The “Fungia patella group” (Scleractinia, Fungiidae) revisited with a description of the mini mushroom coral Cycloseris boschmai sp. n.

Abstract The recent taxonomic history of extant free-living Cycloseris species is briefly reviewed, resulting in the description of Cycloseris boschmai sp. n. (Scleractinia, Fungiidae) and a discussion on the validity of two other recently described species. Some Cycloseris species were previously considered to belong to the Fungia patella group, which also concerned misidentified museum specimens that actually belong to the new species. Other specimens of C. boschmai sp. n. were photographed and collected in the course of 30 years of fieldwork. The new mushroom coral is compared with other free-living Cycloseris species by means of an identification key. With a maximum diameter of 50 mm, it is the smallest free-living mushroom coral discovered so far. It can also be distinguished by its large primary order costae and variable colouration. Its distribution range is limited to the Coral Triangle, where it can be observed as an uncommon species on lower reef slopes.


Introduction
Mushroom corals (Scleractinia, Fungiidae) form a common element in the fauna of most Indo-Pacific coral reefs. Depending on the species, full-grown specimens are either attached or free-living, which are character states occurring in various evolutionary lineages and therefore do not necessarily reflect phylogenetic relationships among the Fungiidae (Cairns 1984, Hoeksema 1989, 1991b, 2009, Benzoni et al. 2012. After settlement, each fungiid individual starts as a small attached coral (anthocaulus). While corals of attached species obtain a foliaceous or encrusting growth form (Hoeksema 1989, 1993a, 2009, Benzoni et al. 2012, those of free-living species eventually become detached from their stalk, reaching the anthocyathus stage (Wells 1966, Hoeksema 1989, Hoeksema and Yeemin 2011, Hoeksema and Waheed 2012. Owing to their charismatic appearance, abundance and large polyp size, these free-living fungiids are usually easy to find. By growing large and occurring in high densities, they may form mono-or multi-species assemblages covering extensive reef areas (Littler et al. 1997, Hoeksema 2004, 2012a, Elahi 2008, Hoeksema and Koh 2009, Hoeksema and Gittenberger 2010, Hoeksema and Matthews 2011, Hoeksema and Benzoni 2013. They can live on various kinds of reef substrates, ranging from silt to solid rock, from nearshore to offshore and from shallow reef flats to deep reef bases (e.g., Hoeksema and Moka 1989, Hoeksema 1991a, Hoeksema 2012a, 2012b, Waheed and Hoeksema 2013). Mushroom corals themselves may in turn act as habitat to associated faunas consisting of molluscs, crabs, shrimps, acoel flatworms, comb jellies, and fish, some of which are host-specific , Gittenberger and Gittenberger 2005, 2011, Hoeksema and Fransen 2011, Owada and Hoeksema 2011, Bos 2012, 2013a, 2013b, Hoeksema and Farenzena 2012, Gittenberger and Hoeksema 2013, Van der Meij and Hoeksema 2013. The various mushroom coral species vary in size (Hoeksema 1989, 1991b and it is obvious that corals with large surface area and thick skeletons offer most habitat space for associated fauna in contrast to small species . The smallest species among free-living mushroom corals appear to be among the most difficult to identify because they show relatively few distinguishing characters and much ecophenotypic variation Moka 1989, Hoeksema 1993d). Döderlein (1901Döderlein ( , 1902 classified them as the "patella group" within the genus Fungia Lamarck, 1801. He considered them to be the most "primitive" species owing to their small size, imperforate (solid) corallum wall, and rudimentary, hardly discernible costal spines and septal dentations (see Scholtz et al. 2012). The fossil record of this F. patella group could be traced back to the Cretaceous, while its distribution ranged from eastern Africa to the west coast of America and its maximum depth was known to be over 100 m (Döderlein 1901).
Previously, species of the F. patella group were considered to belong to the genera Cycloseris Milne Edwards & Haime, 1849, consisting of complete corals, and Diaseris Milne Edwards & Haime, 1849, representing radially fragmenting corals of the The two specimens (ZMA Coel. collection) earlier described by Van der Horst (1921) as F. patella from Siboga Expedition Station 315 in the Paternoster Islands, Indonesia were considered syntypes (Van Soest 1979). One of these syntypes is a coral with a circular outline and a diameter of 48.5 mm (ZMA Coel. 604, herein designated lectotype; Figure 1), whereas the other is a smaller specimen with hexagonal outline, a diameter of 13 mm, and relatively thick primary costae (ZMA Coel. 723, herein designated paralectotype; Figure 2). Based on these two types, F. marginata is considered a junior synonym of F. costulata (Hoeksema 1989). Because of its doubtful identity, the juvenile specimen is not useful as type. Boschma (1923a) assumed that F. costulata does not have a solid corallum wall and has more or less equal costae and therefore described F. marginata as a species with a solid corallum wall, unequal costae, and thick corallum margin as distinguishing characters. Actually, the type of F. costulata does have a solid wall, whereas costae of all mushroom coral species may be dissimilar in size, including F. costulata (Hoeksema 1989, Gittenberger andHoeksema 2006). Furthermore, the  Boschma, 1923 (ZMA Coel. 604, ethanol), which is a specimen of Cycloseris costulata Ortmann, 1889, collected at Siboga Expedition Sta. 315, Anchorage East of Sailus Besar, in the Paternoster islands, Indonesia. a Upper side b Lower side c Collection labels indicating the first identification by Van der Horst (Fungia patella) and the later one by Boschma (Fungia marginata). Scale bar: 0.5 cm.
identity of F. marginata has never been really clear, because most subsequent authors confused it with other species (see Hoeksema 1989). Boschma (1925) had access to many more F. marginata specimens according to the accompanying identification labels, but he did not mention them in the original species description. These specimens are still available in the collections of the Zoological Museum -University of Copenhagen (UZMK) and Naturalis Biodiversity Center (RMNH Coel.). Among these corals, several specimens are slightly larger than the syntypes and they actually do show enlarged lower order costae, although this was not clearly illustrated in his plates (Boschma 1925: pls. 5-6). These specimens are re-examined in the present study along with many small mushroom corals collected during various recent field surveys . The last ones were striking because of their outstanding long and thick costae and their colorful appearance in comparison with the usual brown hues found in individuals of related species (Hoeksema 1989, Gittenberger andHoeksema 2006). Based on this unique set of characters consisting of a relatively small adult size, enlarged primary order costae and variable coloration, these corals are considered to belong to a new species, herein described as Cycloseris boschmai sp. n.
Wedge-shaped, regenerating fragments not known. The length of the fossa, measured at its bottom, is 1/9 to 1/6 of the corallum length. The columella is formed by a mingled mass of tightly to loosely packed trabeculae. Septa densely packed and straight, unequal in thickness and height. The relatively thick and high septa of lower orders are solid; they are flanked by perforated septa of higher orders. Tentacular lobes absent. Septal margins are finely ornamented with sharp and granular dentations. Their number varies  from 20 to 70 per cm. Septal sides are densely covered by fine granulations, which are irregularly dispersed or arranged in rows perpendicular to the septal margin. Compound synapticulae (fulturae) connecting the septa laterally cannot easily be distinguished because of tight septal arrangement. The solid corallum wall is granulated and may show a detachment scar. The lower side varies from flat to slightly convex. Costae unequal in size, straight and prominent near the corallum margin but less distinct at the centre. Corallum margin may be slightly undulating because of enlarged lower order costae. Costae ornamented with fine granular or acute spines. Their number varies from 15 to 80 per cm. Some individuals have small buds over their surface, especially in the proximity of the corallum margin ( Figure 10). Attached juveniles (anthocaulus stage) are rare (Figure 11). The color of the living animal is variable with hues of red or green ( Figures  11-13). Tentacles small and transparent with white acrospheres at their tips ( Figure 13).
Geographical distribution (Figure 14). The distribution range is limited to the Coral Triangle (Hoeksema 2007): eastern Malaysia (Sabah and Layang Layang), east-  Etymology. The species is named after the late Prof. Hilbrand Boschma, former director of the Rijksmuseum van Natuurlijke Historie (now Naturalis Biodiversity Center), who devoted much of his research time to the study of mushroom corals, including specimens of the new species.

Key to recent free-living Cycloseris species (full-grown, unfragmented specimens), partly after Hoeksema (1989)
1a Lower Septa loosely packed, septa of lower orders thicker and more exsert than others .. 7 6a Central fossa short (< 10% of corallum diameter); all septa perforated, nearly equal in size and tightly packed with little space in between them, maximum corallum diameter 8.

Discussion
Although some material of Cycloseris boschmai sp. n. was already available in museum collections (RMNH, UZMK), the species could only be discovered because of much fieldwork  with proportionate opportunities for observations and sampling to enable separation of the new species from resembling ones. Boschma (1923aBoschma ( , 1925 might have had the same species in mind when he described and studied Fungia marginata, but his selection of type specimens from the Paternoster Islands and the unclear comparison with other species of Döderlein's, Fungia patella group are not convincing. He described this species because of its supposedly thick corallum margin as compared to the other species in the F. patella group, but this character is not useful when applied several other Cycloseris species. The F. marginata material from Banda is suitable as type material of the new species. Because the Banda specimens were wrongly identified by him, this does not concern a new name for an existing species but an entirely new species (Hoeksema 1993b).
These old museum specimens are not just useful as type material but also because they supply information about habitat (field data) and asexual reproduction by budding. They also constitute the oldest material of C. boschmai, which gives them potential historical value as baseline material in studies on changing coral faunas (Hoeksema and Koh 2009, Van der Meij et al. 2010, Van der Meij and Visser 2011, Hoeksema and Wirtz 2013. Cycloseris boschmai sp. n. is the smallest mushroom coral known so far (see key). Superficially, it resembles C. costulata, which has less prominent costae, a more even corallum margin (not undulating), a larger maximum size and less colourful appearance (see Hoeksema 1989, Hoeksema and Van Ofwegen 2004, Gittenberger and Hoeksema 2006. Both species can be found on reef slopes and sandy reef bases. C. costulata is common and wide-spread (Hoeksema 1989(Hoeksema , 2012a and has a variable growth form Moka 1989, Gittenberger andHoeksema 2006), which is why much material had to be examined to find sufficient consistency in the diagnostic characters of the new species.
C. boschmai sp. n. also resembles C. tenuis, which is more oval, less corlourful (see Gittenberger and Hoeksema 2006), and with lower order costae that are rougher and more irregularly ornamented. C. tenuis is most common on upper reef slopes (Hoeksema 2012a), whereas the rarer C. boschmai shows a deeper depth range. The new species also resembles C. vaughani, which has sharper lower order costae, a brown colouration (Hoeksema 1989, Hoeksema andVan Ofwegen 2004) and a much deeper depth range (Hoeksema 2012a).
With the inclusion of C. boschmai sp. n., 11 free-living Cycloseris species are distinguished. Since the taxonomic revision of the Fungiidae by Hoeksema (1989) various other mushroom coral species were reported as new to science (Veron 1990, Hoeksema and Dai 1991, Hoeksema 1993a, 1993c, 2009, 2012c, Latypov 1995, Ditlev 2003, Mondal and Raghunathan 2013. Two of these were originally classified as Cycloseris but they appear to be synonyms of previously described species and one of these is not a Cycloseris. Cycloseris colini Veron, 2000 is a synonym of Lithophyllon spinifer (Claereboudt and Hoeksema 1987). The central dome and upward margins, combined with the large corallum size as described by Veron (2002) are characters commonly found in L. spinifer (see Hoeksema 1993a: fig. 14, Veron 2000, Hoeksema and Van Ofwegen 2004, Hoeksema 2008 fig. 9). A specimen from Palau (MTQ G55817) was designated holotype by Veron in 2002, but since the species was described in 2000 this designation was invalid (ICZN 2011). Hence, this specimen is hereby designated lectotype.
Cycloseris densicolummelus Latypov, 2006 has not been described in an official publication but in an electronic document that was distributed via a CD-ROM. This work should have contained a clear publication date and a statement naming at least five major publicly accessible libraries in which copies of the optical disc were to have been deposited (ICZN 2012). Since only the year of translation has been mentioned in the introduction and no names of libraries were given, this name is not valid. Although the publication by Latypov (2006) is said to be an English translation of an original book in Russian, the latter does not mention C. densicolummelus but "Cycloseris sp. 1" (Latypov 1995: 95, pl. 28 fig. 2). The specimen indicated as "holotype", spec. 1/95158 deposited in the Museum of Institute Marine Biology, Vladivostok 69041, Russia, is from Mai Rut Island, Gulf of Thailand. The illustration with the species description (Latypov 2006: figs 46-8) shows that it is a specimen of C. costulata. The well developed tentacular lobes, the intensive granulation of the lateral septal surfaces and the densely packed trabeculae of columella, which are indicated as diagnostic characters, do not really distinguish C. densicolummelus from C. costulata (see Hoeksema 1989, Gittenberger andHoeksema 2006).
Because C. boschmai is a rare species (considering that most material was gathered during fieldwork in a time span of 30 years) and its geographic distribution range is restricted to the Coral Triangle, not much can be said about its ecology. Specimens are difficult to find, owing to their small body size compared to other mushroom coral species (Hoeksema 1991b, which may be restrictive to the settlement of associated fauna and therefore none of its symbionts was reported previously : "Cycloseris sp."). In the present study, one of the photographed specimens shows a coral barnacle (Figure 11e), which is now the only known associated animal.
Small-sized free-living mushroom corals have been reported to show much mobility (Hoeksema 1988, Yamashiro and, which may help them to escape from competition for space with other organisms (Chadwick 1988, Hoeksema andDe Voogd 2012). The distinctive large lower order costae may be useful as ridges in stabilizing the corals in order to prevent them to slide too rapidly downslope to deeper reef zones with sandy substrate (Hoeksema 1988). The enlarged ridge-like costae can also be seen in some other Cycloseris species (see key) and in the smallsized free-living deep-sea coral Deltocyathus rotulus (Alcock, 1898) (see Cairns and Kitahara 2012: fig 18Q).
Although free-living Cycloseris species were previously considered primitive, this is not the case according to their phylogeny reconstruction . Their predominant habitat of deeper sandy substrates can also be considered an advanced trait (Hoeksema 2012b). The sand in the mouth of nearly dead specimens from Banda ( Figure 10) suggests that they were collected from a sandy substrate, which may not be their preferred habitat. During the author's, fieldwork , no specimens were observed on sandy reef bases. C. boschmai corals are small but not thin, which may not facilitate mobility and sediment-shedding as seen in large-polyped corals (Bongaerts et al. 2012, Erftemeijer et al. 2012. The presence of buds in several of the specimens from Banda, in addition to the sand in their stomata, (Boschma 1925; Figure 10) may also indicate that specimens have been buried (Gilmour 2002). Specimens of C. hexagonalis have been observed to show a similar abundance of buds on a sandy slope in eastern Sabah (BWH personal observation 2009). Budding may be a mushroom coral's, last resort of survival when its mouth is clogged and not capable of food intake anymore (Boschma 1922(Boschma , 1923b(Boschma , 1923c.