INTRODUCTION
The gorgonians of the genus Ellisella Gray, 1958 are widely distributed from tropical to temperate waters (Fabricius & Alderslade, Reference Fabricius and Alderslade2001; Weinberg & Grasshoff, Reference Weinberg, Grasshoff and Hofrichter2005). In the Mediterranean Sea, this genus is represented only by one species, Ellisella paraplexauroides Stiasny, Reference Stiasny1936 (family Ellisellidae), forming brick-red candlestick colonies, up to 2 m high (Carpine & Grasshoff, Reference Carpine and Grasshoff1975). The branched colonies have thin, whip-like ramifications arising from a common short stem, heading parallel upwards and dividing dichotomously (Fabricius & Alderslade, Reference Fabricius and Alderslade2001). The unbranched or sparsely branched specimens of this species can be confused with Viminella flagellum (Johnson, 1863) (Carpine & Grasshoff, Reference Carpine and Grasshoff1975; Fabricius & Alderslade, Reference Fabricius and Alderslade2001; Giusti et al., in press), the second ellisellid coral found in the Mediterranean basin, but are easily distinguishable by the sclerites shape and for the red colour, contrasting the white-yellow appearance of V. flagellum.
Ellisella paraplexauroides, similar to V. flagellum, has an Atlanto-Mediterranean distribution (Vafidis et al., Reference Vafidis, Koukouras and Voultsiadou-Koukoura1994), however, in contrast with this species, it has been reported in southernmost warm temperate oceanic waters along the western coasts of Africa (Table 1). The first record of E. paraplexauroides was made by Stiasny (Reference Stiasny1936) from Cap Blanco (Mauritania). Following this, the species was reported in several other Atlantic localities including the coasts of Portugal (Stiasny, Reference Stiasny1939a), the Gulf of Cádiz (Arroyo Tenorio et al., Reference Arroyo Tenorio, Domenech, Lampreave, López-González, Barea-Azcón, Ballesteros-Duperón and Moreno2008; Aguiliar et al., Reference Aguiliar, Pardo, Cornax, García and Ubero2010), several sites along the Moroccan coast (Stiasny, Reference Stiasny1939b; Grasshoff, Reference Grasshoff1972, Reference Grasshoff1992) and in the whole Canary Archipelago (Brito et al., Reference Brito, Cruz, Moreno, Pérez and Bacallado1984; Brito, Reference Brito1985; Arístegui et al., Reference Arístegui, Brito, Cruz, Bacallado, Barquin, Nunez and Perez-Dionis1987; Grasshoff, Reference Grasshoff1992; Ocaña et al., Reference Ocaña, Brito and Nuñez1992; Bianchi et al., Reference Bianchi, Harounc, Morri and Wirtz2000; Brito & Ocaña, Reference Brito and Ocaña2004). It also occurs further south along the African coast (apart from the type locality): in Senegal (Grasshoff, Reference Grasshoff1992; Miralles et al., Reference Miralles, Galonnier, Njinkoue, Samb, Gaydou and Kornprobst1992), Ivory Coast, Ghana, Nigeria and Angola (Grasshoff, Reference Grasshoff1992). No records have been given so far for the Azores, Madeira Islands, Great Meteor and Josephine Seamounts and Cape Verde Archipelago, where, on the contrary, V. flagellum was found. This led Grasshoff (Reference Grasshoff1972) to suppose that E. paraplexauroides was mainly distributed along the continental coasts, excluding the Canary Islands.
Biogeographical records for Ellisella paraplexauroides.
Ellisella paraplexauroides has been firstly reported in the Mediterranean Sea by Stiasny (Reference Stiasny1940), examining fragments collected along the Algerian and Tunisian coasts (Grasshoff, Reference Grasshoff1992). Most of the following records within the Mediterranean Sea came from the Gibraltar Strait (Ocaña et al., Reference Ocaña, Sánchez Tocino, López González and Viciana Martín2000; Brito & Ocaña, Reference Brito and Ocaña2004; Arroyo Tenorio et al., Reference Arroyo Tenorio, Domenech, Lampreave, López-González, Barea-Azcón, Ballesteros-Duperón and Moreno2008; Torres Gavilá, Reference Torres Gavilá2008), Alborán Island (Templado et al., Reference Templado, Garcia Carrascosa, Baratech, Capaccioni, López Ibor, Silvestre and Masso1986, Reference Templado, Calvo, Moreno, Flores, Conde, Abad, Rubio, López-Fé and Ortiz2006; Aguiliar et al., Reference Aguiliar, Torriente and García2008), Alborán Sea (Aguiliar et al., Reference Aguiliar, Torriente and García2008) and along the Moroccan coast, in the Chafarinas Islands, where several biological observations were made by SCUBA diving on a rich shallow water population of E. paraplexauroides (López et al., Reference López, San Martín and Jiménez1996; Peña Cantero & García Carrascosa, Reference Peña Cantero and García Carrascosa2002; Castellanos et al., Reference Castellanos, Hernández-Vega and Junoy2003; González García et al., Reference González García, García Peña and Bueno del Campo2005; Aguiliar et al., Reference Aguiliar, Torriente and García2008; Torres Gavilá, Reference Torres Gavilá2008; Tocino et al., Reference Tocino, Barahona, Barranco and Velasco2009). A further record was documented from the central Mediterranean Sea, at Sidi Daoud (Tunisia) (Mustapha et al., Reference Mustapha, Afli, Hattour and El Abed2004). Finally, Stiasny (Reference Stiasny1942) reported E. paraplexauroides also from the Bay of Naples (representing the northernmost record so far) even if, on the basis of the known distribution of the species, this record was generally considered doubtful (Grasshoff, Reference Grasshoff1972) (Figure 1).
Map of the geographical distribution of Ellisella paraplexauroides (black dots) in the Mediterranean Sea. Black triangle represents the present record.
Few data are available concerning biology and ecology of E. paraplexauroides. This has probably resulted from the analysis of small fragments only (Carpine & Grasshoff, Reference Carpine and Grasshoff1975; Ocaña et al., Reference Ocaña, Brito and Nuñez1992) or from investigations focused on the associated fauna (López et al., Reference López, San Martín and Jiménez1996; Peña Cantero & García Carrascosa, Reference Peña Cantero and García Carrascosa2002; Aguiliar et al., Reference Aguiliar, Torriente and García2008; Torres Gavilá, Reference Torres Gavilá2008), while in situ observations have been rarely dedicated to this species (Bianchi et al., Reference Bianchi, Harounc, Morri and Wirtz2000; Mustapha et al., Reference Mustapha, Afli, Hattour and El Abed2004; Aguiliar et al., Reference Aguiliar, Pastor and Pablo2006, Reference Aguiliar, Torriente and García2008, Reference Aguiliar, Pardo, Cornax, García and Ubero2010).
Typical of the circalittoral plain, E. paraplexauroides may show a wide bathymetric distribution ranging from 15 to 690 m depth, with the shallowest records found mainly in the Mediterranean Sea and the deepest specimens found in the Atlantic Ocean. In particular, it has been reported on the shelf's edge at mesophotic depths between 50 and 150 m (Templado et al., Reference Templado, Garcia Carrascosa, Baratech, Capaccioni, López Ibor, Silvestre and Masso1986, Reference Templado, Calvo, Moreno, Flores, Conde, Abad, Rubio, López-Fé and Ortiz2006; Tocino et al., Reference Tocino, Barahona, Barranco and Velasco2009), but it can also live at bathyal depths, like in the Canary Islands, where it was observed from 63 to 690 m, mainly associated with the assemblages of the scleractinian Dendrophyllia ramea (Linnaeus, 1758) (Brito & Ocaña, Reference Brito and Ocaña2004; Arroyo Tenorio et al., Reference Arroyo Tenorio, Domenech, Lampreave, López-González, Barea-Azcón, Ballesteros-Duperón and Moreno2008). In the Canary Islands it has also been observed that the complexity of the branching pattern and the diameter of the ramifications depends on the type of substrate, as a result the colonies are thinner and sparsely branched when they live on unstable bottoms (Brito & Ocaña, Reference Brito and Ocaña2004).
In the Gulf of Cádiz, Gibraltar Strait and Alborán Sea there are some sites where E. paraplexauroides was observed in very shallow waters, respectively 15–30 m along the coastline of Cádiz (Aguiliar et al., Reference Aguiliar, Pardo, Cornax, García and Ubero2010), 15–35 m depth between the Posidonia oceanica ((L.) Delile, 1813) mattes, at Chafarinas Islands (González García et al., Reference González García, García Peña and Bueno del Campo2005) and 20–25 m depth in Ceuta, along the Moroccan coast (Ocaña et al., Reference Ocaña, Sánchez Tocino, López González and Viciana Martín2000; Brito & Ocaña, Reference Brito and Ocaña2004).
Quantitative data on the populations of E. paraplexauroides have never been reported in the literature. This species has always been considered very rare and occasional (Grasshoff, Reference Grasshoff1992; Arroyo Tenorio et al., Reference Arroyo Tenorio, Domenech, Lampreave, López-González, Barea-Azcón, Ballesteros-Duperón and Moreno2008) and never forming dense meadows, as in the case of V. flagellum (Grasshoff, Reference Grasshoff1971, Reference Grasshoff1972, Reference Grasshoff1977). The richest population known so far is the one at Chafarinas Islands (González García et al., Reference González García, García Peña and Bueno del Campo2005). The tallest colonies reported so far, are from the Mediterranean Sea (Grasshoff, Reference Grasshoff1992).
The colonies may host numerous epibionts, especially in their basal part and on larger ramifications. The associated fauna, occupying dead portions of the colonies, is mainly composed of encrusting algae, bryozoans (González García et al., Reference González García, García Peña and Bueno del Campo2005), hydroids (Peña Cantero & García Carrascosa, Reference Peña Cantero and García Carrascosa2002), stoloniferans such as Sarcodictyon canariensis Ocaña, Brito & Nunez, Reference Ocaña, Brito and Nuñez1992 (Ocaña et al., Reference Ocaña, Brito and Nuñez1992), and ascidians such as Pycnoclavella taureanensis Brunetti, 1991 and Clavelina nana Lahille, 1890 (Aguiliar, Reference Aguiliar2004; Tocino et al., Reference Tocino, Barahona, Barranco and Velasco2009). Crustacean isopods of the genus Paranthura (Castellanos et al., Reference Castellanos, Hernández-Vega and Junoy2003) and numerous species of polychaetes (López et al., Reference López, San Martín and Jiménez1996; Torres Gavilá, Reference Torres Gavilá2008) are the main components of the vagile fauna. The number of colonies with epibionts or dead colonies of E. paraplexauroides tends to decrease depending on the depth (Tocino et al., Reference Tocino, Barahona, Barranco and Velasco2009).
The aim of this paper is to provide the first detailed record of E. paraplexauroides for the Italian waters. Moreover, some remarks on its distribution, biology and ecology are given on the basis of remotely operated vehicle (ROV) video and photographic samplings and specimens collection.
MATERIALS AND METHODS
The Island of Pantelleria lies along the continental rift system of the Sicily Strait (central Mediterranean Sea). It consists exclusively of volcanic rocks (Villari, Reference Villari1974) and the entire area is subjected to intensive volcano–tectonic activity. The structural setting of the island is specified by faults and fractures that follow the regional north-west–south-east and north-east–south-west trends (Civetta et al., Reference Civetta, Cornette, Gillot and Orsi1988).
The study site, named Cala Caruscia (locality Punta Spadillo) (36°49.139′N 12°01.537′E), is located on the north-east side of the island (Figure 2) and was explored through a ROV survey conducted in May 2010 on-board the RV ‘Astrea’. The site is characterized by inclined rocky walls down to about 200 m depth with the bottom first turning into heavily silted rocky boulders and then ending in a gently inclined soft-bottom slope.
Map of the sampling area (black dot) on the north-east coast of Pantelleria Island (Sicily Strait).
The ROV ‘Polluce’ was equipped with a digital camera (Nikon D80, 10 megapixel), an underwater strobe (Nikon SB 400), a high definition video camera (Sony HDR-HC7) and a 3-jaw grabber (SeaBotix Inc.) to take samples. Additionally, it had a depth sensor, a compass, and three parallel laser beams 10 cm apart used as a reference scale to assist the observers in estimating: frame area, sizes (height and width) and branching pattern of what was photographed using the software ImageJ, (Brazeau & Lasker, Reference Brazeau and Lasker1988). Colonies of Ellisella paraplexauroides were photographed in the mesophotic zone, between 80 and 94 m depth. Photographs were then analysed to describe the general morphology of the coral colonies and their in vivo appearance. Direct sampling of one specimen was carried out for the species description. Sclerites were analysed with scanning electron microscopy (SEM) after dissolving the coenenchyme in sodium hypochlorite and lastly, a fragment fixed in 95% ethanol was used for the morphological analysis of polyps carried out with SEM and stereomicroscope.
RESULTS
The coral community of Pantelleria Island is mainly composed of a mixed assemblage of three-dimensional anthozoans. The dominant species up to 80 m depth are the gorgonians Paramuricea clavata (Risso, 1826), Eunicella cavolinii (Koch, 1887), Corallium rubrum (Linnaeus, 1758) and, occasionally, the zoanthid Savalia savaglia (Bertoloni, 1819). Sparse colonies of the black coral Antipathella subpinnata (Ellis & Solander, 1786) were observed around 100 m depth, while the gorgonians Viminella flagellum and Swiftia pallida Madsen, 1970 were typically distributed in the deepest depth range, below 130 m depth (Giusti et al., in press). In total, five red brick colonies of Ellisella paraplexauroides were found scattered on the explored hard substrate (Figure 3A–D), between 80 and 94 m depth.
Colonies were anchored to the substrata with a large basal plate, about 10 cm wide, sometimes covered by fine sediments and other organisms such as sponges or encrusting algae (Figure 3A). The common stem arising from the plate was about 15 cm long and showed a 2–3 cm wide basal diameter, not bearing polyps. Observed colonies reached considerable dimensions, from 83 to 173 cm in height (130 ± 35 cm average) and from 12 and 42 cm in width (25 ± 12 cm average), being taller than larger because of the typical upward arrangement of their branches (Figure 3A–D). The colonies could show up to 30 terminal branches (basal diameter around 3 mm).
Ellisella paraplexauroides from Pantelleria Island. (A–D) Underwater photographs of E. paraplexauroides. Occasionally, colonies can be colonized by sessile organisms (Figure D); (E) expanded polyps of a living colony; (F) scanning electron microscopy image of the arrangement of calyxes on the apical portion of a branch; (G) stereomicroscope photograph of the sclerites, both yellow coloured and colourless; (H) sclerites of E. paraplexauroides composed of: a, double head from the superficial layer of coenenchyme; b, thick capstan; c, thick capstans with high tubercles; d, girdle spindles; e, slender girdle spindle; f, long rods from the deeper layer of the coenenchyme and from calyxes; g, rods from the pharynx. Scale bars: A–E, 10 cm; F, 1 mm; G, 50 µm.
Only one colony showed the basal portion of some branches partially dead (Figure 3D). The naked skeleton was covered by numerous hydroids (unidentified sertularids and eudendrids entrapping a notable quantity of sediment), a colony of Paramuricea clavata, the polychaete Filograna sp. and various encrusting sponges and bryozoans.
During the ROV survey, a sample 35 cm long was collected from a sparsely branched colony 110 cm high. Coenenchyme was red, while polyps, monomorphic and highly contractile, were crowded, cylindrical and whitish. Underwater images showed extended polyps characterized by tentacles almost half the length of the calyxes (Figure 3E). Along the studied apical portion, polyps were arranged in a few longitudinal rows. However, photographs showed multiple rows of calyxes in the most basal parts of the colonies, as already reported in previous descriptions (Grasshoff, Reference Grasshoff1972; Carpine & Grasshoff, Reference Carpine and Grasshoff1975). Polyps emerged from the branches with a sharp inclination and could show a different orientation when compared to the main stem (Figure 3F). Calyxes (up to 1.5 mm high) (Figure 3E, F) were characterized by a thin calyx wall. When contracted, the polyps formed knobs on the surface of the branches.
Surface sclerites were orange-yellow, while subsurface ones were almost colourless (Figure 3G). Sclerites included several types (Figure 3H): symmetrical double heads and thick capstans (up to 50 µm high) (Figure 3Ha-b) were densely packed on the surface of the coenenchyme; thick highly tuberculated capstans (between 60 and 70 µm high) (Figure 3Hc) were organized in the subsurface of the coenenchyme; spindles (between 60 and 80 µm high) were found in the wall of calyxes (Figure 3Hd-e); and 50 µm high rods with few tubercles were found in the pharynx of the anthocodiae (Figure 3Hf-g). Sizes of the sclerites were slightly smaller than what has already been reported for some Atlantic specimens (Carpine & Grasshoff, Reference Carpine and Grasshoff1975), but quite similar to that reported for the Canary Islands (Brito & Ocaña, Reference Brito and Ocaña2004).
DISCUSSION
The present record of Ellisella paraplexauroides adds a new species of alcyonacean to the Italian fauna (Morri et al., Reference Morri, Esposito and Pessani2008) (which now accounts for 27 species) and confirms the presence of this species in the central Mediterranean Sea. This record represents also the most eastern report of E. paraplexauroides in the Mediterranean basin. The ROV observations on the small population found in the mesophotic zone of Pantelleria Island confirm previous data regarding size, colour, branching pattern and associated fauna (Grasshoff, Reference Grasshoff1972; Carpine & Grasshoff, Reference Carpine and Grasshoff1975; Arroyo Tenorio et al., Reference Arroyo Tenorio, Domenech, Lampreave, López-González, Barea-Azcón, Ballesteros-Duperón and Moreno2008). The colonies observed in Pantelleria are also some of the tallest reported in the literature.
Pantelleria Island is situated in a unique area of the Mediterranean Sea, both from the oceanographic and topographic point of view, leading ultimately to an important role in the composition of the benthic fauna (Manzella et al., Reference Manzella, Gasparini and Astraldi1988; Greenpeace International, 2009). In the Sicily Strait, representing the connection between the eastern and western basins of the Mediterranean Sea, two water layers have been observed. The most superficial is composed of the surface Atlantic Waters (AW), running eastward, while the deepest one by the Levantine Intermediate Waters (LIW) flowing in the opposite direction, down to about 500 m (Napolitano et al., Reference Napolitano, Sannino, Artale and Marullo2003). The particular hydrographic conditions of this area probably favour the presence of rich benthic communities of filter-feeding organisms (Bianchi & Morri, Reference Bianchi and Morri2000).
Ellisella paraplexauroides is a typical Atlanto-Mediterranean species with a wide bathymetric distribution range. The superficial variations in temperature of the Mediterranean waters probably confine this species below 50 m depth in the Sicily Strait, although some populations were locally recorded at very shallow depths (15–35 m in the Gulf of Cádiz, Strait of Gibraltar and the Alborán Sea) (Arroyo Tenorio et al., Reference Arroyo Tenorio, Domenech, Lampreave, López-González, Barea-Azcón, Ballesteros-Duperón and Moreno2008).
The scattered distribution of E. paraplexauroides in the explored area was observed in a limited depth range, being the species confined below the distribution limit of the most common gorgonians (Paramuricea clavata and Eunicella cavolinii) and above the distribution range of Viminella flagellum (Giusti et al., in press). Although this species is occasionally considered as characterizing a facies (Gulf of Cádiz, Atlantic Ocean) (Aguiliar et al., Reference Aguiliar, Pardo, Cornax, García and Ubero2010), it never occurs in dense monospecific meadows and can be considered an occasional element in the lower fringe of the circalittoral assemblage.
The recorded susceptibility of E. paraplexauroides to epibiosis may be enhanced by mechanical injuries of the coenenchyme, as already suggested for other deep Mediterranean corals (Tocino et al., Reference Tocino, Barahona, Barranco and Velasco2009). Commercial fishing activities, for example through long-line fishing, directly damage these corals that are particularly vulnerable because of their arborescent morphology, fragile construction and the general slow growth rate (Bavestrello et al., Reference Bavestrello, Cerrano, Zanzi and Cattaneo-Vietti1997; Mortensen & Buhl-Mortensen, Reference Mortensen and Buhl-Mortensen2004; Bo et al., Reference Bo, Bavestrello, Canese, Giusti, Salvati, Angiolillo and Greco2009).
It is well known that assemblages of colonial anthozoans represent biodiversity hotspots (Mortensen & Buhl-Mortensen, Reference Mortensen and Buhl-Mortensen2004; Ballesteros, Reference Ballesteros2006; Bo et al., Reference Bo, Bavestrello, Canese, Giusti, Salvati, Angiolillo and Greco2009; Cerrano et al., Reference Cerrano, Danovaro, Gambi, Pusceddu, Riva and Schiaparelli2010), adding three-dimensional complexity to the habitat and commonly housing a rich associated fauna as well as a great abundance of fish (Tsounis at al., Reference Tsounis, Rossi, Aranguren, Gili and Arntz2006; Mortensen et al., Reference Mortensen, Buhl-Mortensen, Gebruk and Krylova2008). In the Mediterranean Sea, these communities have been studied mainly in shallow waters, and few data are available for deep environments (Bo et al., Reference Bo, Bavestrello, Canese, Giusti, Salvati, Angiolillo and Greco2009, Reference Bo, Bavestrello, Canese, Giusti, Angiolillo, Cerrano, Salvati and Greco2010, Reference Bo, Bertolino, Borghini, Castellano, Covazzi Harriague, Di Camillo, Gasparini, Misic, Povero, Schroeder and Bavestrello2011; Gori et al., Reference Gori, Rossi, Berganzo, Pretus, Dale and Gili2010).
The complex structure and richness of species of the assemblages hosting E. paraplexauroides, together with their vulnerability to human activities, should motivate the decision of including them within the Mediterranean species and habitat list of conservational relevance.
ACKOWLEDGEMENTS
We thank the crew members of the RV ‘Astrea’ for their precious help and work. This work was financed by Italian Ministry of the Environment, Land and Sea Protection.
