Charles G. Messing

Post-Paleozoic crinoid radiation in response to benthic predation preceded the Mesozoic marine revolution

It has been argued that increases in predation over geological time should result in increases in defensive adaptations in prey taxa. Recent in situ and laboratory observations indicate that cidaroid sea urchins feed on live stalked crinoids, leaving distinct bite marks on their skeletal elements. Similar bite marks on fossil crinoids from Poland strongly suggest that these animals have been subject to echinoid predation since the Triassic. Following their near-demise during the end-Permian extinction, crinoids underwent a major evolutionary radiation during the Middle–Late Triassic that produced distinct morphological and behavioral novelties, particularly motile taxa that contrasted strongly with the predominantly sessile Paleozoic crinoid faunas. We suggest that the appearance and subsequent evolutionary success of motile crinoids were related to benthic predation by post-Paleozoic echinoids with their stronger and more active feeding apparatus and that, in the case of crinoids, the predation-driven Mesozoic marine revolution started earlier than in other groups, perhaps soon after the end-Permian extinction.

Fixed, free, and fixed: the fickle phylogeny of extant Crinoidea (Echinodermata) and their Permian-Triassic origin.

Although the status of Crinoidea (sea lilies and featherstars) as sister group to all other living echinoderms is well-established, relationships among crinoids, particularly extant forms, are debated. All living species are currently placed in Articulata, which is generally accepted as the only crinoid group to survive the Permian-Triassic extinction event. Recent classifications have recognized five major extant taxa: Isocrinida, Hyocrinida, Bourgueticrinina, Comatulidina and Cyrtocrinida, plus several smaller groups with uncertain taxonomic status, e.g., Guillecrinus, Proisocrinus and Caledonicrinus. Here we infer the phylogeny of extant Crinoidea using three mitochondrial genes and two nuclear genes from 59 crinoid terminals that span the majority of extant crinoid diversity. Although there is poor support for some of the more basal nodes, and some tree topologies varied with the data used and mode of analysis, we obtain several robust results. Cyrtocrinida, Hyocrinida, Isocrinida are all recovered as clades, but two stalked crinoid groups, Bourgueticrinina and Guillecrinina, nest among the featherstars, lending support to an argument that they are paedomorphic forms. Hence, they are reduced to families within Comatulida. Proisocrinus is clearly shown to be part of Isocrinida, and Caledonicrinus may not be a bourgueticrinid. Among comatulids, tree topologies show little congruence with current taxonomy, indicating that much systematic revision is required. Relaxed molecular clock analyses with eight fossil calibration points recover Articulata with a median date to the most recent common ancestor at 231-252mya in the Middle to Upper Triassic. These analyses tend to support the hypothesis that the group is a radiation from a small clade that passed through the Permian-Triassic extinction event rather than several lineages that survived. Our tree topologies show various scenarios for the evolution of stalks and cirri in Articulata, so it is clear that further data and taxon sampling are needed to recover a more robust phylogeny of the group.

Urchins in the meadow: paleobiological and evolutionary implications of cidaroid predation on crinoids

Abstract Deep-sea submersible observations made in the Bahamas revealed interactions between the stalked crinoid Endoxocrinus parrae and the cidaroid sea urchin Calocidaris micans. The in situ observations include occurrence of cidaroids within “meadows” of sea lilies, close proximity of cidaroids to several upended isocrinids, a cidaroid perched over the distal end of the stalk of an upended isocrinid, and disarticulated crinoid cirri and columnals directly underneath a specimen of C. micans. Guts of two C. micans collected from the crinoid meadow contain up to 70% crinoid material. Two of three large museum specimens of another cidaroid species, Histocidaris nuttingi, contain 14–99% crinoid material. A comparison of cidaroid gut contents with local sediment revealed significant differences: sediment-derived material consists of single crinoid ossicles often abraded and lacking soft tissue, whereas crinoid columnals, cirrals, brachials, and pinnulars found in the cidaroids are often articulated, linked by soft tissue, and unabraded. Furthermore, articulated, multi-element fragments often show a mode of fracture characteristic of fresh crinoid material. Taken together, these data suggest that cidaroids prey on live isocrinids. We argue that isocrinid stalk-shedding, whose purpose has remained a puzzle, and the recently documented rapid crawling of isocrinids are used in escaping benthic predators: isocrinids sacrifice and shed the distal stalk portion when attacked by cidaroids and crawl away, reducing the chance of a subsequent encounter. If such predation occurred throughout the Mesozoic and Cenozoic (possibly since the mid-Paleozoic), several evolutionary trends among crinoids might represent strategies to escape predation by slow-moving benthic predators.

Taphonomy of isocrinid stalks; influence of decay and autotomy

Stalks of isocrinid crinoids are differentiated into cirri-bearing columnals (nodals) and columnals lacking cirri (internodals). This skeletal differentiation allowed us to test whether stalk fragmentation is random or whether it occurs preferentially at a specific articulation. Our analyses indicate that the patterns of fragmentation in multicolumnal segments of extant isocrinids collected by submersible, by dredging, and in sediment samples, as well as those found as fossils, are nonrandom. The preferred plane of fragmentation corresponds to the synostosis, the articulation between a nodal and the internodal distal to it. In isocrinids this articulation has a characteristic morphology and is the site of autotomy. Although stalk shedding by autotomy may contribute to the observed patterns, decay experiments on isocrinid stalks, both in situ and in the lab, suggest that post-mortem disarticulation also results in nonrandom fragmentation. Thus both processes, autotomy and post-mortem decay, contribute to the observed pattern of fragmentation. Underlying both processes is the organization of soft tissues at synostoses.

Compositional and taphonomic variations in modern crinoid-rich sediments from the deep-water margin of a carbonate bank

Multivariate analyses of the coarse-grained fraction (> 2 mm) of sediments accumulating in deep water (419-434 m) along the western margin of the Little Bahama Bank reneal identifiable, small-scale compositional and taphonomic variations among local subhabitats (ridge crest, slope, foreslope, base of slope, pavements and scour pit) separated by meters to tens of meters. Bulk composition varies between planktic- (crest and slope) and lithic-dominated (pavements, scour pit) sediments. Local macrobenthic skeletal components also vary significantly among subhabitats, but are commonly dominated by echinoid and crinoid material; crinoid columnals contribute 9-52% of the coarse skeletal component of 17 sediment samples considered

Light and vision in the deep-sea benthos: I. Bioluminescence at 500–1000 m depth in the Bahamian Islands

SUMMARY Bioluminescence is common and well studied in mesopelagic species. However, the extent of bioluminescence in benthic sites of similar depths is far less studied, although the relatively large eyes of benthic fish, crustaceans and cephalopods at bathyal depths suggest the presence of significant biogenic light. Using the Johnson-Sea-Link submersible, we collected numerous species of cnidarians, echinoderms, crustaceans, cephalopods and sponges, as well as one annelid from three sites in the northern Bahamas (500–1000 m depth). Using mechanical and chemical stimulation, we tested the collected species for light emission, and photographed and measured the spectra of the emitted light. In addition, in situ intensified video and still photos were taken of different benthic habitats. Surprisingly, bioluminescence in benthic animals at these sites was far less common than in mesopelagic animals from similar depths, with less than 20% of the collected species emitting light. Bioluminescent taxa comprised two species of anemone (Actinaria), a new genus and species of flabellate Parazoanthidae (formerly Gerardia sp.) (Zoanthidea), three sea pens (Pennatulacea), three bamboo corals (Alcyonacea), the chrysogorgiid coral Chrysogorgia desbonni (Alcyonacea), the caridean shrimp Parapandalus sp. and Heterocarpus ensifer (Decapoda), two holothuroids (Elasipodida and Aspidochirota) and the ophiuroid Ophiochiton ternispinus (Ophiurida). Except for the ophiuroid and the two shrimp, which emitted blue light (peak wavelengths 470 and 455 nm), all the species produced greener light than that measured in most mesopelagic taxa, with the emissions of the pennatulaceans being strongly shifted towards longer wavelengths. In situ observations suggested that bioluminescence associated with these sites was due primarily to light emitted by bioluminescent planktonic species as they struck filter feeders that extended into the water column.

Lack of chemical defense in two species of stalked crinoids: Support for the predation hypothesis for mesozoic bathymetric restriction

Abstract Methanol/dichloromethane extracts of (1) the arms and pinnules, and (2) the stalk and cirri of the deep water stalked crinoids Endoxocrinus parrae (Gervais) and Neocrinus decorus (Carpenter) were imbedded at ecologically relevant volumetric concentrations in alginate food pellets containing 2% krill as a feeding stimulant and presented in situ to an assemblage of shallow-water reef fish. Experimental pellets were highly palatable to reef fish; no significant differences in pellet consumption occurred between experimental pellets containing extracts from either species of stalked crinoid or control pellets. Small pieces of cirri, stalks, calyx, arms and pinnules of both species were also tested in in situ feeding assays. While immediate consumption by fish was not apparent, Blue Headed Wrasse ( Thalassoma bifasciatum (Block)) and Dusky Damselfish ( Stegastes fuscus (Cuvier)) bit at pieces of each body component. Similar fish biting behaviors were also observed when two living Endoxocrinus parrae were deployed on the shallow reef. Observations indicate that neither species of stalked crinoid is chemically defended from predation by a natural assemblage of reef fish. This supports the predation hypothesis that restriction of stalked crinoids in deep-water habitats may have resulted from the Mesozoic radiation of durophagous fishes in shallow seas, resulting in a reduction of stalked crinoids from shallow water.

The Crinoid Fauna (Echinodermata: Crinoidea) of Palau

ABSTRACT Taxonomic revisions and a recent survey using scuba place the number of shallow-water (< 50 m) crinoid species known from Palau at 22. Five are new records: Clarkcomanthus littoralis, Comanthus suavia, Alloeocomatella pectinifera, Oxycomanthus comanthipinna, and O. exilis. A submersible survey (to 310 m) recovered five additional new records, four of which are the first representatives of their families from Palauan waters: Eudiocrinus venustulus (Eudiocrinidae), Glyptometra sp. (Charitometridae), Cosmiometra belsuchel Messing, n. sp. (Thalassometridae), and Porphyrocrinus verrucosus (Phrynocrinidae), the first stalked crinoid recorded from Palau. Two of the three specimens of the latter have regenerating crowns, suggesting that this species may be subject to substantial predation or an unstable environment.

Phylogeny of Comatulidae (Echinodermata: Crinoidea: Comatulida): a new classification and an assessment of morphological characters for crinoid taxonomy.

Comatulidae Fleming, 1828 (previously, and incorrectly, Comasteridae A.H. Clark, 1908a), is a group of feather star crinoids currently divided into four accepted subfamilies, 21 genera and approximately 95 nominal species. Comatulidae is the most commonly-encountered and species-rich crinoid group on shallow tropical coral reefs, particularly in the Indo-western Pacific region (IWP). We conducted a molecular phylogenetic analysis of the group with concatenated data from up to seven genes for 43 nominal species spanning 17 genera and all subfamilies. Basal nodes returned low support, but maximum likelihood, maximum parsimony, and Bayesian analyses were largely congruent, permitting an evaluation of current taxonomy and analysis of morphological character transformations. Two of the four current subfamilies were paraphyletic, whereas 15 of the 17 included genera returned as monophyletic. We provide a new classification with two subfamilies, Comatulinae and Comatellinae n. subfamily Summers, Messing, & Rouse, the former containing five tribes. We revised membership of analyzed genera to make them all clades and erected Anneissia n. gen. Summers, Messing, & Rouse. Transformation analyses for morphological features generally used in feather star classification (e.g., ray branching patterns, articulations) and those specifically for Comatulidae (e.g., comb pinnule form, mouth placement) were labile with considerable homoplasy. These traditional characters, in combination, allow for generic diagnoses, but in most cases we did not recover apomorphies for subfamilies, tribes, and genera. New morphological characters that will be informative for crinoid taxonomy and identification are still needed. DNA sequence data currently provides the most reliable method of identification to the species-level for many taxa of Comatulidae.

Habitat Characterization, Distribution, and Areal Extent of Deep-sea Coral Ecosystems off Florida, Southeastern U.S.A.

Abstract. The deep-sea (200–1000 m) seafloor off the southeastern U.S. has a variety of extensive deep-sea coral ecosystem (DSCE) habitats including: deep-water coral mounds; various hard-bottom habitats off Florida including the Miami Terrace, Pourtalès Terrace, and deep-water canyons (Agassiz and Tortugas Valleys); and deep island slopes off western Bahamas and northern Cuba. The dominant structure-forming scleractinian corals are Lophelia pertusa and Enallopsammia profunda; other structure-forming taxa include stylasterid corals, gorgonians, black corals, and sponges. This biota is associated with hard-bottom seafloor of variable high-relief topography which can be remotely identified from bathymetric data. NOAA bathymetric contour maps and digital elevation models were used to identify and delineate the areal extent of potential DSCE habitat in the region from northeastern Florida through the Straits of Florida. These were ground-truthed with 241 dives with submersibles and remotely operated vehicles which confirmed deep-sea coral habitat. We estimate a total of 39,910 km2 of DSCE habitat in this region. By comparison, the estimated areal extent of shallow-water coral habitat for all U.S. waters is 36,813 km2. Bottom trawling remains the greatest threat to DSCEs worldwide, and as a result NOAA has established five deep-water Coral Habitat Areas of Particular Concern (CHAPCs), encompassing 62,714 km2 from North Carolina to south Florida, which will protect much of the known deep-sea coral habitat in this region. High-resolution surveys are not only critical to define DSCE habitats but also to define areas devoid of coral and sponge habitats that may allow for potential bottom fisheries and energy development.