Echinophyllia tarae sp. n. (Cnidaria, Anthozoa, Scleractinia), a new reef coral species from the Gambier Islands, French Polynesia

Abstract A new shallow water scleractinian coral species, Echinophyllia tarae sp. n., is described from the Gambier Islands, French Polynesia. It is characterized by an encrusting corallum, a few large and highly variable corallites with protruding walls, and distinctive costosepta. This coral was observed in muddy environments where several colonies showed partial mortality and re-growth. The new species has morphological affinities with both Echinophyllia echinata and with Echinomorpha nishihirai, from which it can be distinguished on the basis of the diameter and the protrusion of the largest corallite, the thickness of the septa, and the development of the size of the crown of paliform lobes.

Presently, Echinophyllia is known to occur in the Indo-Pacific, from the seas around Arabia (Sheppard and Sheppard 1991, Pichon et al. 2010, the Indian Ocean (Obura 2012) and the western and central Pacific Ocean (Chevalier 1971, Veron and Pichon 1980, Best et al. 1989, Veron 2000, Hoeksema and van Ofwegen 2004 to French Polynesia in the east, including the Society, Tuamotu, Austral and Gambier Islands (Pichon 1985, Glynn et al. 2007. The remote and relatively poorly studied Gambier Islands are found at the southeast end of the vast French Polynesian territory (Figure 1a, b). The actual islands were once all part of the same volcano, which in time has almost completely drowned (Brousse et al. 1974). Today, they are found in a lagoon approximately 35 km long (north to south) and 30 km wide (west to east) delimited by a continuous reef, which emerges at low tide in the north and is submerged in the south (Brousse et al. 1974 (Figure 1c). The current knowledge of reef-dwelling corals from the Gambier Archipelago is based on the studies carried out in the mid-seventies by Chevalier (1974), who published a preliminary list including 60 species of zooxanthellate and azooxanthellate scleractinians. Since then, no further studies were carried out on the coral fauna of the islands until the Tara Oceans scientific Expedition with MV Tara (Karsenti et al. 2011) allowed sampling of 24 sites between June and July 2011, which also resulted in an update on the local mushroom coral fauna (Hoeksema and Benzoni 2013).
With regard to Echinophyllia species, Chevalier (1974) only reported on the presence of E. aspera. According to him this species is typical of fringing reefs around the main islands in the large lagoon. During the recent Tara Oceans Expedition the presence of Echinophyllia aspera was actually not recorded. However, another Echinophyllia species, morphologically different from others already known, was commonly observed at the fringing reefs and lagoon pinnacles of the Gambier Islands. The species is here described as Echinophyllia tarae sp. n. and its similarities with its congeners as well as Echinomorpha nishihirai (Veron, 1990) are discussed.

Methods
A reference collection of Scleractinia was sampled in the Gambier, including coral skeletons and tissues fixed for DNA, after in situ photographs were taken. The collection contained five specimens of Echinophyllia tarae sp. n. Sampling took place during SCUBA diving at different sites around the islands of Taravai, Akamaru, and Makaroa ( Figure 1). Digital images of living corals in the field were taken with a Canon G9 in an Ikelite underwater housing system. Coral specimens were collected, tagged, and for each specimen a fragment of 1 cm 2 was broken off the colony and preserved in CHAOS solution for further molecular analysis. The remaining corallum was placed for 48 hours in sodium hypochlorite to remove all soft parts, rinsed in freshwater and dried for microscopic studies. Images of coral skeletons were taken with a Canon G9 digital camera and through a Leica M80 microscope equipped with a Leica IC80HD camera. For high resolution and deep field close ups of three-dimensional details of corallites and septa, a series on images of the same subject at different focus intervals were taken (approximately 10) and the images were fused using the Helicon Focus 5.3 software (Kozub et al. 2000(Kozub et al. -2012. A total of 24 sites was surveyed (Table 2). Each site position was recorded with a Garmin eTrex GPS. At each site all coral species encountered in a 1 hour SCUBA dive were recorded and data were included into a geo-referenced database. At least two images per specimen were taken underwater, one of the complete colony and one close-up. Digital images were then analyzed to verify underwater preliminary records and species presence records were used to produce a species per site matrix. Data on the occurrence of E. tarae sp. n. in the field in the different sites was extracted from this species per site database.
The holotype was deposited at Museum National d'Histoire Naturelle (MNHN) in Paris, the other four specimens are at the University of Milano-Bicocca (UNIMIB) coral facility together with the rest of the Tara Oceans Expedition collection (186 specimens), which will ultimately be housed at the MNHN once their study is completed. Specimens of other Echinophyllia species were examined at the Museum of Tropical Queensland (MTQ), Townsville, Australia, and at the Institut de Recherche pour le Développement (IRD), Nouméa, New Caledonia. Corallum: The holotype is a knob-shaped, plocoid, encrusting colony attached to a fragment of a dead tabular Acropora coral ( Figure 2). The specimen is 9.2 cm high, and 8.5 x 5 cm wide at the base in its original growth position.

Order
Corallites: The 12 corallites are oval in shape and variable in size (Figure 2, 3), ranging from 3.3 cm in diameter (C1 in Figure 2, 3a) to 1.0 cm. Corallites are organically united (see terminology in Budd et al. 2012). The central position of C1 (the largest corallite) is less obvious in the holotypes due to its knob-shaped growth form. Corallites protrude up to 1 cm and are directed in different directions ( Figure 2). Corallite wall is septothecal.
Costosepta: Variable in number depending on the size of the corallite (Figure 3a Table 1). The largest corallite observed (specimen UNIMIB TO-GA099, Figure 4d) is 3.5 cm in diameter, the smallest, in the same specimen, 0.9 mm (Figure 5e). The numbers of septa, orders of septa, and paliform lobes vary between and within colonies. First order septa always thicker than the others and in some cases up to 4 mm thick (Figure 5f). Columella always present, large and oval in the largest corallite, less developed is smaller corallites. Costae typically thick, alternating in size (Figure 5c, d) and strongly dentate, although variably so between specimens.   the size and shape of the corallites may be hard to detect. The crown of paliform lobes is always prominent ( Figure 5) and often obvious, especially in the largest corallite (Figures 6, 7b).  Ecology: Echinophyllia tarae sp. n. inhabits protected reef habitats and was observed between 5 and 20 m depth. It commonly grows on dead coral fragments, usually parts of branching or tabular Acropora colonies, which are covered by crustose coralline algae and fleshy macroalgae (Figures 6-7). This species can grow on well-illuminated surfaces but also encrusts shaded underhangs. In well-lit conditions the appearance is  Figures 4b, 5d) showing the irregularly shaped colony with a very rugged and almost inflated appearance, Akamaru Island (Site 2). Sites are indicated in Figure 1.  Figure 7. Variation of shape, spikiness of septa and costae, and colouration of large colonies Echinophyllia tarae sp. n. observed in situ a brown encrusting colony with free margins, bright green oral discs and raised corallites, Akamaru Island (Site 2) b brown encrusting colony with white oral discs, raised corallites (larger one in the stippled circle), and very spiky costae, Taravai Island (Site 9 -type locality), the prominent crown of paliform lobes of the largest corallite is indicated by the white arrow c brown knob shaped colony with bright green oral discs and raised corallites, note the white colouration of the tips of costae teeth, Taravai Island (Site 9 -type locality) d a bright green knob shaped colony, Taravai Island (Site 9 -type locality) e brown encrusting colony with bright green oral discs and relatively low-lying corallites, note the uniform colouration of the costae, Taravai Island (Site 9 -type locality) f mottled brown encrusting colony with free margins and relatively low-lying corallites, note the uniform colouration of the costae, Taravai Island (Site 9 -type locality). Sites are indicated in Figure 1.   typically corrugated (Figures 6a-b, e-f, 7a-d). However, in some cases a certain degree of inflation of the soft tissues was observed (Figures 6a-b, f), although this generally depends on the very developed ornamentation of the underlying costosepta, which is most obvious when a live colony (Figure 6f) is compared with the clean skeleton (Figures 4b, 5d). In poorly lit conditions the overall appearance is smoother and the colouration more uniform (e.g. Figures 6d, 7e-f) although the oral discs remain generally brightly coloured and different from the rest of the tissues. Re-growth of partially dead colonies, especially at the margins, is common (Figure 8). Such patters of partial death and recovery could result from competition with other benthic invertebrates, like softbodied corallimorpharians and zoanthids which can co-occurr with this species (Figure  8a). The observed patterns of partial death may also be caused by deposition of sediment on the living corals. In fact, Echinophyllia tarae sp. n. is most commonly found at sheltered sites characterized by calm water conditions and muddy sediment which could be stirred up and deposit on benthic organisms suffocating them (Erftemeijer et al. 2012). The dead parts of the corallum are generally encrusted by coralline algae over which the coral can re-grow or re-settle (Figure 8b).
Occurrence: This species was commonly encountered on the fringing reefs off Mangareva, Aukena, Tekava, Akamaru, Kamaka, Makaroa, Agakauitai, and Taravai islands as well as at the base of the lagoon pinnacles found in the lagoon north of Mangareva Island (Figure 1, Table 2). Its distribution outside the Gambier archipelago is unknown although it could also occur in the Austral Islands (see Discussion section). No record is known from other localities.
Affinities: In its encrusting growth form, and in the presence of a central larger and protruding corallite this species is similar to Echinophyllia echinata and Echinomorpha nishihirai (see Discussion). Ongoing molecular analyses will reveal the phylogenetic relationships of this species with its congeners.
Etymology. This species is named after MV Tara, which allowed the exploration of coral reefs in Gambier. Moreover, the name "tara" in the Polynesian language may refer to a spiny, pointed object, which applies well to the new species typically featuring pointed skeletal structures. In the same language, Tara is also the name of a sea goddess.

Discussion
The study of the Echinophyllia tarae sp. n. material and the in situ observations indicated a remarkable phenotypic variation within and between specimens regarding calice size, shape, and inclination, and the number of septa and paliform lobes in the corallite. Thus, E. tarae sp. n. is distinct from the other Echinophyllia species by the presence of a larger central corallite with a raised wall, thicker primary costosepta, and a very pronounced crown of paliform lobes. In addition, E. tarae sp. n. forms relatively small colonies with few corallites.
The type species of Echinophyllia, E. aspera, has overall smaller and more evenly sized corallites than E. tarae sp. n. Although a central corallite can be recognized in small colonies of E. aspera (Veron and Pichon 1980), this is smaller than in the new species and does not have its very thickened septa and pronounced crown of paliform lobes. Although the few secondary corallites in E. tarae sp. n. may be smaller than the central one and comparable in size to those in E. aspera (Figures 5b-c, e), in the latter species the septa are equally thin, while in the former the first cycle septa are markedly thicker. Moreover, E. aspera can form much larger colonies than E. tarae sp. n. (see Veron and Pichon 1980, figures 516, 520). Echinophyllia rugosa Chevalier, 1975, from New Caledonia, has smaller corallites than E. aspera and less numerous septa (Chevalier 1975). E. rugosa was synonymized with E. aspera by Veron and Pichon (1980), and has smaller corallites than E. tarae sp. n.
Among the remainder of the Echinophyllia species, E. echinoporoides and E. costata, have smaller and more numerous corallites with less prominent costosepta ornamentation and a more poorly developed crown of paliform lobes, whereas a central larger corallite is not distinguishable (Veron and Pichon 1980, Veron 2000, 2002. Although a central corallite may be present in E. pectinata and in some colonies of E. patula (Veron 2000), in these species corallites are also smaller than in E. tarae sp. n.. Moreover, in E. pectinata, costae are equal and typically smooth (Veron 2002), corallites of E. patula are typically flush with the colony surface (Hodgson and Ross 1982), and a crown of paliform lobes is absent in both species.
Echinophyllia orpheensis has larger corallites than any of the aforementioned Echinophyllia species. A larger central corallite can be observed in some specimens like in one of the paratypes (Veron and Pichon 1980: Figure 525), and it forms a well-developed crown of paliform lobes and exert septa. However, when compared to E. tarae sp. n., the corallites of E. orpheensis are still smaller and more uniform in average diameter. Furthermore, in E. orpheensis, corallites are often raised and more exsert than in the new species. They also point more irregularly in various directions and have fewer septa with smaller dentations than in E. tarae sp. n..
Live specimens of E. tarae sp. n. can bear strong resemblance with Echinophyllia echinata (confront Figure 9a and Figure 9c) and Echinomorpha nishihirai (confront Figure 9b and Figure 9d). However, the skeletal morphology (Figures 9e-f, 10) helps to distinguish the new species from these two. Echinophyllia echinata forms thin flat to vase shaped colonies, with a conspicuous central corallite and widely spaced radials (Veron and Pichon 1980). The holotype of this species (Saville-Kent, 1871) was most likely a juvenile, as also remarked by Veron and Pichon (1980). The original illustration shows the obvious larger central corallite and the thick costae continuing until the corallum margin, like in specimen IRD HS 3171 from New Caledonia (Figures 9c,  e). Specimens of E. echinata illustrated by Veron and Pichon (1980) were examined at the MTQ, but none of these bears close morphologic similarity with E. tarae sp. n.. In fact, the corallum growth form in E. echinata and the presence of a larger central corallite may indeed remind of E. tarae sp. n. However, the usual pattern of corallite arrangement around the central one in E. echinata typically deriving from a circumoral budding (Figure 9e) is not observed in E. tarae sp. n., in which peripheral budding is observed (Figures 6b, d). Furthermore, the central corallite in E. echinata (Figure 10a) does not have the pronouncedly raised wall typical of E. tarae sp. n. (Figure 10b). Septa in E. echinata are thinner, septal teeth are smaller and more regularly spaced, and are devoid of the typical crown of well developed paliform lobes of E. tarae sp. n.. Echinomorpha nishihirai initially described by Veron (1990) in Echinophyllia and later moved to a new monotypic genus, is similar to E. tarae sp. n. in having a prominent central corallite, widely spaced peripheral corallites of smaller size, and by forming small encrusting colonies with a few corallites. Some of the colonies of E. tarae sp. n. observed in situ bear resemblance with in vivo images of E. nishihirai (Figures 9b,  d). Despite this similarity, the skeletons of the two taxa are remarkably different. The holotype of E. nishihirai (MTQ G 32483) was examined (Figures 9f, 10c). Although the central corallite of the largest collected specimen of E. tarae sp. n. collected is similar in size to that of E. nishihirai, the latter lacks the typical raised rim of the former and its septa are more numerous, thinner and with finer dentations (Figure 10c). In another specimen of E. nishihirai (MTQ G 70283) the central corallite is actually more protruding from the colony surface than in the holotype, with which it shares thinner and more numerous septa reaching the columella and a denser and more acute ornamentation. Furthermore, the typical and obvious crown of paliform lobes of E. tarae sp. n. is not present in E. nishihirai.
In his report on the diversity and distribution of scleractinian corals of the Gambier Islands Chevalier (1974) indicated the presence of Echinophyllia aspera typically found on fringing reefs. Unfortunately, his publication did not include illustrations of the coral species listed by him. The author was a remarkably thorough scientists and his unpublished field notes (cahiers de terrain) are an example of a naturalist's dedication and passion. He wrote these down in a series of notebooks in which he numbered pages and he registered painstakingly all details of reef profile, species distribution, specimens identification, colour and more. The complete series of notebooks is deposited at the MNHN in Paris and I could examine them during a visit in 2012. Field notes of 1969 (from page 1637 to 1707) include notes of Chevalier's fieldwork in the Gambier and served as reference for his 1974 publication. The author collected several specimens of Echinophyllia sp. at different sites in the lagoon which he later identified as E. aspera (Chevalier, 1974). At Agakauitai Island, he sampled specimen GAM78b which he identifies as "Echinophyllia encroutant mais peut être espèce differente, couleur vert foncé" [encrusting Echinophyllia but possibly a new species, colour dark green]. Unfortunately, despite much effort, the Gambier collection of Chevalier could not be located in the Scleractinia collection of the MNHN in Paris. Hence I was unable to verify if the possibly new species found by Chevalier is indeed the same as the one presently described, or if any of the specimens he collected belong to E. tarae sp. n.
In their compilation of zooxanthellate scleractinian coral species at 19 localities in the Eastern, South-eastern, and Central Pacific Ocean Glynn et al. (2007) reported Echinophyllia aspera from the Society, Tuamotu, and Austral Islands in French Polynesia and E. echinata from the Austral mostly based on data from Chevalier (1982) and later additions reworked by Pichon (1985). Again, in absence of a reference collection it is impossible to verify if E. tarae sp. n. has been misidentified with these species and, hence, if its distribution is actually wider than presently reported.

Conclusion
Echinophyllia tarae sp. n. is described from the Gambier Islands, French Polynesia. The species is characterized by a high intraspecific variation of several morphological traits. It also shows typical features that distinguish it from the other Echinophyllia species and from Echinomorpha nishihirai, such as the dimensions and the protrusion of the largest corallite (centrally located in flat colonies), the thickness of the septa, and the development of the crown of paliform lobes. Although the new species is common in the Gambier Islands, its occurrence elsewhere is unknown. The sampling of coral tissue from the type specimens of E. tarae sp. n. will allow molecular analyses in order to examine its phylogenetic relationships with its congeners and other species in the Lobophylliidae.