Meij, S.E.T. van der

Infrequently studied coral species are seldom mentioned as host organisms of associated fauna. Here we report on the stony coralAgaricia tenuifoliaDana, 1848 hosting a gall crab (Cryptochiridae) for the first time. This coral-dwelling crab was observed at the southern coast of Bonaire in the Dutch Caribbean. Based on the shape of the dwelling, and the host specificity of cryptochirids, the crab is tentatively identified asOpecarcinus hypostegus (Shaw & Hopkins, 1977).

The iconic gastropod genus Cyphoma is commonly observed in the Caribbean, where it lives in association with various octocorallian hosts. Each species in the genus Cyphoma has a unique, characteristic mantle pattern and colouration, which separates the valid taxa. Because of its abundance and recognisability Cyphoma gibbosum has been used as a model organism in several studies concerning allelochemicals, reef degradation, and physical defence mechanisms. Molecular analyses based on four molecular markers (COI, 16S, H3 and 28S) for three Cyphoma species (C. gibbosum, C. mcgintyi, C. signatum) and an unidentified black morph, collected from three localities in the Caribbean, show that they represent morphological varieties of a single, genetically homogeneous species. This outcome is in agreement with previous anatomical studies. As a result C. mcgintyi and C. signatum are synonymised with C. gibbosum, which is a key result for future work using C. gibbosum as a model organism. The striking morphological differences in mantle pattern and colouration are hypothesised to be the result of one of three possible scenarios: rapid divergence, supergenes (including balanced polymorphism), or incipient speciation. 

The effectiveness of migration in marine species exhibiting a pelagic larval stage is determined by various factors, such as ocean currents, pelagic larval stage duration and active habitat selection. Direct measurement of larval movements is difficult and, consequently, factors determining the gene flow patterns remain poorly understood for many species. Patterns of gene flow play a key role in maintaining genetic homogeneity in a species by dampening the effects of local adaptation. Coral-dwelling gall crabs (Cryptochiridae) are obligate symbionts of stony corals (Scleractinia). Preliminary data showed high genetic diversity on the COI gene for 19 Opecarcinus hypostegus specimens collected off Curaçao. In this study, an additional 176 specimens were sequenced and used to characterize the population structure along the leeward side of Curaçao. Extremely high COI genetic variation was observed, with 146 polymorphic sites and 187 unique haplotypes. To determine the cause of this high genetic diversity, various gene flow scenarios (geographical distance along the coast, genetic partitioning over depth, and genetic differentiation by coral host) were examined. Adaptive genetic divergence across Agariciidae host species is suggested to be the main cause for the observed high intra-specific variance, hypothesised as early signs of speciation in O. hypostegus.

In order to demonstrate how scleractinian corals contribute to marine biodiversity by their host function, information on associated fauna was gathered during a biological survey at St. Eustatius, eastern Caribbean. This knowledge is especially urgent for a host coral such as Helioseris cucullata (Agariciidae), which has undergone strong declines in abundance at various Caribbean localities and has a poor record of associated fauna. New records of H. cucullata as host are presented for the coral gall crab Opecarcinus hypostegus (Cryptochiridae), the Christmas tree worm Spirobranchus giganteus (Serpulidae) and an unidentified serpulid tube worm of the genus Vermiliopsis. A second association record is reported for the coral barnacle Megatrema madreporarum (Pyrgomatidae). Coral-associated copepods were not found on H. cucullata despite a search for these animals. The new records were compared with previous records of other host coral species that showed elements of the same associated fauna. The present findings indicate that new discoveries concerning Caribbean coral reef biodiversity can still be made during field expeditions by targeting the assemblages of associated fauna of specific benthic host species.

Coral-associated invertebrates form a major part of the diversity on reefs, but their distribution and occurrence patterns are virtually unstudied. For associated taxa data are lacking on their distribution across shelves and environmental gradients, but also over various depths. Off Curaçao we studied the prevalence and density of coral-dwelling gall crabs (Cryptochiridae), obligate symbionts of stony corals. Belt transects (10 × 0.5m2) were laid out at 6, 12 and 18 m depth intervals at 27 localities. Twenty-one known host coral species were surveyed, measured, and the number of crab dwellings was recorded to study the influence of host occurrence, depth distribution, and colony size on the occurrence rates of three Atlantic gall crab species: Opecarcinus hypostegus, Troglocarcinus corallicola and Kroppcarcinus siderastreicola. The overall gall crab prevalence rate was 20.3% across all available host corals at all depths. The agariciid-associated species O. hypostegus was found to mostly inhabit Agaricia lamarcki and its prevalence was highest at deeper depths, following the depth distribution of its host. Kroppcarcinus siderastreicola,associated with Siderastrea and Stephanocoenia, inhabited shallower depths despite higher host availability at deeper depths. The generalist species T. corallicola showed no clear host or depth specialisation. These results show that the primary factors affecting the distribution and occurrence rates over depth intervals differed between each of the three Atlantic cryptochirid species, which in turn influences their vulnerability to reef degradation.

Curaçao, Dutch Caribbean, is home to three species of gall crabs belonging to Cryptochiridae, a family obligatorily associated with a wide range of scleractinian host species. Gall crabs are reliant on their host coral; females are sedentary and never leave their dwelling (van der Meij 2014a). One of the three Atlantic gall crab species is Opecarcinus hypostegus (Shaw and Hopkins, 1977), which inhabits corals of the genus Agaricia. Corals of this genus are abundant in the photic zone (<30 m), but also in the mesophotic zone (30–150 m), where they predominantly belong to Agaricia grahamae Wells, 1973 and Agaricia lamarcki Milne- Edwards and Haime, 1851. The latter was found to be most abundant at depths of 25–60 m (Bongaerts et al. 2013). 

During a survey on 31 March, 2014, with the manned CuraSub submersible launched from Substation Curaçao (12°05 ́04.14 ̋N, 68°53 ́53.16 ̋W), a colony of A. lamarcki was observed at approximately 60 m depth (Panel B) exhibiting the characteristic tunnel formed by O. hypostegus. The shape of this tunnel is virtually identical to those found with O. hypostegus crabs in A. lamarcki at shallower depths (Panel A: Slangenbaai, Curaçao). Hence, we contend that this is strong evidence of O. hypostegus at mesophotic depth. 

The present finding is relevant in the light of the “deep reef refugia” hypothesis, which states that mesophotic reefs may act as a refuge in the face of global reef decline (Bongaerts et al. 2010), as it furthers our knowledge on the communities that presently thrive on these deep reefs. 

Coral-associated invertebrates dominate the biodiversity of coral reefs. Some of the associations involving symbiotic invertebrates remain unknown or little studied. This holds true even for relatively wellstudied coral reefs, like those in the Caribbean Sea. Coral gall crabs (Cryptochiridae), obligate symbionts of stony corals, form a much-overlooked component of coral reef communities. Most recent studies on the Atlantic members of Cryptochiridae have been conducted off Brazil and little recent data have become available from the Caribbean region. During fieldwork off Curaçao (southern Caribbean Sea), eight new host coral species, belonging to four coral families, were recorded for three cryptochirid species. Kroppcarcinus siderastreicola Badaro, Neves, Castro and Johnsson, 2012, previously only known from Brazil, and Opecarcinus hypostegus (Shaw and Hopkins, 1977) are new additions to the fauna of Curaçao. Besides the new hosts and geographic range extensions, a free-living male Troglocarcinus corallicola Verrill, 1908 was observed visiting a female of the same species lodged in her gall in an Orbicella annularis (Ellis and Solander, 1786) colony. This is the first photodocumented record of the “visiting” mating system in Cryptochiridae.

Botanical and zoological collections may serve as archives for historical ecologi- cal research on the effects of global change and human impact on coral reef biota. Museum collections may harbour old specimens of reef-dwelling species that have become locally extinct. Such collections also help to determine whether early records of invasive species can be obtained from times when they were not yet recognized as such. A case study (2006) involving Saba Bank, Caribbean Netherlands (former Netherlands Antilles), suggests that the coral reef fauna here may have become impoverished when compared with data obtained during an earlier expedition in 1972. However, the 1972 sampling may have been incomplete, as it was performed by professional divers who were not trained taxonomists, whereas the collecting in 2006 was done by expe- rienced marine biologists who knew the taxa they were sampling. As Saba Bank has been under stress due to the anchoring of large vessels, and invasive species have been a potential threat as well, future studies are needed to obtain more insights into the changing reef biota of Saba Bank. Using this Saba Bank exam- ple, we want to address the importance of natural history collections as reser- voirs of valuable data relevant to coral reef biodiversity studies in a time of global change. As such, these collections are still underexplored and underexploited.