Diversification and distribution of gall crabs (Brachyura: Cryptochiridae: Opecarcinus) associated with Agariciidae corals

Coral reefs are home to the greatest diversity of marine life, and many species on reefs live in symbiotic associations. Studying the historical biogeography of symbiotic species is key to unravelling (potential) coevolutionary processes and explaining species richness patterns. Coral-dwelling gall crabs (Cryptochiridae) live in obligate symbiosis with a scleractinian host, and are ideally suited to study the evolutionary history between heterogeneous taxa involved in a symbiotic relationship. The genus Opecarcinus Kropp and Manning, 1987, like its host coral family Agariciidae, occurs in both Indo-Pacific and Caribbean seas, and is the only cryptochirid genus with a circumtropical distribution. Here, we use mitochondrial and nuclear DNA gene fragments of Opecarcinus specimens sampled from 21 Indo-Pacific localities and one Atlantic (Caribbean) locality. We applied several species delimitation tests to characterise species diversity, inferred a Bayesian molecular-clock time-calibrated phylogeny to estimate divergence times and performed an ancestral area reconstruction. Time to the most recent common ancestor (tMRCA) of Opecarcinus is estimated at 15−6 Mya (middle Miocene—late Miocene). The genus harbours ~ 15 undescribed species as well as several potential species complexes. There are indications of strict host-specificity patterns in certain Opecarcinus species in the Indo-Pacific and Atlantic, however, a robust phylogeny reconstruction of Agariciidae corals—needed to test this further—is currently lacking. The Indo-West Pacific was inferred to be the most probable ancestral area, from where the Opecarcinus lineage colonised the Western Atlantic and subsequently speciated into O. hypostegus. Opecarcinus likely invaded from the Indo-West Pacific across the East Pacific Barrier to the Atlantic, before the full closure of the Isthmus of Panama. The subsequent speciation of O. hypostegus, is possibly associated with newly available niches in the Caribbean, in combination with genetic isolation following the closure of the Panama Isthmus.

Biogeography and Host Usage of Coral-Associated Crustaceans: Barnacles, Copepods, and Gall Crabs as Model Organisms

Most of the diverse groups of crustaceans associated with scleractinian and fire corals form symbiotic relationship with their coral hosts. Coral-associated barnacles include species from the orders Acrothoracica and Thoracica. Most of the coral-associated barnacles belong to the family Pyrgomatidae in Thoracica. Within Pyrgomatidae, the subfamily Ceratoconchinae contains mostly extant species and is present from Florida through the Caribbean to Brazilian waters. The subfamily Megatrematinae has lower species diversity and has a cosmopolitan distribution (except the Eastern Pacific). The Pyrgomatinae are the most species-rich subfamily and distributed only in Indo-West Pacific waters. Host usage of pyrgomatinid barnacles varies spatially, probably related to coral host diversity. Copepods are the most common and most abundant coral-associated crustaceans, often associated with scleractinian, gorgonian, and alcyonacean corals. More than 90% of coral-associated copepods are endemic to the Indo-West Pacific. In contrast, only a few species (<10%) have been discovered from the Atlantic due to several historical perturbations reducing the diversity of their coral hosts. The communities of coral-associated copepods thus show dramatic differences between geographic regions, notably between the Indian, Pacific, and Atlantic Oceans. Brachyurans of the family Cryptochiridae (gall crabs) are obligate associates or parasites, of scleractinian coral hosts in tropical and subtropical seas, being a monophyletic group of only 52 species, from the intertidal to the deep sea (to 512 m) habitats with most (46) recorded in the seas of the tropical Indo-West Pacific and none being cosmopolitan. Atlantic species of Cryptochiridae, apparently not phylogenetically related, display less strict host specificity than their Indo-West Pacific counterparts. Current phylogenetic understandings of the group remain preliminary, while one consistent Indo-West Pacific clade reflects rapid species diversification during the last ~15 million years.

The coral genus Caulastraea Dana, 1846 (Scleractinia, Merulinidae) as a new host for gall crabs (Decapoda, Cryptochiridae), with the description of Lithoscaptus tuerkayi sp. nov.

A new gall crab species is described from the stony coral genusCaulastraea, a new host coral genus for Cryptochiridae crabs. Specimens were collected during fieldwork off Kudat (Malaysian Borneo) and Okinawa (Japan). Further material was retrieved from the collections of the Institute of Oceanography in Nha Trang (Vietnam). The new species, here namedLithoscaptus tuerkayisp. nov., is the tenth assigned to the genus in which it is tentatively placed. It can be separated from its congeners by the strongly demarcated, inverted V-shaped protuberance flanking the mesogastric region, with denuded spots on the anterolateral sides of this inverted V-shape, as well as the denuded area just below the frontal margin. Based on morphology and COI sequence data, the closest species toL.tuerkayisp. nov. is determined to beLithoscaptus helleri(Fize & Serène, 1957).

Occurrence patterns of coral-dwelling gall crabs (Cryptochiridae) over depth intervals in the Caribbean

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 corallicolaandKroppcarcinus siderastreicola. The overall gall crab prevalence rate was 20.3% across all available host corals at all depths. The agariciid-associated speciesO. hyposteguswas found to mostly inhabitAgaricia lamarckiand its prevalence was highest at deeper depths, following the depth distribution of its host.Kroppcarcinus siderastreicola,associated withSiderastreaandStephanocoenia,inhabited shallower depths despite higher host availability at deeper depths. The generalist speciesT. corallicolashowed 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.

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.