Cryptochiridae Research Articles

Characteristics of the infestation of Seriatopora corals by the coral gall crab Hapalocarcinus marsupialis Stimpson, 1859 on the great reef of toliara, Madagascar

This study describes the association between the obligatory symbiont coral gall crab Hapalocarcinus marsupialis and its stony coral hosts Seriatopora sp. within the Great Reef of Toliara in Madagascar and attempts to discuss their symbiotic status through comparison with previous studies. These corals are inhabited by crabs living in galls that can be categorised in four distinct morphological stages, where the first one corresponds to a small bud and the last one represents a completely closed gall surrounding the crab inside. Within the reef, 563 colonies of Seriatopora species were observed by scuba-diving at ten different stations: 37.8 % of them were infested by H. marsupialis, with a total of 763 galls, and with a majority of stage 4 galls. Galls are monopolised by females that can have different morphologies. Females store the sperm in two spermathecae and are fertilised when their morphology and size are similar to males and the gall is not closed. Histological observations coupled with scanning electronic microscopy analyses show that closed galls are made of an external living tissue, a mid skeletal layer and an internal living tissue. The internal living tissue includes polyps similar to the external tissue, some of them being sexually mature. Nitrogen and carbon isotopic signatures confirmed that these crabs are filter-feeders and do not feed on their host. This association perfectly highlights the difficulties to define the symbiotic status of a symbiont if one considers inflexible the three categories of symbiosis commonly defined.

Phylogenetic ecology of gall crabs (Cryptochiridae) as associates of mushroom corals (Fungiidae).

Coral-associated fauna is a relatively understudied topic. Hence, the nature of the relationship between an associated organism and its host is usually unknown. In the present study, the obligate associations between gall crabs (Decapoda: Cryptochiridae) and mushroom corals (Scleractinia: Fungiidae) are reviewed from a phylogenetic perspective. Based on field surveys, examination of museum material and a literature review, a total of 35 fungiid species have been found that act as hosts for four gall crab species. Fungiid-associated gall crabs appear to be more geographically widespread than previously known, with new records showing their occurrences from the Red Sea and western Indian Ocean all the way to the central Pacific Ocean. The obligate nature of the association between cryptochirids and their hosts makes them an ideal model taxon to test for possible cospeciation events. The congruence between their phylogenies was tested by using the program Jane 4.0, resulting in cospeciation and duplication events between the crabs and their host corals. The sharing of several closely related host coral species by the same gall crab species or genus may provide support to models indicating phylogenetic relationships within the Scleractinia.

Grapsoid and Gall Crabs (Crustacea: Brachyura: Grapsoidea and Cryptochiroidea) of Easter Island

The grapsoid and gall crab fauna of Easter Island is reviewed, based on historical records and material collected by the Science Museum of Long Island Easter Island Expedition of 1998–1999. Previously, nine grapsoids identified to the species level, but no gall crabs, were recorded from the island. The present work reports on eight species of grapsoids: Pachygrapsus laevimanus Stimpson, 1858 (previously recorded from the island as Pachygrapsus transversus [Gibbes, 1850]); Pachygrapsus plicatus (H. Milne Edwards, 1837) (new record); Leptograpsus variegatus (Fabricius, 1793); Cyclograpsus longipes Stimpson, 1858; Ptychognathus easteranus Rathbun, 1907; Percnon pascuensis Retamal, 2002 (redescribed and figured); Guinusia dentipes (De Haan, 1835); and Guinusia integripes (Garth, 1973) (new combination). Geograpsus crinipes (Dana, 1851) and Guinusia chabrus (Linnaeus, 1758) have been previously recorded from the island; no material of the former was collected and the latter is considered an erroneous identification of Guinusia dentipes. Dacryomaia japonica (Takeda & Tamura, 1981) is the first identified gall crab from the island. Color notes for six species and illustrations for several important morphological characters of Percnon pascuensis are provided.

Metabarcoding dietary analysis of coral dwelling predatory fish demonstrates the minor contribution of coral mutualists to their highly partitioned, generalist diet.

Understanding the role of predators in food webs can be challenging in highly diverse predator/prey systems composed of small cryptic species. DNA based dietary analysis can supplement predator removal experiments and provide high resolution for prey identification. Here we use a metabarcoding approach to provide initial insights into the diet and functional role of coral-dwelling predatory fish feeding on small invertebrates. Fish were collected in Moorea (French Polynesia) where the BIOCODE project has generated DNA barcodes for numerous coral associated invertebrate species. Pyrosequencing data revealed a total of 292 Operational Taxonomic Units (OTU) in the gut contents of the arc-eye hawkfish (Paracirrhites arcatus), the flame hawkfish (Neocirrhites armatus) and the coral croucher (Caracanthus maculatus). One hundred forty-nine (51%) of them had species-level matches in reference libraries (>98% similarity) while 76 additional OTUs (26%) could be identified to higher taxonomic levels. Decapods that have a mutualistic relationship with Pocillopora and are typically dominant among coral branches, represent a minor contribution of the predators’ diets. Instead, predators mainly consumed transient species including pelagic taxa such as copepods, chaetognaths and siphonophores suggesting non random feeding behavior. We also identified prey species known to have direct negative interactions with stony corals, such as Hapalocarcinus sp, a gall crab considered a coral parasite, as well as species of vermetid snails known for their deleterious effects on coral growth. Pocillopora DNA accounted for 20.8% and 20.1% of total number of sequences in the guts of the flame hawkfish and coral croucher but it was not detected in the guts of the arc-eye hawkfish. Comparison of diets among the three fishes demonstrates remarkable partitioning with nearly 80% of prey items consumed by only one predator. Overall, the taxonomic resolution provided by the metabarcoding approach highlights a highly complex interaction web and demonstrates that levels of trophic partitioning among coral reef fishes have likely been underestimated. Therefore, we strongly encourage further empirical approaches to dietary studies prior to making assumptions of trophic equivalency in food web reconstruction.

A new gall crab species (Brachyura, Cryptochiridae) associated with the free-living coral Trachyphyllia geoffroyi (Scleractinia, Merulinidae)

A new species of gall crab is described from the free-living stony coral Trachyphyllia geoffroyi. Specimens were collected during field work in Lembeh Strait (Indonesia) and off Kudat (Malaysian Borneo). This new species, here named Lithoscaptus semperi sp. n., is the ninth species assigned to the genus. It can be separated from its congeners by not having the internal orbital angle extending beyond the external orbital angle, and by the stout female P2 merus with prominent distomesial projection. In addition, the carapace surface appears smooth, despite having small tubercles on the anterior half, and is without noticeable spines, other than those on the frontal margin. The distinctive carapace pattern in life is a diagnostic character in male specimens.

Host relations and DNA reveal a cryptic gall crab species (Crustacea: Decapoda: Cryptochiridae) associated with mushroom corals (Scleractinia: Fungiidae)

Mushroom corals of the Indo-West Pacific Fungiidae (Scleractinia) provide habitats for a rich associated fauna, including three species of gall crabs (Cryptochiridae). During the course of the present study gall crabs were sampled from many different fungiid hosts. Based on this ‘reversed’ approach - by studying coral symbionts from a host perspective - a previously unnoticed host specificity pattern was detected. The sampling of gall crab fauna per host coral combined with molecular analyses of H3 nDNA, 16S and COI mtDNA revealed a cryptic gall crab species closely related to Fungicola fagei. This new species, described hereafter as Fungicola syzygia sp. nov., is predominantly associated with the mushroom coral genera Cycloseris and Pleuractis, whereas its sibling species F. fagei is only known to be associated with the host genera Podabacia and Sandalolitha. Based on morphology F. syzygia sp. nov. is difficult to distinguish from F. fagei, but there are subtle differences in carapace shape, the lateral carapace margins, the border between the orbital angles and the merus of the third maxilliped, as well as in the carapace length/width ratio. The type material of F. utinomi and F. fagei is figured for comparison.

Host species, range extensions, and an observation of the mating system of Atlantic shallow-water gall crabs (Decapoda: Cryptochiridae)

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 Curacao (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 Curacao. 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.

The curious case of Neotroglocarcinus dawydoffi (Decapoda, Cryptochiridae): unforeseen biogeographic patterns resulting from isolation

Coral gall crabs form a commonly overlooked component of the associated fauna of shallow-water reef corals and therefore little is known about their ecology and biogeography. This study investigated the biogeography and phylogenetic position of the informal ‘Detocarcini’ species group within the Cryptochiridae. We used molecular data for two mitochondrial markers (COI and 16S) obtained from gall crabs covering (part of) a wide geographic range: the Red Sea, Malaysia, Indonesia and New Caledonia. Our phylogeny reconstructions portrayed the ‘Detocarcini’ as paraphyletic within the monophyletic Cryptochiridae. A phylogeographic clustering was noticed in Neotroglocarcinus dawydoffi that was absent in its sister species, N. hongkongensis, and the closely related species Pseudocryptochirus viridis. A Neighbour Network was estimated for the N. dawydoffi dataset to visualize the similarity between sequences from different biogeographic areas, resulting in three groupings: (1) New Caledonia with Lembeh/Ternate (eastern Indonesia), (2) Semporna/Kudat (eastern Malaysia), and (3) Red Sea (Saudi Arabia). Cryptic speciation rather than isolation is discussed and rejected as an alternative explanation for the observed biogeographic pattern.

Monophyly and phylogenetic origin of the gall crab family Cryptochiridae (Decapoda : Brachyura)

The enigmatic gall crab family Cryptochiridae has been proposed to be phylogenetically derived from within the Grapsidae (subsection Thoracotremata), based on the analysis of 16S mtDNA of one cryptochirid, Hapalocarcinus marsupialis, among a wide array of thoracotremes, including 12 species of the family Grapsidae. Here, we test the monophyly and phylogenetic position of Cryptochiridae using the same gene, but with an extended representation of cryptochirids spanning nine species in eight of 21 genera, in addition to further thoracotreme representatives. The results show that gall crabs form a highly supported monophyletic clade within the Thoracotremata, which evolved independently of grapsid crabs. Therefore, the Cryptochiridae should not be considered as highly modified Grapsidae, but as an independent lineage of Thoracotremata, deserving its current family rank. Further molecular and morphological studies are needed to elucidate the precise placement of the cryptochirids within the Eubrachyura.

First Evidence of Coral-Inhabiting Gall Crabs (Cryptochiridae) from the Fossil Record

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GALL POLYMORPHISM OF CORAL-INHABITING CRABS (DECAPODA, CRYPTOCHIRIDAE): A NEW PERSPECTIVE

Coral-inhabiting gall crabs are either obligate symbionts or parasitic associates with their host corals. They form a variety of galls/pits inside the skeleton of living corals. Nine genera of gall crabs on several scleractinian corals were used to test the hypothesis that galls vary among cryptochirid genera. Phylogenetic and morphometric observations were combined to analyze the possible evolutionary significance of gall construction. A high degree of conservation of gall shapes was observed in relation to the gall crabs’ phylogeny. Gall/pit morphology and fidelity was studied in each of the different species of gall crabs. In addition, the correlation analysis results showed a significant linear relationship between crab size (carapace width) and its gall/pit size (opening diameter of gall/pit) (p < 0.001), demonstrating that crabs have the ability to create the gall/pit size which suits to their own size. Phylogenetically related crab species exhibit similar gall shapes; thus, the galls/pit morphology can be considered as an extention of the crabs’ phenotypes.

Assemblages of Two Gall Crabs within Coral Species Northern Red Sea, Egypt

Assemblages of Two Gall Crabs within Coral Species Northern Red Sea, Egypt

Distribution of gall crabs inhabiting mushroom corals on Semporna reefs, Malaysia

Coral reef cryptofauna forms an important component of tropical marine biodiversity, consisting primarily of invertebrates dwelling in and on corals. During a survey carried out around the Semporna peninsula (Sabah, NE Borneo), the occurrence of gall crabs inhabiting mushroom corals was examined on reefs ranging from sheltered to exposed conditions. Out of 44 fungiid species, 19 were found to be associated with gall crabs. The gall crabs were observed at 85 % of the 62 studied sites, and their occurrence rates per site ranged between 0 and 25 %. High occupancy rates were almost equally distributed over the northern (sheltered) and southern (exposed) sites. Sites without gall crabs were all wave-exposed and predominantly under the influence of disturbances, such as blast fishing or relatively high nutrient loads.

Gall crab city: an aggregation of endosymbiotic crabs inhabiting a colossal colony of Pavona clavus

Gall crab city: an aggregation of endosymbiotic crabs inhabiting a colossal colony of Pavona clavus

Host preferences, colour patterns and distribution records of Pseudocryptochirus viridis Hiro, 1938 (Decapoda, Cryptochiridae)

The coral gall crab Pseudocryptochirus viridis is an obligate symbiont of some species of the Indo-West Pacific coral genus Turbinaria. The colour pattern variation within the species is illustrated for the first time. Overviews of the coral host species and distribution records are provided, including new records from Indonesia, Malaysia and Australia.

The mushroom coral as a habitat

The evolution of symbiotic relationships involving reef corals has had much impact on tropical marine biodiversity. Because of their endosymbiotic algae (zooxanthellae) corals can grow fast in tropical shallow seas where they form reefs that supply food, substrate and shelter for other organisms. Many coral symbionts are host-specific, depending on particular coral species for their existence. Some of these animals have become popular objects for underwater photographers and aquarists, whereas others are hardly noticed or considered pests. Loss of a single coral host species also leads to the disappearance of some of its associated fauna. In the present study we show which mushroom corals (Scleractinia: Fungiidae) are known to act as hosts for other organisms, such as acoel flatworms, copepods, barnacles, gall crabs, pontoniine shrimps, mytilid bivalves, epitoniid snails, coralliophilid snails, fish and certain types of zooxanthellae. Several of these associated organisms appear to be host-specific whereas other species are generalists and not even necessarily restricted to fungiid hosts.Heliofungia actiniformisis one of the most hospitable coral species known with a recorded associated fauna consisting of at least 23 species. The availability of a phylogeny reconstruction of the Fungiidae enables comparisons of closely related species of mushroom corals regarding their associated fauna. Application of a phylogenetic ecological analysis indicates that the presence or absence of associated organisms is evolutionarily derived or habitat-induced. Some associations appear to be restricted to certain evolutionary lineages within the Fungiidae, whereas the absence of associated species may be determined by ecomorphological traits of the host corals, such as coral dimensions (coral diameter and thickness) and polyp shape (tentacle size).

New records of gall crabs (Decapoda, Cryptochiridae) from Orchid Island, Taiwan, northwestern Pacific

[Orchid Island (Lan-Yu) (22°1′N 121°5′E), Taitung county, a remote island off Taiwan, harbours well developed hard coral communities. These may provide various favourable habitats for their obligate symbionts, gall crabs. Until now, not even a single species of these crabs had been recorded from Orchid Island. For this study, we collected hard corals by SCUBA diving at the coral reefs surrounding Orchid Island. We identified nine species of gall crabs belonging to nine genera. They include Cryptochirus coralliodytes inhabiting Goniastrea australensis; Lithoscaptus paradoxus on G. australensis; Hiroia krempfi on Hydnophora exesa; Neotroglocarcinus hongkongensis on Turbinaria mesenterina and T. peltata; Pseudocryptochirus viridis on T. mesenterina; Dacryomaia edmonsoni on Psammocora contigua; Opecarcinus crescentus on Coscinaraea columna and Pavona venosa; Utinomiella dimorpha on Pocillopora verrucosa; and Hapalocarcinus marsupialis on P. verrucosa. Including the new records from Orchid Island in this study, the established brachyuran crab fauna of Taiwan now stands at 611 species. Orchid Island (Lan-Yu) (22°1′N 121°5′E), Taitung county, une ile eloignee au large de Taiwan, abrite des communautes de coraux bien developpees. Celles-ci fournissent des habitats varies, favorables a leurs symbiontes obliges que sont les crabes qui forment des galles. Jusqu'a present, pas une seule espece de ces crabes n'avait ete recensee a Orchid Island. Pour cette etude, nous avons recolte des coraux durs en utilisant la plongee sous-marine (SCUBA) dans les recifs entourant l'ile. Nous y avons identifie neuf especes de crabes formant des galles, appartenant a neuf genres differents. Ce sont Cryptochirus coralliodytes, vivant sur Goniastrea australensis; Lithoscaptus paradoxus sur G. australensis; Hiroia krempfi sur Hydnophora exesa; Neotroglocarcinus hongkongensis sur Turbinaria mesenterina et T. peltata; Pseudocryptochirus viridis sur T. mesenterina; Dacryomaia edmonsoni sur Psammocora contigua ; Opecarcinus crescentus sur Coscinaraea columna et Pavona venosa ; Utinomiella dimorpha sur Pocillopora verrucosa ; et Hapalocarcinus marsupialis sur P. verrucosa. Si l'on ajoute les donnees nouvelles recueillies a Orchid Island lors de cette etude, la faune des crabes brachyoures de Taiwan atteint maintenant 611 especes., Orchid Island (Lan-Yu) (22°1′N 121°5′E), Taitung county, a remote island off Taiwan, harbours well developed hard coral communities. These may provide various favourable habitats for their obligate symbionts, gall crabs. Until now, not even a single species of these crabs had been recorded from Orchid Island. For this study, we collected hard corals by SCUBA diving at the coral reefs surrounding Orchid Island. We identified nine species of gall crabs belonging to nine genera. They include Cryptochirus coralliodytes inhabiting Goniastrea australensis; Lithoscaptus paradoxus on G. australensis; Hiroia krempfi on Hydnophora exesa; Neotroglocarcinus hongkongensis on Turbinaria mesenterina and T. peltata; Pseudocryptochirus viridis on T. mesenterina; Dacryomaia edmonsoni on Psammocora contigua; Opecarcinus crescentus on Coscinaraea columna and Pavona venosa; Utinomiella dimorpha on Pocillopora verrucosa; and Hapalocarcinus marsupialis on P. verrucosa. Including the new records from Orchid Island in this study, the established brachyuran crab fauna of Taiwan now stands at 611 species. Orchid Island (Lan-Yu) (22°1′N 121°5′E), Taitung county, une ile eloignee au large de Taiwan, abrite des communautes de coraux bien developpees. Celles-ci fournissent des habitats varies, favorables a leurs symbiontes obliges que sont les crabes qui forment des galles. Jusqu'a present, pas une seule espece de ces crabes n'avait ete recensee a Orchid Island. Pour cette etude, nous avons recolte des coraux durs en utilisant la plongee sous-marine (SCUBA) dans les recifs entourant l'ile. Nous y avons identifie neuf especes de crabes formant des galles, appartenant a neuf genres differents. Ce sont Cryptochirus coralliodytes, vivant sur Goniastrea australensis; Lithoscaptus paradoxus sur G. australensis; Hiroia krempfi sur Hydnophora exesa; Neotroglocarcinus hongkongensis sur Turbinaria mesenterina et T. peltata; Pseudocryptochirus viridis sur T. mesenterina; Dacryomaia edmonsoni sur Psammocora contigua ; Opecarcinus crescentus sur Coscinaraea columna et Pavona venosa ; Utinomiella dimorpha sur Pocillopora verrucosa ; et Hapalocarcinus marsupialis sur P. verrucosa. Si l'on ajoute les donnees nouvelles recueillies a Orchid Island lors de cette etude, la faune des crabes brachyoures de Taiwan atteint maintenant 611 especes.]

Ecological note on Troglocarcinus corallicola (Brachyura: Cryptochiridae) living in symbiosis with Manicina areolata (Cnidaria: Scleractinia) in the Mexican Caribbean

Coral reefs are considered the most diverse and pro-ductive ecosystems on the planet (Levinton 1982).Symbiotic interactions between phylogenetically unre-lated organisms play a very important role in coral reefecology (Carrera-Parra and Vargas-Herna´ndez 1997),and stony corals host many organisms that live on theirsurface or within their skeletons (Abelson et al. 1991).Crabs are commonly associated with corals and may betotally dependent on coral for protection against pre-dators, or as a food source either from coral mucus ortrapped particulate material (Patton 1974; Castro 1976;Rinkevich et al. 1991). Cryptochiridae, or gall crabs asthey are commonly known, are obligate symbionts ofstony corals. These crabs can modify coral morphologyby affecting growth (Simon-Blecher and Achituv 1997;Simon-Blecher et al. 1999). This, in turn, can alter localwater flux and thus the movement of suspended partic-ulate food (Abelson et al. 1991). Two forms of growthmodification have been observed: depressions, called‘‘pits,’’ in massive corals, and flattened spheres, called‘‘galls,’’ made of two valves in branching corals. Thesetwo forms of coral growth modification are associatedwith the alimentary mechanisms of the crabs. Thosefeeders that form pits obtain food from materialdeposited in the depression while those that form gallsare suspension feeders (Abelson et al. 1991).In this note we present ecological and ethologicaldata for Troglocarcinus corallicola Verrill, one of the twoknown species of gall crabs in the Mexican Atlanticwhich lives in symbiosis with the host stony coral,Manicina areolata Linnaeus. Troglocarcinus corallicolaoccurs throughout the Atlantic and is the most widelydistributed of the Atlantic cryptochirids. In the westernAtlantic, this species has been recorded in Bermuda andlocalities from southeastern Florida to Brazil. In theGulf of Mexico it has been previously found in Barra delTordo, Tamaulipas, and in the Veracruz Reef System,Veracruz. The species has been reported as a symbiontof several species of stony corals, including M. areolata(Kropp and Manning 1987).

ASPECTS OF THE GROWTH AND REPRODUCTION OF THE CORAL GALL CRAB HAPALOCARCINUS MARSUPIALIS

Abstract Growth and reproduction were studied in the coral gall crab Hapalocarcinus marsupialis from fringing reefs in the Egyptian Red Sea. The host coral was Stylophora pistillata. The galls were divided into five stages, and the later stages contained larger crabs and a higher proportion of ovigerous females. Female crabs ranged from 1.17 to 5.33 mm in carapace width. They matured at about 2.5-mm carapace width (probably in the fourth instar); maturity was indicated by an increase in abdomen size, ripening ovaries, mating, and egg laying. The largest females were probably in the seventh instar. After maturity females survived for some 10 months and were ovigerous for 80% of that time, producing eight or more broods. These were all fertilised from the original mating. Reproductive investment was high, both per brood and per year.

Aspects of the Growth and Reproduction of the Coral Gall Crab Hapalocarcinus Marsupialis

Aspects of the Growth and Reproduction of the Coral Gall Crab Hapalocarcinus Marsupialis