are very part of an ongoing survey of NIS in Madeira. Following the variable between autozooids, in some cases dependent on methods used by Canning-Clode et al. (2013a) and most re- the degree of the calcification. Condyles lacking. No oral cently by Ramalhosa et al. (2014), ten polyvinylchloride spines. Avicularia suboral on an umbo, present in some zo- (PVC) settlement plates (14 × 14 × 0.3 cm) were individually oids, rostrum elliptical, with the distal portion denticulate. attached to a brick in a horizontal orientation facing down- Large vicarious avicularia, cystid with rounded marginal wards and hung at about 1 meter depth, from pontoons in all pores similar to the ones present in the autozooid; rostrum four marinas. Settlement plates were collected every 3 months raised, with rounded and serrated tip, sometimes externally (starting in July 2013; finishing in August 2014) for fouling cover by secondary calcification. Cross-bar complete, thin, species identification, a duration after which fully developed without columella, palate with very large foramen. Ooecium colonies could be observed. Fouling communities were first non-cleithral, widely open; covered by granular secondary observed with the aid of a stereomicroscope (Leica Wild-M3 calcification. Heerbrugg), and digital photographs were taken of specimens Distribution from settlement plates using a Sony DSC-W55 camera. For Known from Vanuatu (South Pacific Ocean) and Safaga the purpose of this analysis, only bryozoan samples were col- Bay (Red Sea). This paper reports its first record for lected from the plate in the different marina sites, and pre- Madeira Island. To date, our monitoring surveys did not detect served in 95 % ethanol. Bryozoan specimens were later ex- Celleporaria inaudita in Porto Santo Island. Remarks amined with a stereomicroscopy Leica MZ12. Colony Mar Biodiv (2018) 48:977–986 979 Fig. 1 Location of the four study sites where samples were collected in the Madeira archipelago Celleporaria inaudita was described from Vanuatu as this new record confirms its identification, and its presence forming nodules on corals and anthropogenic structures, across the marinas of Madeira island. e.g., Port Vila harbor on Efate Island (Tilbrook et al. 2001). Family Smittinidae Levinsen, 1909 Ostrovsky et al. (2011) also included this species in a checklist Genus Parasmittina Osburn, 1952 of bryozoans from Safaga Bay (Red Sea); see figures in Parasmittina alba Ramalho, Muricy and Taylor, 2011 Ostrovsky et al. (2015). According to Tilbrook et al. (2001), (Fig. 3, Table 2) C. inaudita is similar to C. aperta, but the latter species has Parasmittina alba Ramalho, Muricy and Taylor, 2011: oral spines and a lanceolate rostrum in the spatulate 769, Fig. 2. avicularium, which is absent in C. inaudita. The specimens Material examined: MMF44612 from Caniçal, collected in Madeira, as well as the specimens described by MMF44613 and MMF44614 from Calheta, MMF44615 from Tilbrook et al. (2001) and the Safaga Bay specimens, indicate Porto Santo. that there is variability in several characters, not only between Description colonies, but also between zooids in the same colony. The Colony encrusting, unilaminar or multilaminar, pale white morphology of the orifice is very variable, and although the in color. Autozooids mainly rectangular, in some cases hex- presence of the two asymmetrical sinuses is constant, their agonal, longer than wide, disposed initially in linear series; morphology is very variable and the smaller sinus can be very linear pattern in old colonies lost. Frontal wall coarse, imper- reduced. Here we figured the denticulation of the rostrum of forate centrally, and with large marginal pores. Primary orifice the spatulate avicularia, not visible in the Safaga Bay collec- wider than long, surrounded by a proximo-lateral peristome, tion, was probably due to erosion of the specimens. Similarly, incomplete proximally, with a proximal fissure usually qua- the lyrula is very variable and not a good taxonomic character drangular. Distal edge round, with two curved, thin, and point- (see, for example, Kuklinski et al. 2013; Berning et al. 2014). ed condyles, curved and directed to the lyrula. In ovicellate The morphology of the orifice in general, and the sinus in zooids, the distal margin of the orifice has two symmetrical particular can be very variable in some species of notches that could be more or less developed. Wide lyrula in Celleporaria, both between colonies and within the same col- the proximal border. One or two spines in the distal margin of ony; see the case of Celleporaria brunnea (Hincks, 1884) the orifice. Three kinds of adventitious avicularia. In most (Canning-Clode et al. 2013b;Harmelin 2014;Lodola etal. cases only one per zooid (although two in some cases), located 2015). Therefore, orifice morphology is not a very useful tax- latero-proximal to the orifice. Although, there are large areas onomic character for this genus. In 2006 and 2007, Canning- in the colony without avicularia. Avicularia are small oval, Clode et al. (2013a) collected specimens at Quinta do Lorde very abundant, variable in size and form, generally longer than Marina that were identified as Celleporaria cf. inaudita;thus, wide and with the distal margin rounded and wider than the 980 Mar Biodiv (2018) 48:977–986 Fig. 2 Celleporaria inaudita. a General aspect of the colony surface, with vicarious avicularia. b Autozooid orifices, vicarious avicularia and ooecia. c Ooecia in unbleached specimen. d Vicarious avicularia. e, f, g, h Morphological variability between orifices and suboral avicularia proximal portion. Small triangular avicularia directed to the elongated and spatulate of variable morphology, covering al- margin of the zooid, lightly raised, and with the margins most the whole frontal wall of the zooid. Ovicell slightly serrated. Large, spatulate avicularia not common, sit- hyperstomial, ooecium formed by the distal autozooid, glob- uated close to the orifice and directed proximally, rostrum ular, about as wide as long, ectooecium perforated by Table 1 Measurements (in mm) Mean SD Minimum Maximum N of Celleporaria inaudita Zooidal orifice length 0.147 0.0107 0.126 0.169 19 Zooidal orifice width 0.169 0.0168 0.147 0.204 19 Spatulate avicularia length 0.430 0.0148 0.411 0.448 6 Spatulate avicularia width 0.192 0.0110 0.175 0.204 6 Ooecium length 0.130 0,0186 0,094 0,175 11 Ooecium width 0.275 0.0191 0.228 0.299 11 SD standard deviation, N number of measurements Mar Biodiv (2018) 48:977–986 981 Fig. 3 Parasmittina alba. a General view of the colony margin. b Autozooid orifice, with condiles and the base of oral spines. c Autozooids with lateral small triangular avicularia. d Autozooids with latero-suboral oval avicularia. e Spatulate avicularia. f, g Ovicellate zooids with variability in the morphology of the ooecia. h Detail of ovicell; arrows indicate symmetrical notches in the distal margin of the orifice numerous, although variable in number, irregularly-shaped and had not been recorded elsewhere until now. Some pseudopores. Secondary calcification very variable in devel- differences are noted between the original material and opment, covering the distal and lateral portions of the ovicell, our specimens; mainly in the figured ovicells the ectooecium visible only in the circular frontal–proximal (Ramalho et al. 2011:Fig. 2b, h), which have large area. pores in the ectooecium, but are smaller in our speci- Distribution mens. This difference could be attributed to the vari- Only known previously from Arraial do Cabo, Rio de ability of this structure and difference in level of cal- Janeiro, Brazil. Now present in Porto Santo and Madeira cification, as was observed by us between colonies Island (Calheta and Caniçal), Portugal. and even between ovicells in the same colony Remarks (Fig. 3f, g, h). Madeira specimens have two symmet- The specimens found in Madeira fully match the rical notches in the distal margin of the orifice in morphological characteristics given for Parasmittina ovicellate zooids (Fig. 3h); this structure was also not- alba. This species was described from Arraial do ed in P. alba from Arraial do Cabo (Fig. 2g and h in Cabo in Rio de Janeiro, Brazil (Ramalho et al. 2011) Ramalho et al. 2011), although comments about this 982 Mar Biodiv (2018) 48:977–986 Table 2 Measurements (in mm) Mean SD Minimum Maximum N of Parasmittina alba Zooidal length 0.488 0.0697 0.390 0.670 24 Zooidal width 0.340 0.0580 0.240 0.460 24 Primary orifice length 0.082 0.0056 0.076 0.101 20 Primary orifice width 0.125 0.0102 0.103 0.143 20 Oval avicularia length 0.092 0.0095 0.074 0.104 9 Oval avicularia width 0.056 0.0037 0.051 0.063 9 Pointed avicularia length 0.078 0.0067 0.068 0.089 10 Pointed avicularia width 0.047 0.0050 0.037 0.054 10 Ooecium length 0.265 0.0177 0.235 0.297 20 Ooecium width 0.267 0.0184 0.233 0.300 20 SD standard deviation, N number of measurements were not included in the original description. Only one peristome, laterally more developed, proximally poorly devel- avicularium per autozooid is indicated in the original oped and distally interrupted by one (in some cases two) distal description, while two triangular avicularia were ob- spines. This peristome is not visible when the secondary cal- served in one ovicellate zooid, but this seems very cification is more developed. Proximal border of the orifice infrequent. In addition, the adventitious avicularia with a variable lyrula, usually short and occupying from one were not seen in our specimens. quarter to two third of the proximal border. Condyles stout, This species is very similar to Parasmittina betamorphaea sharply pointed. Avicularia monomorphic, oval (lightly point- Winston 2005, distributed in the Gulf of Mexico and Brazil. ed when is in direct contact with the margin of the zooid), very But according to Ramalho et al. (2011) Parasmittina alba is numerous in some parts of the colony, but always two or more differentiated by the presence of more than one avicularium per zooid. The avicularia occur on the margins of the zooids. per zooid in P. betamorphaea, lacking the serrated rostrum in Rostrum is slightly spatulate. Ovicell subimmersed, and be- small avicularia, possessing the giant avicularia with a more coming endozooidal because of the strong secondary calcifi- rounded rostrum, and by the different positioning and shape of cation. Ooecium formed by the distal autozooid. Ectooecium the pores in the ovicell. Much of the difference between these almost flat frontally, with several irregularly-shaped species, in the ovicell and avicularia morphology, is attributed pseudopores. The secondary calcification covers the distal, to characters that are very variable between colonies or even lateral and, in some cases, the proximal part of the ectooecium, between zooids in the same colony. In the figures of the orig- leaving only a central area with exposed pseudopores. In some inal description of P. betamorphaea, it is not possible to see ovicells only the peripheral area of the secondary calcification more than one avicularium per zooid. Both species, P. alba is truly calcified, whereas the rest is membraneous, in cleaned and P. betamorphaea, were described from only two colonies, specimens showing the ectooecium with pseudopores which indicates that more specimens should be studied more underneath. carefully, particularly to examine the intra-colonial variability Distribution and to evaluate the possibility of the two species being Currently only known from Porto Santo Island, Madeira, synonyms. Portugal. Parasmittina multiaviculata sp. nov. Remarks (Fig. 4, Table 3) According to the literature, only two species of this Material examined: Holotype: MMF44616 from Porto genus were previously recorded in Madeira, Santo; Paratype: MMF44617 from Porto Santo. Parasmittina trispinosa (Johnston, 1825) by Waters Etymology: In reference to the numerous avicularia per (1899)and Norman (1909)and Parasmittina protecta zooid. (Thornely, 1905) by Canning-Clode et al. (2013a). The Description two colonies reported in the current study show signif- Colony encrusting, unilaminar or multilaminar, initially icant differences from these two species and from the translucent. Rectangular to hexagonal autozooids in the first previously described species, P. alba. According to layer and more irregular in the second layers. Frontal wall Harmelin et al. (2009), P. protecta presents a peristome nodular, with marginal large pores. Orifice longer than wide, interrupted distally, and raised proximally; the orifice is surrounded by a normally rectangular (but very variable in broader than high, and the avicularia are infrequent and when present, they occur in two morphologies and are morphology, and more rounded in ovicellated zooids) Mar Biodiv (2018) 48:977–986 983 Fig. 4 Parasmittina multiaviculata sp. nov. a General view of the autozooids and ooecia in an unbleached specimen. b Bleached specimen, showing ooecia and abundant frontal avicularia. c Ovicellate zooids and frontal avicularia. d, e Primary orifice with variations in the lyrula morphology. f Condile. g Bleached ovicellate and non ovicellate zooids. h Ovicellate zooid in unbleached specimen large. According to the descriptions by Hayward and specimens are similar to Parasmittina inalienata Tilbrook Ryland (1999) and Soule and Soule (2002), 2006, described from the Solomon and Fiji Islands; but differ P. trispinosa presents an orbicular orifice with a big from that species by having a slightly bigger orifice with a triangular avicularium lateral to the orifice, which is, wider lyrula, (Fig. 35D in Tilbrook 2006), less globular in some cases, replaced by a smaller avicularium. ovicells which are almost flat in the frontal plane, and by Furthermore, the ovicells in P. trispinosa are character- lacking a round peristome in the ovicellate zooids. The ized by having few, irregular large pores. avicularia of P. inalienata seem to be numerous with a slightly The genus Parasmittina is very specious with currently spatulate rostrum which is always directed proximo-medially 122 known species (Bock 2015a; WoRMS 2015), distributed or medially, while in the Madeira specimens, the direction of around all oceans, but with a high number of species in the the rostrum is disordered, without a clear pattern, and the Pacific and Indian Oceans. Among this diversity, there are few rostrum in some cases is slightly pointed. species that have an orifice that is longer than wide, mono- Most species of this genus (c. 99 species) seem to be morphic avicularia, and one or two distal oral spines. Madeira natives from the Pacific and Indian Oceans (e.g., 984 Mar Biodiv (2018) 48:977–986 Table 3 Measurements (in mm) Mean SD Minimum Maximum N of Parasmittina multiaviculata sp nov Zooidal length 0.576 0.0719 0.464 0.720 14 Zooidal width 0.366 0.0392 0.307 0.429 14 Primary orifice length 0.110 0.0076 0.093 0.124 14 Primary orifice width 0.081 0.0081 0.079 0.109 14 Avicularia length 0.103 0.0161 0.065 0.130 18 Avicularia width 0.050 0.0082 0.036 0.062 18 Ooecium length 0.218 0.0125 0.198 0.241 18 Ooecium width 0.275 0.0158 0.249 0.297 18 SD standard deviation, N number of measurements Tilbrook et al. 2001;Tilbrook 2006; Soule and Soule the extent by which these species have established themselves 1973, 2002;Gordon 1984, 1989;Hayward 1988;Bock in the natural environment. 2015a;Seo 2002; Hayward and Parker 1994), and are The natural fauna of Madeira shows close affinities with particularly abundant in coral reef habitats (Hayward the fauna of Lusitania, Mediterranean, and Mauritanian re- and Parker 1994). Several other Parasmittina species gions (Wirtz 1998); nevertheless, the three species of bryo- identified or recorded from other oceans and seas are zoans found here show closer affinities with species from the considered non-indigenous (e.g., Harmelin et al. 2009). Pacific (C. inaudita, P. multiaviculata sp. nov.) and the The exclusive presence of Parasmittina multiaviculata Caribbean (P.alba). Several Brazilian and Caribbean species sp. nov. on artificial plates deployed in harbors in of macroinvertebrates were detected in recent years in Madeira, and the fact that there are no previous records Madeiran waters (e.g., Wirtz and Canning-Clode 2009; of similar species in the area, suggests this could be a Canning-Clode et al. 2013a, b; Ramalhosa et al. 2014; Souto new introduction. The presence of this species in only et al. 2015). Beania maxilladentata Ramalho, Muricy and one locality may indicate a recent introduction. Its mor- Taylor 2008, a bryozoan only previously known from Brazil phological proximity to P. inalienata could indicate (Ramalho et al. 2008; Vieira et al. 2010), was also found in Parasmittina multiaviculata sp. nov. may have a Madeiran waters (Souto et al. 2015), but in this case, only on Pacific origin. natural substrates. In addition, several other species with West Atlantic distributions, mainly from the Gulf of Mexico, were also recently found in Madeira (Canning-Clode et al. 2013a; Discussion Ramalhosa et al. 2014) such as the bryozoans Schizoporella pungens (Canu and Bassler 1928), Cradoscrupocellaria Knowledge of the Madeira marine invertebrate fauna is scarce bertholetti (Audouin 1826), Amathia verticillata (Delle and in the case of bryozoans, very limited (Busk 1858a, b, Chiaje 1822), the ascidian Distaplia corolla Monniot F. 1859, 1860, 1861;Hincks 1880; Johnson 1897; Waters 1899; 1974 and the sabellid polychaete Branchiomma bairdi Norman 1909). However, in recent years, monitoring surveys (McIntosh 1885). Also a few species from the Indo-Pacific for non-indigenous species in the archipelago has resulted in region were detected (Norman 1909; Canning-Clode et al. new records and undescribed species in the islands (d’Hondt 2013a; Ramalhosa et al. 2014; Ramalhosa and Canning- 1985; Alves and Cocito 2002; Berning and Kukliński 2008; Clode 2015), but most of these species appeared first in Berning et al. 2008; Wirtz and Canning-Clode 2009; Berning European waters (e.g., Cabezas et al. 2015; Arias et al. 2012;Souto etal. 2014, 2015; Ramalhosa et al. 2016). 2013;Cinar 2009; Giangrande et al. 2013; Garcia Raso Nevertheless, the lack of a comprehensive checklist of bryo- 1981; Turon et al. 2005;Rylandetal. 2009, 2011). zoans in Madeira makes the detection and dating of new an- Nevertheless, none of the three species reported in the current thropogenic introductions a complex challenge. Due to the paper were recorded in other areas close to Madeira. Of them, sessile mode of life of their adults and the estimated short- only Celleporaria inaudita was recently found in the Red Sea, lived non-feeding pelagic phase of their larvae, the presence after its original description in the Pacific Ocean. The direct of the three species reported here in Madeiran waters is diffi- introduction of these species from their original localities to cult to explain by natural dispersion methods, so anthropogen- Madeira seems not very plausible. It is possible that these ic vectors seem more reasonable. The presence in other sub- species have a broader distribution than currently known, par- strates different from the settlement panels (natural or artifi- ticularly in European and North African waters, and have been cial) was not checked, so no inferences can be made regarding probably introduced to Madeira via hull fouling (recreational Mar Biodiv (2018) 48:977–986 985 Arias A, Giangrande A, Gambi MC, Anadon N (2013) Biology and new and/or cruise vessels). Currently, most shipping can be attrib- records of the invasive species Branchiomma bairdi (Annelida: uted to tourist cruise ships and sailing yachts visiting for re- Sabellidae) in the Mediterranean Sea. Mediterr Mar Sci 14:162–171 fuel and rest stops from different parts of the world (APRAM Berning B (2012) Taxonomic notes on some Cheilostomata (Bryozoa) 2014). Furthermore, recent findings by Ramalhosa et al. from Madeira. Zootaxa 3236:36–54 Berning B, Kukliński P (2008) North-east Atlantic and Mediterranean (2016) have shown that dry dock inspections on local and species of the genus Buffonellaria (Bryozoa, Cheilostomata): impli- foreign recreational vessels support the hypothesis from other cations for biodiversity and biogeography. Zool J Linn Soc 152: studies, that emphasize hull fouling as the key introduction 537–566. doi:10.1111/j.1096-3642.2007.00379.x vector that contribute to the arrival and spread of NIS to Berning B, Tilbrook KJ, Rosso A (2008) Revision of the north-eastern Atlantic and Mediterranean species of the genera Herentia and neighbouring islands. Moreover, the genus Parasmittina is a Therenia (Bryozoa: Cheilostomata). J Nat Hist 42:1509–1547 very specious genus with currently 122 known species (Bock Berning B, Tilbrook KJ, Ostrovsky AN (2014) What, if anything, is a 2015a; WoRMS 2015) and 17 fossil species. Similar diversity lyrula? In: Rosso A, Wyse Jackson PN, Porter JS (eds) Bryozoan is present in the Celleporaria genus, with 90 species (Bock Studies, Museo delle Scienze, Trento pp 21–28 2015b). This large number of species in these genera makes Bock P (2015) Recent and fossil Bryozoa: Parasmittina Osburn, 1952. Available from: http://www.bryozoa.net/cheilostomata/smittinidae/parasmittina.html. correct identification challenging, possibly resulting in some Accessed 16 September 2015) species being misidentified and lumped together. So records in Bock P (2015) Celleporaria Lamouroux, 1821. In: Bock P, Gordon D other parts of the world of these species could go unnoticed. (2015) World List of Bryozoa. Accessed through: World Register of Here, three species of bryozoans are added to the nine other Marine Species at http://www.marinespecies.org/aphia.php?p= taxdetails&id=205020. Accessed16June2016 non-indigenous bryozoan species known from the Madeira Busk G (1858a) Zoophytology. On some Madeiran Polyzoa. Quart J archipelago (Wirtz and Canning-Clode 2009; Canning-Clode Micros Sci 6:124–130 et al. 2013a; Ramalhosa et al. 2016). Currently, the Busk G (1858b) Zoophytology. On some Madeiran Polyzoa. Quart J xenodiversity in Madeira Island is probably underestimated, Micros Sci 6:261–263 and therefore this number is likely to increase in the next Busk G (1859) Zoophytology. On some Madeiran Polyzoa. Quart J Micros Sci 7:65–67 years. Busk G (1860) Zoophytology. Catalogue of the Polyzoa collected by J.Y. Johnson, Esq., at Madeira, in the years 1859 and 1860, with descrip- tions of new species. Quart J Micros Sci 8(213–214):280–285 Acknowledgments Open access funding provided by Univeristy of Busk G (1861) Description of new Polyzoa collected by J.Y.Johnston Vienna. Esq., at Madeira. Quart J Micros Sci New Ser 1:77–80 We are grateful to Oscar Reverter-Gil and Linda McCann for the Cabezas MP, Xavier R, Branco M, Santos AM, Guerra-García JM (2015) valuable revision of an earlier version of this manuscript. Thanks also Invasion history of Caprella scaura Templeton, 1836 (Amphipoda: to Kevin Tilbrook and Andrew Ostrovsky for their comments that helped Caprellidae) in the Iberian Peninsula: multiple introductions re- to improve this paper. The work of J.S. was supported by the Austrian vealed by mitochondrial sequence data. Biol Invasions 16:2221– Science Fund (FWF, Lise Meitner Program M1444-B25 and Project Number AP28954-B29). P. Ramalhosa holds a research fellowship in the Project M1420-01-0145-FEDER-000001 — project Observatório Canning-Clode J (2015) General introduction: aquatic and terrestrial bi- Oceânico da Madeira (OOM). J. Canning-Clode was supported by a ological invasions in the 21st century. In: Canning-Clode J (ed) starting grant in the framework of the 2014 FCT Investigator Biological invasions in changing ecosystems: vectors, ecological Programme (IF/01606/2014/CP1230/CT0001). We thank Porto Santo impacts, management and predictions. De Gruyter Open, Berlin, Line for their travel aid to the Island of Porto Santo, and the administra- pp 13–20 tion of the four marinas monitored in this study (Porto Recreio da Calheta, Canning-Clode J, Fofonoff P, McCann L, Carlton JT, Ruiz G (2013a) Marina do Funchal, Marina da Quinta do Lorde and Marina do Porto Marine invasions on a subtropical island: fouling studies and new Santo). This is contribution number 32 of the Marine Biology Station records in a recent marina on Madeira Island (East Atlantic Ocean). of Funchal. Finally, we are grateful to the anonymous reviewers and Dr Aquat Invasion 8:261–270 A. Waeschenbach for their valuable revision and comments. Canning-Clode J, Souto J, McCann L (2013b) First record of Celleporaria brunnea (Bryozoa: Lepraliellidae) in Portugal and in Open Access This article is distributed under the terms of the Creative he East Atlantic. Mar Biodivers Rec 6, e108 Commons Attribution 4.0 International License (http:// Carlton JT, Hodder J (1995) Biogeography and dispersal of coastal ma- creativecommons.org/licenses/by/4.0/), which permits unrestricted use, rine organisms: experimental studies on a replica of a 16th-century distribution, and reproduction in any medium, provided you give appro- sailing vessel. Mar Biol 121:721–730 priate credit to the original author(s) and the source, provide a link to the Cinar ME (2009) Alien polychaete species (Annelida: Polychaeta) on the Creative Commons license, and indicate if changes were made. southern coast of Turkey (Levantine SEA, eastern Mediterranean), with 13 new records for Mediterranean Sea. 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Marine BiodiversitySpringer Journals

Published: Oct 22, 2016

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