INTRODUCTION
The genus Scrupocellaria van Beneden, Reference Van Beneden1845 comprises about 80 extant species of Candidae (Bock, Reference Bock2012) characterized by bifurcation type 8 (acc. Harmer, Reference Harmer1923) and zooids with a basal vibracular chamber. Despite the morphological variations found among species assigned to Scrupocellaria (e.g. shape of zooids, opesia and polymorph structures; see Harmer, Reference Harmer1926), only one species has been reassigned to a distinct subgenus. The subgenus Retiscrupocellaria d'Hondt, Reference d'Hondt1988, erected for Acamarchis jolloisii Audouin, Reference Audouin and Panckoucke1826, is distinguished by branches joined by transversal tubes and basal vibracular chambers with an oblique groove to the axis. No additional records or taxonomic information have been published on this subgenus since its description, and a thorough search of the bryozoan taxonomic literature revealed that van Beneden (1850) had already introduced a new genus Licornia for Acamarchis jolloisii, giving that name priority.
Acamarchis jolloisii was described from Egypt (Audouin, Reference Audouin and Panckoucke1826), and later recorded in the Red Sea by Waters (Reference Waters1909) under two different names, Scrupocellaria jolloisii, for specimens with spines, and a new species Scrupocellaria mansueta Waters, characterized by unarmed zooids. Both were synonymized by d'Hondt (Reference d'Hondt1988) under S. jolloisi (incorrect subsequent spelling). Waters (Reference Waters1909) noted the absence of Scrupocellaria jolloisii in the Suez Canal, but Hastings (Reference Hastings1927) later reported its occurrence from the Suez Canal (Port Said area, Egypt). D'Hondt (1988) reported the species from the Mediterranean coast of Israel.
The present study includes a description of the genus Licornia and the type species, Licornia jolloisii. Additional information on the genus Licornia is provided, and new combinations for nine species previously assigned to Scrupocellaria are established. We also report Licornia jolloisii for the first time outside the Red Sea and Mediterranean waters; newly invasive for the south-eastern Atlantic coast of the United States of America and the north-eastern coast of Brazil.
MATERIALS AND METHODS
Western Atlantic material of Licornia jolloisii was obtained from 1–2 m of water under overhangs in the limestone walls of a man-made canal at Big Torch Key, one of the Florida Keys. It was collected in December, 2005 by Don De Maria of Sea Samples, Summerland Key, Florida. North-eastern Brazilian specimens were obtained from 1 m depth on artificial substratum at Itaparica, Todos os Santos Bay, Bahia state. They were collected in January, 2011 by Laura Pioli Kremer and in February, 2012 by Rosana Moreira Rocha from fouling panel samples. Voucher specimens were deposited at the Virginia Museum of Natural History (VMNH, USA) and Museu de Zoologia da Universidade de São Paulo (MZUSP, Brazil). Comparative specimens listed are deposited at the Natural History Museum, London (NHMUK, UK), Museum of Tropical Queensland, Townsville (MTQ, Australia), Museum Victoria (NMV, Australia), Santa Barbara Museum of Natural History (SBMNH, USA) and the Smithsonian Institution, National Museum of Natural History (NMNH, USA). In addition to the comparative material, type and non-type specimens of Scrupocellaria deposited in different collections, including those of American Museum of Natural History (AMNH, USA), Museum of Comparative Zoology (MCZ, USA) and Muséum national d'Histoire naturelle (MNHN, France) were also examined.
All colonies were examined under a stereomicroscope and selected specimens were mounted for examination in a scanning electron microscope (SEM), a Zeiss EVO-60 at the VMNH for coated specimens and an SEM with an environmental chamber, a LEO 1455-VP at the NHMUK for uncoated specimens. Measurements were made from digital SEM images using the analysing software ImageJ®.
SYSTEMATICS
Class GYMNOLAEMATA Allman, Reference Allman1856
Order CHEILOSTOMATA Busk, Reference Busk and MacGillivray1852
Suborder NEOCHEILOSTOMINA d'Hondt, Reference d'Hondt1985
Infraorder FLUSTRINA Smitt, Reference Smitt1868
Family CANDIDAE d'Orbigny, Reference d'Orbigny1851
Genus Licornia van Beneden, 1850
TYPE SPECIES
Acamarchis jollaisii (sic) Audouin, Reference Audouin and Panckoucke1826 (misspelling of Acamarchis jolloisii Audouin) by original designation.
SYNONYM
Retiscrupocellaria d'Hondt, Reference d'Hondt1988 [Type species: Acamarchis jolloisi Audouin, Reference Audouin and Panckoucke1826 (incorrect subsequent spelling) by original designation, see d'Hondt (Reference d'Hondt1988), p. 198]
DIAGNOSIS
Candidae having almost rectangular zooids with broadly oval opesia occupying most of the frontal surface, and with anastomosing tubes connecting the colony branches. Joints crossing the proximal opesia of outer zooids and below the opesia of the inner zooids at the bifurcation. Cryptocyst vestigial or absent. Frontal scuta and oral spines often present. Frontal avicularia present, triangular to aquiline. Vibracular chamber tapering distally, triangular to drop-shaped, with a proximal rhizoidal foramen; uncurved setal groove directed obliquely to the axis of the internode and occupying about two-thirds of vibracular chamber length; single axial vibraculum. Ooecia with porous ectooecium.
REMARKS
Bryozoan taxonomists have long considered Scrupocellaria van Beneden, Reference Van Beneden1845 to be a well-defined genus. Mixtures of characters, however, are observed among the many species assigned to this genus: viz. ovicells with single fenestra or with many pores, variable shape and size of opesia, basal vibracular chamber, and frontal and lateral avicularia (Tilbrook & Vieira, Reference Tilbrook and Vieira2012). D'Hondt (1988) also recognized the presence of shared characteristics between Acamarchis jolloisii and some other species of both Scrupocellaria and Canda, and designated a new subgenus, Retiscrupocellaria. This subgenus was characterized as having anastomosing tubes connecting the colony branches, as in Canda Lamouroux, Reference Lamouroux1816—but having internodes with zooids in a single plane, unlike Canda which has zooids in two series with their frontal surfaces facing obliquely outwards from the axis—having a vibracular chamber at the proximal end of the basal zooidal surface (as in Scrupocellaria), having colonies with planar branches (as in Scrupocellaria), but being distinct from Canda and Scrupocellaria in having a dagger-shaped scutum. On the basis of these differences in morphological characters between Acamarchis jolloisii and some other Scrupocellaria we also consider Retiscrupocellaria a distinct taxon.
However, Van Beneden (Reference Van Beneden1850) had already erected a new genus, Licornia, for Acamarchis jollaisii (sic) Audouin, although its morphological features or distinctions were not described in the original publication. This genus name has not been used since its original description, but according to the principle of priority of ICZN (1999, Art. 23), Retiscrupocellaria d'Hondt, Reference d'Hondt1988 must be considered a junior synonym of Licornia van Beneden, 1850 and no reversal of precedence can be applied (ICZN, 1999, Art. 23.9).
Despite the absence of morphological unity in the genus Scrupocellaria (see Tilbrook & Vieira, Reference Tilbrook and Vieira2012), the genus (and those species to be included within the genus) must include most of the diagnostic characteristics observed in the type species Scrupocellaria scruposa, viz. (i) joints crossing the proximal opesia of outer zooids and below the opesia of the inner zooids at the bifurcation, (ii) aquiline lateral avicularium, (iii) vibraculum with slightly curved setal groove obliquely directed and occupying two-thirds of vibraculum length, (iv) two axial vibracula, (v) ovicell with single small ectooecial fenestra and with an associated avicularium (Figure 1A, B). We used five morphological characteristics to define Licornia and distinguish species belonging to the genus from some of the species previously assigned to Scrupocellaria: (i) joints crossing the proximal opesia of outer zooids and below the opesia of the inner zooids at the bifurcation (Figure 1C), (ii) lateral avicularia with straight rostrum (Figure 1C), (iii) vibracular chamber almost triangular with oblique to the axis and uncurved setal groove occupying two-thirds of vibracular chamber length (Figure 1D), (iv) single axial vibraculum (Figure 1D) and (v) ooecia with a porous ectooecium (Figure 1C). The combination of porous ectooecium, uncurved oblique setal groove occupying two-thirds of vibracular chamber length, and single axial vibraculum does not occur in other species of Canda and Scrupocellaria with the exception of Licornia jolloisii and the other nine species assigned to the genus (see below).
Licornia jolloisii (Audouin, Reference Audouin and Panckoucke1826)
(Figures 1C, D, 2A–F, 7A, B; Table 1)
Acamarchis jolloisii Audouin, Reference Audouin and Panckoucke1826: [figured by Savigny, 1817].
Scrupocellaria jolloisii: Waters, Reference Waters1909; Hastings, Reference Hastings1927.
Scrupocellaria mansueta Waters, Reference Waters1909.
Scrupocellaria (Retiscrupocellaria) jolloisi (sic): d'Hondt, Reference d'Hondt1988.
Retiscrupocellaria jolloisii: d'Hondt, Reference d'Hondt2006.
Fig. 1. Morphological differences between the type species of Scrupocellaria and Licornia: (A, B) Scrupocellaria scruposa (Linnaeus, Reference Linnaeus1758), NHMUK 1847.9.15.28, British waters; see the small avicularium at the distal edge of the ooecium (white arrow); (C, D) Licornia jolloisii (Audouin, Reference Audouin and Panckoucke1826), NHMUK 1926.9.6.84, neotype, Red Sea. Scale bars: A, B: 0.1 mm; C, D: 0.2 mm.
Table 1. Measurements (mm) of neotype of Licornia jolloisii (Audouin, Reference Audouin and Panckoucke1826) from Red Sea (NHMUK 1926.9.6.84).
Min: minimum; Max: maximum; N: number; SE: standard error.
TYPE MATERIAL
Neotype (choosen here): Red Sea [NHMUK 1926.9.6.84, Figures 1C, D, 2A–C].
Fig. 2. Licornia jolloisii (Audouin, Reference Audouin and Panckoucke1826): (A, B, C) NHMUK 1926.9.6.84, neotype, Red Sea; (D, E, F) VMNH 13708.0000, Florida, USA. Scale bars: A: 0.4 mm; B, C, D, E, F: 0.2 mm.
ADDITIONAL MATERIAL
Licornia jolloisii (Audouin, Reference Audouin and Panckoucke1826). Scrupocellaria jolloisii, A.B. Hastings det., Red Sea [NHMUK 1926.9.6.85–94]; OM9G-0366-5, 24o25′18.80″S 81o15′23.50″W, Florida, Big Torch Key, #2, collected on 11 December 2005 by Don De Maria, 1–2 m, on limestone [acc. no.2009-015, VMNH 13708.0000, Figure 2D–F]; 12o53′21″S 38o41′03″W, Itaparica, Baía de Todos os Santos, Bahia, Brazil, collected on January 2011 by Laura P. Kremer, 1 m, on panels [MZUSP 1001–1004].
REDESCRIPTION
Colony erect, branched, with branches comprising 5–17 zooids, sometimes joined by anastomosing transversal tubes, pale reddish brown in colour in life. Internode almost straight, with chitinous joints passing across the proximal opesia in both outer zooids at the branch bifurcation. Autozooids elongate, almost rectangular, slightly wider distally than proximally, with curved distal edges. Oval opesia occupying three-quarters of the zooidal length, broader distally. Cryptocyst absent. Scutum often present, inserted at midline or slightly distal of inner edge of the opesia, spine-like, shaped like a stout, straight elephant tusk, obliquely directed forward and over frontal membrane. One outer and one inner oral spine, vestigial, often absent. Axial zooid without oral spines, or rarely with 1–2 vestigial oral spines. A lateral avicularium present near distal outer edge in each zooid, small, laterally directed; rostrum triangular with hooked mandible. Frontal avicularia (sometimes absent) at inner proximal margin of opesia, monomorphic; rostrum triangular, serrated, angled proximally, triangular mandible hooked distally. A vibracular chamber present on basal surface of each zooid, sometimes inconspicuous in frontal view, tapering distally, almost triangular, small, with oblique setal groove and one proximal rhizoidal foramen; uncurved setal groove occupying two-thirds of the vibracular chamber length; vibracular setae smooth, as long as two zooids. Single axial vibraculum, with proximal rhizoidal foramen. Rhizoids tubular with some retroussé hooks. Ovicells almost globular, with ectooecium perforated by funnel-shaped elongate to circular pores.
TAXONOMIC REMARKS
Acamarchis jolloisii was described by Audouin (Reference Audouin and Panckoucke1826) based on Egyptian specimens figured by Savigny (Reference Savigny1817). Audouin (Reference Audouin and Panckoucke1826) dedicated the species to Mr Jollois, genitive ending –ii, the genitive ending for the Latinized version ‘jolloisius’ of that personal name. As was true for other taxonomic authors of the time Audouin did not explain whether species names based on personal names were Latinized or not, and of the names he used, some have –i endings and some –ii. Since his choice of endings appears to have been deliberate and not a case of lack of knowledge of Latinization, it seems preferable to leave his endings as they stand (ICZN, 1999, Art. 31.1.3) rather than emend them all to follow one pattern.
No type material exists for Acamarchis jolloisii. Therefore, we here designate a neotype from the Red Sea (NHMUK 1926.9.6.84) that is consistent with Savigny's original figures and with the most recent redescription of the species given by d'Hondt (Reference d'Hondt1988).
Waters (Reference Waters1909) described a new species from the Red Sea, Scrupocellaria mansueta, distinct from L. jolloisii only by the absence of scuta and oral spines in many zooids. We did not have the opportunity to search the remaining original material of the Waters Collection at Manchester Museum to learn if that material still exists (Winston & Woollacott Reference Winston and Woollacott2008:192, explains some of the history of the Waters Collection). In all examined specimens from the Red Sea, Suez Canal, Florida and Brazil, however, the presence or absence of oral spines, as well as of the stout spiny scuta, changes randomly along the branches of L. jolloisii (Figures 1C, 2A). Therefore S. mansueta was considered by Hastings (1929) and d'Hondt (Reference d'Hondt1988) to be a junior subjective synonym of Licornia jolloisii, a decision with which we agree.
ADDITIONAL SPECIES OF LICORNIA EXAMINED
Licornia annectens (MacGillivray, Reference MacGillivray1887) comb. nov. Syntypes: Scrupocellaria annectens MacGillivray, MacGillivray det., 3 microslides, Gaspar Strait, Indonesia, Indian Ocean [NMV F.45606.1–3, the balsam slide specimens could not be examined with SEM, but the light microscopy images of these specimens can be found at the home page of Museum Victoria – http://collections.museumvictoria.com.au].
Licornia cervicornis (Busk, Reference Busk and MacGillivray1852) comb. nov. Holotype: Scrupocellaria cervicornis Busk, G. Busk det., British Museum Catalogue Collection, Voyage of HMS ‘Rattlesnake’, off Cumberland Island, 45.7 m (25 fms) [NMHUK 1854.11.15.81]. Paratypes: Scrupocellaria cervicornis Busk, G. Busk det., Voyage of HMS ‘Rattlesnake’, Australia [NMHUK 1899.7.1.4552–3]. Additional specimens: Scrupocellaria diadema Busk, S. Harmer det., Siboga Expedition, St. 163, specimen 501.G4, Malay Archipelago, Seget, N. end of New Guinea, 29 m [NHMUK 1928.3.6.180, Figure 3A, B].
Fig. 3. Species of Scrupocellaria herein reassigned to Licornia: (A, B) Licornia cervicornis (Busk, Reference Busk and MacGillivray1852) comb. nov., NHMUK 1928.3.6.180, north of New Guinea; (C, D) Licornia cyclostoma (Busk, Reference Busk and MacGillivray1852) comb. nov., NHMUK 1899.6.1.340, Port Phillip Heads, Australia; (E, F) Licornia diadema (Busk, Reference Busk and MacGillivray1852) comb. nov., NHMUK 1854.11.15.80, holotype, Moreton Bay, Australia. Scale bars: A, B, E, FL 0.2 mm; C, D: 0.4 mm.
Licornia cyclostoma (Busk, Reference Busk and MacGillivray1852) comb. nov. Holotype: Scrupocellaria cyclostoma Busk, G. Busk det., British Museum Catalogue Collection, Voyage of HMS ‘Rattlesnake’, Bass Straits, Australia, 82.3 m (45 fms) [NHMUK 1854.11.15.77]. Additional specimen: Scrupocellaria annectens MacGillivray, T. Hincks det., Port Phillip Heads, Victoria, Australia (= Scrupocellaria cyclostoma Busk, S. Harmer det., 12.7.1922) [NHMUK 1899.6.1.340, Figure 3C, D].
Licornia diadema (Busk, Reference Busk and MacGillivray1852) comb. nov. Holotype: Scrupocellaria diadema Busk, G. Busk det., British Museum Catalogue Collection, Voyage of HMS ‘Rattlesnake’, Moreton Bay [NHMUK 1854.11.15.80, Figure 3E, F]. Additional specimens: Scrupocellaria diadema Busk, Canu & Bassler det., US Fish Commission Steamer Albatross, St. 5478, off Tacbuc Point, East Leyte, Philippines, 104 m (57 fms) [NMNH 7894]; Scrupocellaria diadema Busk, Great Barrier Reef Expedition, St. 12, collected on 24 February 1929 [NMNH 9565].
Licornia gaspari (Thornely, Reference Thornely1907) comb. nov. Syntypes: Scrupocellaria gaspari Thornely, L. Thornely det., Gaspar Strait, Indonesia [NHMUK 1936.12.30.146, Figure 4A, B; 1907.8.24.1pt]; Scrupocellaria gaspari Thornely, L. Thornely det., Andaman Islands, Indian [NHMUK 1936.12.30.126; NHMUK 1936.12.30.136].
Fig. 4. Species of Scrupocellaria herein reassigned to Licornia: (A, B) Licornia gaspari (Thornely, Reference Thornely1907) comb. nov., NHMUK 1936.12.30.146, Syntype, Gaspar Strait, Indonesia; (C, D) Licornia ferox (Busk, Reference Busk and MacGillivray1852) comb. nov., NHMUK 1928.3.6.156, Java; (E, F) Licornia longispinosa (Harmer, Reference Harmer1926) comb. nov., Schizoholotype, NHMUK 1928.3.6.189, Maluku Islands, Indonesia. Scale bars: A, B, D, E, F: 0.4 mm; C: 0.2 mm.
Licornia ferox (Busk, 1852) comb. nov. Holotype: Scrupocellaria ferox Busk, G. Busk det., British Museum Catalogue Collection, Voyage of HMS ‘Rattlesnake’, Louisiade Archipelago [NHMUK 1854.11.15.76]; balsam slide with part of holotype (schizoholotype), mounted by S. Harmer, 28.vi.1922 [NHMUK 1899.7.1.6540]. Additional specimen: Scrupocellaria ferox Busk, S. Harmer det., ‘Siboga’ Expedition, St. 7, specimen 2.A2, Batjulmati, Java, coral reef [NHMUK 1928.3.6.156, Figure 4C, D].
Licornia longispinosa (Harmer, Reference Harmer1926) comb. nov. Holotype: Scrupocellaria longispinosa Harmer, S. Harmer det., ‘Siboga’ Expedition, St. 144, specimen 108.Ai, Maluku Islands, Indonesia, anchorage N of Solamakiëe, 07.viii.1899, 45 m [ZMA 01063au, schizoholotype; RMNH 00054, schizoholotype, NHMUK 1928.3.6.189–90, schizoholotypes, Figure 4E, F; NMNH 9389, schizoholotype].
Licornia macropora (Osburn, Reference Osburn1950) comb. nov. Paratypes: Scrupocellaria macropora Osburn, R. Osburn det., AHF 33, Allan Hancock Pacific Expedition, ‘Velero III’, St. 1162-40, 33o33′5″N 118o9′45″W, California, Orange County, 11 miles of South of Seal Beach, collected on 23 July 1940 [SBMNH 96151]; Scrupocellaria macropora Osburn, R. Osburn det., Allan Hancock Pacific Expedition, St. 1263-41, 1.5 miles off north end of Cedros Island, Mexico, Lower California, 82–100 m (45–55 fms) [NMNH 553519]. Additional specimen: US Fish Commision Steamer ‘Albatross’, station 2886, off Oregon Coast [NMNH 553520, Figure 5A, B].
Fig. 5. Species of Scrupocellaria herein reassigned to Licornia: (A, B) Licornia macropora (Osburn, Reference Osburn1950) comb. nov., NMNH 553520, off Oregon, USA; (C–F) two undescribed species of Licornia, previously assigned to Scrupocellaria diadema Busk, Reference Busk and MacGillivray1852: (C, D) NHMUK 1928.3.6.178, Malay Archipelago; (E, F) NHMUK 2005.7.27.12, Palau. Scale bars: A–F: 0.4 mm.
Licornia prolata (Tilbrook & Vieira, Reference Tilbrook and Vieira2012) comb. nov. Holotype: Scrupocellaria prolata Tilbrook & Vieira, Site 813, Sample Id 000125, SBD 001581, Great Barrier Reef, 18.635°S, 147.275°E, 18 September 2003 [MTQ G25341, figured by Tilbrook & Vieira, Reference Tilbrook and Vieira2012: fig. 10].
Licornia spp. (two undescribed species). Comparative material: Scrupocellaria diadema Harmer, S. Harmer det., Siboga Expedition, St. 99, specimen 68.B2, N. Ubian, Sulu Archipelago, 16–23 m [NHMUK 1928.3.6.178, Figure 5C, D]; Scrupocellaria diadema Harmer, P. Hayward det., Coral Reef Research Foundation, OCDN2370-L, KB CHAN, 07°19.24′N, 134°31.28′E, Palau, Channel between Koror and Babeldaod, 14.v.1994, 20 m [NHMUK 2005.7.27.12, Figure 5E, F].
REMARKS ON SPECIES OF LICORNIA
We examined in detail a huge range of material of Scrupocellaria deposited in different scientific collections and found some specimens that share the following characters with Licornia jolloisii: almost rectangular zooids with opesia occupying more than half of frontal area; joints passing across the proximal opesia in both outer zooids at the bifurcation; cryptocyst vestigial or absent; frontal scuta sometimes absent; small, almost triangular vibracular chamber with oblique and uncurved setal groove, single axial vibraculum, and ooecium with many ectooecial pores.
These characteristics are observed in Scrupocellaria diadema (see Harmer, Reference Harmer1926; Tilbrook & Vieira, Reference Tilbrook and Vieira2012), and this species is reassigned to Licornia.
Harmer (Reference Harmer1926) noted that many specimens previously assigned to L. diadema showed variation in the size of the vibracular chamber, the shape of scuta and the number of oral spines. However, despite the differences among specimens in material from Indo-Pacific waters, Harmer (Reference Harmer1926) synonymized three previously described species under Busk's L. diadema: Scrupocellaria cervicornis Busk, Reference Busk and MacGillivray1852, Scrupocellaria annectens MacGillivray, Reference MacGillivray1887, and Scrupocellaria gaspari Thornely, Reference Thornely1907. Our study shows that the type specimens of these three species belong to Licornia and that they are morphologically distinct from each other in autozooid shape, presence and shape of frontal scuta and the number of oral spines. Figure 3A, B shows L. cervicornis: with distinct large shield-shaped or heart-shaped scutum, very small lateral avicularium and frontal avicularium with a short base; Figure 4A, B show: L. gaspari, without scutum and 2–4 oral spines. L. annectens is a balsam slide specimens and no SEM image was possible, but it is distinct in having a small scutum present in ovicelled zooids and large frontal avicularia in axial zooids. All are distinct from Busk's L. diadema; e.g. Figure 3E, F which is characterized by possession of a gracile club-shaped scutum and aquiline frontal avicularia with a tubular base (Tilbrook & Vieira, Reference Tilbrook and Vieira2012).
Osburn (Reference Osburn1950) recorded 18 Scrupocellaria species from the Eastern Pacific, seven of them described as new to science. Examination of the Osburn's Scrupocellaria specimens deposited at the SBMNH and NMNH revealed one species, Licornia macropora (Osburn, Reference Osburn1950) (Figure 5A, B), which shares with Licornia jolloisii and Licornia diadema the characteristic shape of zooids, position of the joints, frontal avicularia, ovicells and basal vibracula; Licornia macropora is distinct in having a rounded scutum and ooecia with more than 15 pseudopores.
Most characteristics of L. jolloisii are also seen in Busk's Scrupocellaria cyclostoma (Figure 3C, D) and Scrupocellaria ferox (Figure 4C, D), as well as in the Scrupocellaria longispinosa Harmer, Reference Harmer1926 (Figure 4E, F); these three species are reassigned to Licornia. Licornia cyclostoma comb. nov. is distinct by the presence of ringed rhizoids, lateral avicularium with a long base, and the aquiline laterally directed frontal avicularia. Licornia ferox comb. nov. has frontal avicularia longer than those of L. cyclostoma; they are also distinct by the shape of the lateral avicularium and absence of scutum in L. cyclostoma. Licornia longispinosa comb. nov. has very long distal spines and zooids with oval scutum in both ovicelled and non-ovicelled zooids.
Tilbrook & Vieira (Reference Tilbrook and Vieira2012, figure 10) described a new species from the Queensland coast, Scrupocellaria prolata, which is here reassigned to Licornia because of its morphological similarities with L. diadema and L. cervicornis. However, L. prolata comb. nov. is distinct in producing frontally directed elongate frontal avicularia and in having larger zooids than those of L. diadema and L. cevircornis (see Tilbrook & Vieira, Reference Tilbrook and Vieira2012). In addition, Tilbrook (Reference Tilbrook2006) noted differences between Busk's S. diadema and some specimens from Indonesian and Malaysian regions, but the specimens he recorded under the name Scrupocellaria diadema (SBMNH 365098–99; see Tilbrook, Reference Tilbrook2006: 58, pl. 9, figures A–C) belong to an undescribed species of Licornia (see additional comparison in Tilbrook & Vieira, Reference Tilbrook and Vieira2012, pp. 33–34).
Among the taxa herein assigned to Licornia, two species, L. annectens and L. ferox, are characterized by the absence of frontal scuta, while in L. cyclostoma the scuta are present only in ovicelled zooids. In type specimens of Licornia diadema the scutum is often present and dimorphic in ovicelled zooids, but its presence varies in non-ovicelled zooids, as in L. prolata. Licornia jolloisii is distinguished from other species of Licornia by the presence of a stout spine-like scutum with a sharp point.
In summary, in addition to the type species, L. jolloisii, another nine species previously assigned to Scrupocellaria, including most of those described by Busk (Reference Busk and MacGillivray1852), are herein reassigned to the genus Licornia van Beneden, 1850: Licornia annectens (MacGillivray, Reference MacGillivray1887) comb. nov., Licornia cervicornis (Busk, Reference Busk and MacGillivray1852) comb. nov., Licornia cyclostoma (Busk, Reference Busk and MacGillivray1852) comb. nov., Licornia diadema (Busk, Reference Busk and MacGillivray1852) comb. nov., Licornia ferox (Busk, Reference Busk and MacGillivray1852) comb. nov., Licornia gaspari (Thornely, Reference Thornely1907), Licornia longispinosa (Harmer, Reference Harmer1926) comb. nov., Licornia macropora (Osburn, Reference Osburn1950) comb. nov., and Licornia prolata (Tilbrook & Vieira, Reference Tilbrook and Vieira2012) comb. nov. Two undescribed species of Licornia were previously assigned to Scrupocellaria diadema Busk, Reference Busk and MacGillivray1852 (see Figure 5C–F).
DISCUSSION
The redescription of L. jolloisii allows us to reassign 11 additional species to this genus (two of those are undescribed, see Figure 5C–F); thus the formerly a monospecific subgenus, now comprises a genus of 12 species, characterized by (i) fan-shaped colonies with joints crossing the proximal opesial area of outer zooids at the bifurcation, (ii) lateral avicularia with straight rostrum, (iii) small, almost triangular basal vibracular chambers, with oblique and uncurved setal grooves occupying two-thirds of vibracular chamber length, (iv) single axial vibracula and (v) ovicells with many ectooecial pores.
The jointed transversal tubes on the branches, described for L. jolloisii (Figure 1A), were also observed in some colonies of L. gaspari and L. diadema. The majority of species have rhizoids with hooks, but L. cyclostoma has distinctly annulated rhizoids. Hincks (Reference Hincks1880) noted smooth and hooked rhizoids in different colonies of Scrupocellaria reptans from British waters, while Waters (Reference Waters1909), Tilbrook & Vieira (Reference Tilbrook and Vieira2012) and Vieira & Spencer Jones (Reference Vieira and Spencer Jones2012) used these characteristics to distinguish different species of Scrupocellaria. No variation in the surface of rhizoids was observed in different species of Licornia, which suggests that the different morphology in distinct specimens (hooked, smooth or annulated) is not an ecological response and may be useful to distinguish different taxa (cf. Scrupocellaria hamata Tilbrook & Vieira, Reference Tilbrook and Vieira2012; cf. Scrupocellaria ellisi Vieira & Spencer Jones, Reference Vieira and Spencer Jones2012). Further observation using SEM will be important to distinguish additional characteristics (e.g. shape of frontal scuta, shape and position of frontal avicularia) necessary for detection of species complexes (e.g. Licornia diadema, see Harmer, Reference Harmer1926), such as have been observed for other bryozoan taxa (Berning et al., Reference Berning, Tilbrook and Rosso2008; Winston & Woollacott, Reference Winston and Woollacott2008; Vieira et al., Reference Vieira, Migotto and Winston2010, Reference Vieira, Winston and Fehlauer-Ale2012; Tilbrook, Reference Tilbrook2012).
The genus Licornia is widely distributed in Indian and Pacific waters and more species may exist, but the group does not seem to be as diverse in the Atlantic. Crossland's specimen from Cape Verde Island of Scrupocellaria cervicornis Busk was redescribed as Scrupocellaria tridentata Waters, Reference Waters1918, but because of the presence of very large basal vibracula and distinct trifoliate frontal avicularia this species is not reassigned to Licornia. Specimens of L. diadema were previously collected by Miss Gatty from Cape Verde Island (under the name Scrupocellaria ciliata Audouin, Reference Audouin and Panckoucke1826; see Busk Reference Busk1884, p. 23), but reexamination is required to confirm the occurrence of L. diadema in this region. Recently Licornia diadema has been recorded from the Western Atlantic from Rio de Janeiro, Brazil, by Ramalho et al. (Reference Ramalho, Muricy, Taylor, Moyano, Cancino and Wyse Jackon2005), making the Florida Keys and Brazilian specimens of Licornia jolloisii the second record for the genus in Atlantic waters (Figure 6). Due to the presence of similar species in Australian waters (Tilbrook & Vieira, Reference Tilbrook and Vieira2012) and the possibility of cryptic species among colonies from Korea (Lee et al., Reference Lee, Kwan, Kong, Min, Seo and Won2011), however, we suggest detailed morphological studies on specimens reported by Ramalho et al. (Reference Ramalho, Muricy, Taylor, Moyano, Cancino and Wyse Jackon2005) as Scrupocellaria diadema to confirm the identity of Brazilian specimens.
Fig. 6. Type locality of Licornia species worldwide [stars; note that the type locality, if Egypt, can be Red Sea coast of Egypt] and new locality records: 1, Licornia jolloisii (Audouin, Reference Audouin and Panckoucke1826); 2, Licornia annectens (MacGillivray, Reference MacGillivray1887); 3, Licornia cervicornis (Busk, Reference Busk and MacGillivray1852); 4, Licornia cyclostoma (Busk, Reference Busk and MacGillivray1852); 5, Licornia diadema (Busk, Reference Busk and MacGillivray1852); 6, Licornia gaspari (Thornely, Reference Thornely1907); 7, Licornia ferox (Busk, 1952); 8, Licornia longispinosa (Harmer, Reference Harmer1926); 9, Licornia macropora (Osburn, Reference Osburn1950); 10, Licornia prolata (Tilbrook & Vieira, Reference Tilbrook and Vieira2012). Additional records of Licornia jolloisii [triangle] and Licornia diadema [square] in Atlantic and Mediterranean; Busk's Scrupocellaria ciliata Audouin from Cape Verde Island was noted with a question mark in the map, as its placement is still uncertain.
McCann et al. (Reference McCann, Hitchcock, Winston and Ruiz2007) reported 35 species on plates in six different localities of the Southern United States, four of those classified as non-native. Among species classified as cryptogenic (unknown origin), only one member of the family Candidae, Scrupocellaria bertholletii Audouin, Reference Audouin and Panckoucke1826, was recorded, but examination of the specimens at the VMNH showed that two supposedly endemic species are involved, one of them belonging to Scrupocellaria curacaoensis Fransen, Reference Fransen1986. Recently, Johnson et al. (Reference Johnson, Winston and Woollacott2012) reported the first invasive Candidae species on the north-eastern Atlantic coast, Tricellaria inopinata d'Hondt & Occhipinti-Ambrogi, 1985. Therefore, Licornia jolloisii is the second non-native Candidae species reported from the Atlantic coast of United States, the first on the south-east coast.
Licornia jolloisii was first reported on an artificial substratum (buoy) by Waters (Reference Waters1909) from Suez Bay, while Robertson (Reference Robertson1921) noted that this species was very common in the vicinity of the Bay of Bengal, between 70–90 m depth. The species was first reported as invasive at six different points along the Suez Canal, including Port Said, at the Mediterranean entrance of the Suez Canal (Hastings, Reference Hastings1927). The latest record for L. jolloisii from the Mediterranean (Israel) was reported by d'Hondt (Reference d'Hondt1988), who found colonies on sandstones and banks of bivalves, an invasion supposedly carried from the North Suez Canal to the coast of Israel, but with an unknown dispersal vector (Galil, Reference Galil2007). The location of the Florida Keys specimens (Figure 7) in a man-made canal near a major recreational boat route to and from Key West, as well as the volume of commercial shipping traffic through the Straits of Florida, makes it likely that it represents a recent invasion of the area. More collections in this region are needed to determine whether or not the species has persisted or spread since 2005. More recently, some specimens of L. jolloisii were also found on artificial panels in Itaparica, Baía de Todos os Santos, NW Brazilian coast. This place is characterized by intense recreational and commercial shipping traffic due to the presence of small boat marinas, the Harbour of Aratu and one oil refinery, with piers for the oil cargo ships and a large shipyard. Further efforts towards extending the understanding of local invasive marine species dynamics are in progress in this area (L.P. Kramer & R.M. Rocha, personal communication).
Fig. 7. (A, B) Colonies of Licornia jolloisii (Audouin, Reference Audouin and Panckoucke1826) on natural substrata found in Florida Keys, USA. Scale bars: 2 cm. Photographs by Don De Maria, Sea Samples, Summerland Key, Florida.
ACKNOWLEDGEMENTS
We are grateful to Laura Pioli Kremer and Rosana Moreira Rocha for sending the Brazilian specimens included in this study, and to Karen and Don De Maria for the donation of a voucher of the Florida specimen of L. jolloisii to the VMNH. Karin H. Fehlauer Ale, Centro de Biologia Marinha, provided a map for Figure 5. We are grateful to JoAnn Sanner (National Museum of Natural History, Smithsonian Institution) and Chris Rowley (Museum Victoria) for providing photographs of specimens deposited at the NMNH and NMV; Henry W. Chaney (Santa Barbara Museum of Natural History) who loaned Osburn's specimens included in this study; Kevin Tilbrook provided SEM images of some species for comparison; Aline Staskowian Benetti who sent museum numbers of Brazilian specimens deposited at the MZUSP; Alvaro E. Migotto gave suggestions on the manuscript. Logistical support was provided for L.M. Vieira by the American Museum of Natural History (USA), the Museum of Comparative Zoology (USA), the Muséum National d'Histoire Naturelle (France), the Natural History Museum, (UK), the Nationaal Natuurhistorisch Museum—Naturalis (Netherlands), the Smithsonian National Museum of Natural History (USA) and the Virginia Museum of Natural History (USA). We thank Kevin Tilbrook and three anonymous referees for their suggestions to improve this manuscript.
FINANCIAL SUPPORT
This study is part of the L.M. Vieira's PhD thesis supported by FAPESP (Proc. 2008/10619-0) through the Graduate Program in Zoology of the Departamento de Zoologia, IBUSP. This study was also partially supported by the International Bryozoology Association.
