Description of a new genus of Cryptochiridae ( Decapoda : Brachyura ) associated with Siderastrea ( Anthozoa : Scleractinia ) , with notes on feeding habits

Members of the Cryptochiridae are small gall-crabs that live as obligate symbionts of scleractinian corals. Only two species have so far been recorded in the western Atlantic Ocean. Herein a new Cryptochiridae genus and species is described, and new information is added on the life history of cryptochirids. The new genus is characterized by having the carapace with the lowest deflection angle among the genera, and also shows the following features: thoracic sternite 4 with setules and constriction smaller than half of the width of the basis, anterior margin curved with apical row of granules; third maxilliped with subcircular exopod reaching medially the lateral margin of the ischium; pereiopod 2 with prominent distomesial and anterolateral expansion on the merus, propodus almost twice larger than dactylus; thoracic sternite 7 with complete medial suture, female pleopod 3 uniramous with longitudinal opening. Male first pleopod straight with subdistal curvature of approximately 90°. Individuals belonging to the new genus are found in galls in massive corals although this structure is cited as being characteristic of ramified corals. The long plumose setae of the maxilliped 3 suggest a filter-feeding function, but the toothless chelae suggest that they are used to gather mucus.


INTRODUCTION
The Cryptochiridae Paul'son 1875 constitutes a group of small, sexually dimorphic, cryptic crabs, commonly referred to as "gall-crabs" as they are all obligate symbionts of scleractinian corals.
Described from shallow tropical waters to depths of 140 m approximately, the family is so far represented by 20 genera and 46 species (Kropp andManning 1995, Ng et al. 2008).
Sexual partners may inhabit distinct, adjoining cavities on the coral surface with contact occurring during breeding periods (Kropp andManning 1987, Johnsson et al. 2006).Males usually may move from one colony to another to mate, and are occasionally found outside the cavities as free-living, benthic individuals (Potts 1915, Edmondson 1933, Fize and Serene 1957, Castro 1976, McCain and Coles 1979).Because of their small size, males have also been observed sharing a single gall with conspecific females, eventually attached to the females' abdomen (Henderson 1906, Warner 1977).In fact, it has been suggested that females are likely to be fertilized before the formation of the gall (Warner 1977).Once established on the host surface, cryptochirids are thought to affect or even inhibit coral growth through microscale environmental changes resulting in skeletal flattened spheres ("galls") or depressions ("pits") (Simon-Blecher et al. 1999).Nevertheless, while the galls have been mostly attributed to ramose colonies enclosing water-filtering crabs, the pits have been related to massive corals that usually shelter individuals adapted to feed on living and nonliving particles deposited on the border of the cavities (Potts 1915, Carricart-Ganivet et al. 2004).Hence, circumstantial differentiation among gall and "pit" dwellers has apparently provided a base for the correlation among the different feeding mechanisms of crabs, and the effectiveness of the morphological spatial arrays (branching vs. massive) of coral hosts (Abelson et al. 1993, Carricart-Ganivet et al. 2004).
Functionally, the symbiosis has been biased by a wide range of morphological and behavioral trends, such as the structure of mouthparts, chelae characteristics (Kropp 1986) and filter feeding (Potts 1915, Marshall and Orr 1960, Carricart-Ganivet et al. 2004) in contrast to feeding on coral mucus, tissues and/or trapped particulate material (Kropp 1986, Abelson et al. 1991, Simon-Blecher et al. 1999).Kropp (1986), however, pointed out discrepancies among the filterfeeding apparatus (such as the plumose net associated to the third maxillipeds, antennae and chelae) in other decapods, including caridean shrimps, porcellanid and anomuran crabs, and the fanning system of the cryptochirid maxillipeds, which supports the structure for collecting soft detrital material (as mucus) and tissue from the surface of the host.
Although remaining largely conjectural, as stated by Kropp (op. cit.,p: 382) "ingestion of mucus by cryptochirids does not represent a metabolic drain on the host", and thus gall crabs are unlikely to fit into the category of parasites.
Data on Atlantic species are scattered and refer to the cryptochirids studied when Kropp and Manning (1987) revised the species recorded in the region and erected Detocarcinus (Kropp and Manning, 1987), Cecidocarcinus (Kropp and Manning, 1987) and Opecarcinus (Kropp and Manning, 1987), the former and the latter based on species from Troglocarcinus (Verril, 1908) and Pseudochryptochirus (Hiro, 1938) respectively.Since that revision, no new species records have been added to the Cryptochiridae inventory for the region and the gall crab fauna is exclusively restricted to the occurrence of four species Troglocarcinus corallicola (Verril, 1908), Detocarcinus balssi (Monod, 1956), Opercarcinus hypostegus (Shaw and Hopkins, 1977), and Cecidocarcinus brychius (Kropp and Manning, 1987), all belonging to monospecific genera.Apart from Johnsson et al. (2006), which extended the distribution of O. hipostegus and included some observations on the biology of the family, the literature on Brazilian chryptochirids is restricted to checklists (Coelho and Ramos-Porto 1995, Young 1998, Coelho et al. 2008) or ecological studies of coral associated fauna (Nogueira 2003, Oigman-Pszczol andCreed 2006).
The record of only two species of cryptochirids in Brazil seems more related to the reduced activity in taxonomic research than to the true faunal diversity, indicating that the diversity has been underestimated (Neves et al. 2006, Neves et al. 2008, Neves and Johnsson 2009).
Siderastrea is the most abundant scleractinian coral in Brazil, being easily found in shallow areas of the plateau reef flat, sometimes partially exposed to desiccation (Neves et al. 2006).
Detailed studies have indicated the existence of three siderastreids along the Brazilian coast (Neves et al. 2010) with S. radians and S. stellata being sympatric (Neves et al. 2008).
The present work describes a new genus and species of Cryptochiridae associated with siderastreids and adds new information to the life history of these organisms.
The colonies were immediately transferred to plastic bags and transported to the laboratory, where crabs were located in the sediment or removed from galls under a stereomicroscope (NIKON SMZ 1000) with the aid of flexible forceps, and fixed in 90% alcohol.
Identification of the coral host was at genus level due to the impossibility of differentiating S. stellata and S. radians in the field.For the morphometric and taxonomic analyses, the specimens of Cryptochiridae were measured, dissected and photographed.Photographic documentation was obtained with a Nikon Coolpix 995 digital camera attached to the stereoscopic microscope.Appendages used in diagnosis and definition of the genera were mounted on permanent blades using CMC-9® and then drawn using an Olympus CH30 optical microscope with a camera lucida.SEM images of the carapace were taken to elucidate the microstructure.Specimens were dried at room temperature for a period of 96 hrs, after which they were cleaned with a soft brush.The entire procedure for capturing the images was conducted at the Instituto de Quimica, Universidade Federal da Bahia (IQ/UFBA).The samples were mounted onto SEM stubs, and coated with 35 nm of gold in a Shimadzu IC-50 sputter coater.They were examined and photographed in a Shimadzu Superscan SS-550.
Antennule apex with prominent spine.MXP3 with subcircular exopod reaching half length of outer margin of ischium; anteromesial lobe of ischium reaching merocarpal articulation; merus with prominent distolateral projection.Thoracic sternite 4 covered with setules with constriction smaller than half width of basis, anterior margin curved with apical row of distinct granules.Thoracic sternite 7 with complete medial suture.P2 merus with prominent distomesial and anterolateral expansions, carpus with moderate mesial expansion.PLP3 of female uniramous, longitudinal abdomen opening.Male PLP1 straight, curved approximately 90° subdistally.
Etymology.Kroppcarcinus n. gen. is a combination of Kropp, in honor of Dr. Roy K. Kropp, who has dedicated a good part of his life to the study of Cryptochiridae, plus carcinus, Greek for "crab".Remarks.The Cryptochiridae is so far known by 20 described genera (Ng et al. 2008).Opecarcinus, Troglocarcinus, Cecidocarcinus and Detocarcinus are all recorded in the Atlantic Ocean -Opecarcinus in the western Atlantic and Ascension Island, Troglocarcinus has an amphiatlantic distribution, Cecidocarcinus occurs in deeper environments in the southeastern Atlantic (off western African coast) and in New Caledonia (Pacific Ocean), and Detocarcinus in the eastern Atlantic (western African coast) (Kropp andManning 1987, Manning 1991).
The dorsal surface of the carapace of Kroppcarcinus n. gen. is deflected at an angle varying between 30° and 35°, being 40° in Opecarcinus (Kropp 1990), and approximately 60° in Troglocarcinus (Kropp and Manning 1987).All remaining genera occurring in the Atlantic do not have detectable deflection in the carapace (Kropp and Manning 1987).The pterygostomial region of the new genus shows a suture separating it from the carapace as seen in Troglocarcinus and Cecidocarcinus, while in Opecarcinus and Detocarcinus the pterygostomian region is fused to the carapace.
Kroppcarcinus n. gen.has a subcircular MXP3 exopod, reaching medially the lateral margin of the ischium as in Troglocarcinus, while in Opecarcinus and Cecidocarcinus it reaches ¾ of the total length of the ischium.Distinctly, Troglocarcinus and Cecidocarcinus have an oval exopod while in Opecarcinus it is elliptical.The exopod is absent in Detocarcinus.In Kroppcarcinus n. gen. the MXP3 has anteromesial lobe of the ischium extending to the merocarpal articulation, as observed in Cecidocarcinus.However, in all remaining Atlantic genera it extends beyond the referred articulation (Kropp andManning 1987, Kropp 1990).The thoracic sternite 4 of Kroppcarcinus n. gen. is covered with setules, the constriction is smaller than half the width of the basis and the anterior margin is curved, with an apical row of granules, and is therefore structurally different from Troglocarcinus, which possesses a smooth sternite, the constriction is larger than half the width of the basis and the anterior margin it smooth, and Opecarcinus which shows a thoracic sternite 4 with a traverse line of tubercles close to the constriction and smaller tubercles near the insertion of the P1 (Kropp 1990: Fig. 9c).In Detocarcinus the thoracic sternite 4 is granular, whereas in Cecidocarcinus the sternite is smooth (Kropp and Manning 1987: Figs. 1d and 3b).Kroppcarcinus n. gen.has P2 with prominent distomesial expansion on the merus as in Troglocarcinus and Cecidocarcinus, being discrete in Opecarcinus and Detocarcinus.The carpus of Troglocarcinus is highly prominent, being alternatively moderate in Kroppcarcinus n. gen.and Opecarcinus, and absent in Detocarcinus and Cecidocarcinus.
In Kroppcarcinus n. gen. the male PLP1 is straight with a subdistal curvature of approximately 90°, in Troglocarcinus PLP1 is slightly curved along his extension, while in Opecarcinus and Detocarcinus it is slightly curved distally with a robust tip directed later-ally at the apex.In Cecidocarcinus PLP1 is quite curved distally, with a robust tip at the apex and lobe expanded and directed laterally (Kropp and Manning 1987).
Besides these general characteristics, the P1 of Kroppcarcinus n. gen. is visible in the dorsal view in both sexes, while in Troglocarcinus and Opecarcinus the structure is visible just in the male.
In Detocarcinus the medial suture of sternite 7 is absent, but it is complete in Koppcarcinus n. gen.Other differentiating characteristics are the biramous PLP3 in the Detocarcinus and Cecidocarcinus females -in Kroppcarcinus n. gen., Opecarcinus and Troglocarcinus it is uniramous; and the female abdomen opening, transverse only in Detocarcinus (Kropp and Manning 1987) while in the rest of the genera, including Kroppcarcinus n. gen., it is longitudinal.
Besides the two Atlantic genera, Troglocarcinus and Opecarcinus, eight other Cryptochiridae genera have an anteriorly deflected carapace as in Kroppcarcinus n. gen.Among these genera, Neotroglocarcinus (Takeda and Tamura, 1980) and Zibrovia (Kropp and Manning, 1995) have sternite 4 with tubercles, therefore differing from the smooth sternite of the new genus.
Kroppcarcinus n. gen. is distinguishable from Neotroglocarcinus due to a medial suture of sternite 7, but they share a distomesial expansion on the merus of P2 that is absent in all other genera.Description.Female: Carapace (Figs. 2A, 5A, 6A) 1.3 times longer than broad; slightly laterally inflated at branchial region, narrowing slightly towards front, as far as irregular depression near protogastric region; posterior surface convex.Anterolateral angle without lobe or spine; carapace with lateral margin lacking distinct border of tubercles.
Antennule with lateral projection reaching inner margin of eyestalk; ornamented with spines, including prominent distal one, surface covered with setae and sparse small tubercles (Figs.2D and 5B).
MXP3 (Fig. 2E) with subcircular exopod, reaching medially lateral margin of ischium, armed with seta; ischium covered with sparse setae, lateral margin toothed, with 4 setae, mesial margin with 6 setae and 14 insertions of possibly broken setae, anteromesial lobe of ischium reaching merocarpal articulation.Merus slightly longer than wide; narrower than half ischium width, external lateral margin toothed, with 6 insertions of setae; distolateral projection prominent, armed with 8 setae.Number of setae increasing considerably in the last three segments.All setae plumose.Remaining mouthparts as in representatives of Troglocarcinus and Opecarcinus.
Chelipeds (P1) (Fig. 2F) equal.Dactylus longer than dorsal margin of palm; smooth dorsally (Fig. 2F).Dorsal margin of palm showing small tubercles and setae.External surface of palm flat, with small setae.Carpus, merus tuberculate, dorsal margin with setae.Merus not extending beyond anterolateral angle of carapace, visible in dorsal view.Sternite 4 (Figs.3A, 5C-D) with setae, constriction smaller than half of width of basis, anterior margin curved with distinct apical line of granules.
Description.Male: similar to the female, though smaller (Figs. 4a,6b).Cheliped more robust than in the female.Margins of abdomen convex, telson semi-oval (Fig. 4B).PLP-I with accentuated naked curvature distally (Fig. 4C).External lateral margin of PLP-I with a row of plumose setae ranging from the midlength to the end; inner lateral margin with plumose setae subdistally and proximal region covered with short setae.
Distribution.Although Kroppcarcinus siderastreicola n. gen.n. sp. has been recorded from the typelocality of Guarajuba and also in Praia do Forte, both located closely to the north coast of Bahia State, it is probable that it has a wider distribution, because the host is found from Rio de Janeiro to Maranhão States.

DISCUSSION
Cryptochirids are responsible for peculiar deformities in the growth pattern of coral colonies (Simon-Blecher andAchituv 1997, Simon-Blecher et al. 1999).These organisms, however, do not follow the process of endolithic animals such as some bivalves, sponges and polychaetes, which perforate the calcium carbonate skeletal matrix, forming galleries and tunnels inside the corals (Tribollet and Golubic 2005).In fact, the cavities where the crabs are lodged derive solely from the contact of the symbiont' s body on the polyp, causing a local loss of tissue, followed by the feeding activities that can provoke small scale alterations in the circulation pattern of the water around the colony.Despite the cryptic habit of the females who live their life cycle inside the cavities, cryptochirids should be considered symbionts and part of the epibenthic fauna living associated with scleractinid corals.
As established by Carricart-Ganivet et al. (2004), the structure designated 'cavity' ('pits') is typically observed in massive corals, while those denominated 'galls' occur in branching corals.There is, however, no consensus about the use of these terms in the literature.In fact, it was not possible to apply this concept to K. siderastreicola n. sp. and its coral host.
Siderastrea corals are distributed on the reef plateau along the northeast coast of Brazil, and include two species: the endemic S. stellata and the Caribean S. radians.Both are characterized by massive, eventually incrusting or slightly flat, semi-or spherical colonies (Neves 2004, Neves et al. 2006).Despite the host characteristics, the cavities of K. siderastreicola n. sp.(Fig. 6c) induce the formation of galls instead of pits as shown in the massive coral Mancina areolata by Carricart-Ganivet et al. (2004).
The gall pattern of Kroppcarcinus n. gen.can be related to the colony morphology of Siderastrea, since a similar arrangement has been observed in incrusting colonies of Agaricia agaricites, another species hosting cryptochirids and found in shallow water.Galls therefore take on the shape of a dome corresponding to the exact outline of the crab lodged in its interior.It was also verified that the galls are shallow, being wider at the opening, and not extending beyond the length of the symbiont.
The feeding habit of cryptochirids may be related to the burrow type they occupy.Carricart-Ganivet et al. (2004) suggested that cavity inhabitants feed on the material deposited in the depression, while gall-formers feed on suspension material (e.g.filter-feeding).
Laboratory observations of live specimens of K. siderastreicola n. sp., however, indicate that crabs do not follow any of these patterns.
The long and abundant plumose setae of the third maxilliped are similar to the homologous appendage described by Kropp (1986) for Utinomiella dimorpha, Favicolla rugosa and Hapalocarcinus marsupialis, suggesting a filter-feeding pattern as previously described among chriptochirids by Marshall and Orr (1960).Notwithstanding, the new species also uses the chelipeds to take food to the mouth parts as reported for H. marsupialis by Kropp (1986), which are capable of tearing tissue fragments with toothed chelae.The toothless chelae of the new species would hardly be able to undertake such a task and therefore are most probably used solely for gathering mucus portions for the mouth parts.
In spite of these characteristics, K. siderastreicola is not considered a parasite because the feeding habit based on filtering and mucus gathering agrees with Kropp's (1986) interpretation that such cryptochirids may not represent a metabolic drain.
Most studies on Brazilian cryptochirids have been restricted to ecological studies.Nogueira (2003) cited the occurrence of T. corallicola and O. hypostegus in colonies of Mussismilia hispida Verrill 1902.The identifications were possibly based on Melo (1996), in which there were only brief descriptions of the two species, cited as the only Brazilian representatives of the family.Melo (1996) did not list the species from the southeast coast of Brazil, and Opecracinus had not been described, until then, in association with representatives of mussid corals.Similarly, Oigman-Pszczol and Creed (2006) dealt with the distribution and abundance of the associated fauna Siderastrea stellata and Mussismilia hispida.No destructive methods were applied and they based their results solely on field observations.Considering the singular characteristics of the Brazilian coral fauna and the role played by the coral as a specialized habitat for several life forms, including the symbiotic gall crabs, which are important examples of co-adaptation and co-evolution in coral reef communities, it is expected that the updates and taxonomic revisions of fauna inventories will reveal a greater diversity than previously known for the South Atlantic.