Non-technical Summary
The phylum Echinodermata (e.g., sea urchins and starfish) includes enigmatic cyclocystoid fossils. We report skeletal details from exquisite new specimens to revise and reconstruct cyclocystoids and their mode of life. New views of echinoderm evolution show that the unique ‘water vascular system’ supporting the tube feet was within an outer ring of stout ossicles (floor plates). The disk within that ring was a radiating network of plates pierced by numerous holes supporting respiratory structures. Cyclocystoids had a central mouth on the bottom of the disk and were able to traverse the sea bottom using the ring of peripheral tube feet.
Introduction
Cyclocystoids are a rarely encountered and poorly understood class of echinoderms ranging in age from Middle Ordovician to early Carboniferous. Microscopic details of their skeletons are seldom preserved, which means that skeletal homologies, functional morphology, and life mode have long remained enigmatic. Most published reports, including those of Salter and Billings (Reference Salter and Billings1858), Hall (Reference Hall1872), Bather (Reference Bather, Lancester and Black1900), Raymond (Reference Raymond1913), Begg (Reference Begg1934, Reference Begg1939), Kolata (Reference Kolata1975, Reference Kolata and Sprinkle1982), Berg-Madsen (Reference Berg-Madsen1987), Haude and Thomas (Reference Haude, Thomas, Hackler, Heinrich and Krause1994), Smith and Wilson (Reference Smith and Wilson1995), Jell and Jell (Reference Jell and Jell1999), Boczarowski (Reference Boczarowski2001), Glass et al. (Reference Glass, Ausich and Copper2003), Reich and Kutscher (Reference Reich, Kutscher, Harris, Böttger, Walker and Lesser2010), Sprinkle et al. (Reference Sprinkle, Reich, Lefebvre, Zamora and Rábano2015), Reich et al. (Reference Reich, Sprinkle, Lefebvre, Rössner, Zamora and Rahman2017), Ewin et al. (Reference Ewin, Reich, Graham and Cournoyer2019), Müller and Hahn (Reference Müller and Hahn2019), and Ausich and Zehler (Reference Ausich and Zehler2023), focused on the documentation of new occurrences. Reports focusing on aspects of functional morphology and life mode include Sieverts-Doreck (Reference Sieverts-Doreck1951), Kesling (Reference Kesling1963, Reference Kesling and Moore1966), Nichols (Reference Nichols1969, Reference Nichols1972), Kolata (Reference Kolata1975), Derstler (Reference Derstler1985), and Kolata et al. (Reference Kolata, Frank, Kaplan and Guensburg2023). The most thorough investigation is that of Smith and Paul (Reference Smith and Paul1982), whose comprehensive monograph included observations regarding skeletal morphology, anatomy, growth, functional morphology, mode of life, stratigraphic and geographic distribution, phylogeny, evolution, and systematics. Despite this synthesis and the long history of collection and observation, cyclocystoid functional morphology, skeletal homologies, and life mode remain poorly understood.
Here we describe a suite of exceptionally preserved cyclocystoid specimens from the Upper Ordovician (Katian) Kirkfield and Verulam formations of the Lake Simcoe region of southern Ontario, Canada. The stratigraphic framework followed here is that of Paton and Brett (Reference Paton and Brett2020). These specimens are part of a highly biodiverse, well-preserved echinoderm fauna that includes asteroids, ophiuroids, paracrinoids, rhombiferans, edrioasteroids, homalozoans, and cyclocystoids (Sumrall and Gahn, Reference Sumrall and Gahn2006; Cole et al., Reference Cole, Ausich, Wright and Koniecki2018; Blake and Koniecki, Reference Blake and Koniecki2019). The four cyclocystoid species recognized are Cyclocystoides cf. C. scammaphoris Smith and Paul, Reference Smith and Paul1982 , Nicholsodiscus cf. N. anticostiensis Glass, Ausich, and Copper, Reference Glass, Ausich and Copper2003, Zygocycloides marstoni Smith and Paul, Reference Smith and Paul1982, and Brechincycloides stanhynei new genus new species. These new specimens reveal heretofore unreported skeletal details that provide fundamental insights into cyclocystoid anatomy and functional morphology.
Revised cyclocystoid skeletal homologies and orientation require changes in terminology
Adoption of the Extraxial–Axial Theory (EAT) (Mooi et al., Reference Mooi, David, Marchand, David, Guille, Féral and Roux1994, Reference Mooi, David and Wray2005; Mooi and David, Reference Mooi and David1997, Reference Mooi, Rowe, David, Mooi and Telford1998, Reference Mooi and David2008; David and Mooi, Reference David, Mooi, Mooi and Telford1998, Reference David and Mooi1999) for determination of echinoderm skeletal homologies and topologies of the main body components opens the door to a new understanding of cyclocystoids within the framework of early radial echinoderm anatomies (Zamora et al., Reference Zamora, Lefebvre, Hosgör, Franzen, Nardin, Fatka and Álvaro2015; Zhao et al., Reference Zhao, Rahman, Zamora, Chen and Cong2022). Examination of the new taxa offers evidence that the central disk is composed of a complex of ramular and interramular plates with associated epispires, a central periproct, and peripherally placed hydropore/gonopore. Application of the EAT reveals that the central disk is perforate extraxial in origin and did not support the water vascular system (WVS) as suggested in some previous investigations, including that of Smith and Paul (Reference Smith and Paul1982).
These findings require abandonment of traditional cyclocystoid terminology (Table 1). Most fundamentally, we standardize a terminology for anatomical orientation that is independent of life habit interpretation by discontinuing the use of the terms dorsal and ventral, instead applying the term “oral” to the surface bearing the tube foot basins (previously “cupules”) and “aboral” to the surface bearing the epispires. For convenience, we refer to the oral surface as “lower” and aboral surface as “upper” as needed when describing relative positions of features within the cyclocystoid skeleton that lie on neither the oral nor aboral surface. We adopt the terms ramule (adjective: ramular) and interramule (adjective: interramular) to describe the ramified thecal plates of the central disk, now considered aboral. This new terminology is needed in order to avoid terms such as “radial” and “interradial” that would otherwise predispose one to think that these plates collectively housed a WVS (Smith and Paul, Reference Smith and Paul1982).
Revised terminology for morphologic concepts introduced by Smith and Paul (Reference Smith and Paul1982)
Evidence discussed below indicates a living orientation with the epispires facing upward and the tube foot basins of the floor plates facing the substrate. Nichols’s (Reference Nichols1969, fig. 18) description and diagrammatic illustration of cyclocystoid anatomy and orientation are consistent with the skeletal anatomy observed in the specimens described herein. Nichols’s description and prescient illustration reveal (1) a bottlecap-shaped body with a plated aboral surface bearing epispires that likely supported respiratory papulae, (2) a separate but not heavily plated oral surface with a centrally positioned mouth, and (3) a peripheral skirt curving downward over tube feet occupying the tube foot basins on the oral side of the floor plates.
Like all known cyclocystoids, the Brechin specimens possess an aboral central disk consisting of a single layer of ramules and interramules replete with epispires. The oral surfaces of the ramules have shallow channels that extend from the primary ramules at the disk’s center distally through three or four uniserial bifurcations to the proximal edge of the floor plates. The radiating channels likely supported nervous and/or haemal tissue (Kolata et al., Reference Kolata, Frank, Kaplan and Guensburg2023). The structure and organization of the ramules are not consistent with their interpretation as some kind of highly modified, highly branched system of floor plates in which the channels contained water vascular canals, as suggested by Smith and Paul (Reference Smith and Paul1982). Interramules form uniserial rows between the ramules, lack a central channel, and meet the ring of floor plates at floor plate junctures. Epispires are surrounded by annular ossicles that are either in lateral mutual contact as in Cyclocystoides or else widely separated as in Brechincycloides new genus. This anatomical scheme appears to hold for all known cyclocystoids.
Smith and Paul (Reference Smith and Paul1982, p. 606) viewed the organization of the central disk as “effectively a single layer in life” consisting of a network of “radials” (now ramules) and “interradials” (now interramules). For them, this scheme, in combination with the annular ossicles, precluded any extensive internal anatomy. However, the reduced body cavity suggested by this view is unlike that in any known echinoderm (Kolata et al., Reference Kolata, Frank, Kaplan and Guensburg2023). Moreover, our data show that the aboral surface, including ramules, interramules, and annular ossicles, forms a body wall that is most parsimoniously interpreted as a single, integrated layer. Existence of a more extensive body cavity positioned on the oral side of the ramules and interramules of the central disk is, in part, implied by the network of microscopic facet canals that permeate the proximal parts of the floor plates in all known cyclocystoids. The tissue that occupied the canals appears to have originated from a linear series of pores on the proximal side of the floor plates immediately above the radial ducts. In Cyclocystoides cf. C. scammaphoris Smith and Paul, Reference Smith and Paul1982, a total of up to 500 pores can be arranged around the proximal edges of floor plates (Kolata et al., Reference Kolata, Frank, Kaplan and Guensburg2023, p. 646). This network of facet canals also has been observed in Moroccodiscus smithi Reich et al., Reference Reich, Sprinkle, Lefebvre, Rössner, Zamora and Rahman2017 (Reich et al., Reference Reich, Sprinkle, Lefebvre, Rössner, Zamora and Rahman2017, fig. 7.8), and in Sievertsia devonica (Sieverts-Doreck, Reference Sieverts-Doreck1951) as illustrated in Smith and Paul (Reference Smith and Paul1982, pl. 7, fig. 117). The overall distribution of the pores suggests that they emanated from a ring-like structure on the proximal side of the floor plates. The proximal projection of the radial duct and facet canal axes further suggests a higher, more expansive coelomic cavity in continuity with the proximal side of the floor plates below the level of the radial ducts (Figs. 1, 2.1, 2.4, 2.5). Without a lower body wall, the tissue occupying the radial ducts and facet canals would have been positioned outside the body cavity, lacking any obvious function. This evidence and reasoning indicate that the cyclocystoid body cavity was surrounded by: (1) an aboral disk consisting of a layer of ramules and interramules, (2) a ring of floor plates, and (3) a weakly or non-calcified body wall forming the oral surface (Kolata et al., Reference Kolata, Frank, Kaplan and Guensburg2023) that bore the mouth. The latter point explains why evidence for this opening has otherwise been weak in any previous interpretation.
General cyclocystoid anatomy as revealed in perspective views of Cyclocystoides cf. C. scammaphoris Smith and Paul, Reference Smith and Paul1982. (1) Aboral view showing secondary cover plates, floor plates, central disk of annular ossicles resting on and concealing the ramular and interramular plates, papulae (yellow), and centrally positioned periproct; (2) oral view with oral membrane omitted in order to show interior surface of ramular and interramular plates of central disk, periproct and epispires, as well as presumptive nerve and/or haemal tissue; interior of floor plates shows openings of facet and radial canals and inferred position of a pair of water vascular ampullae (blue); exterior surface of floor plates shows tube foot basins, primary and secondary cover plates, and circumferential channel of floor plates supporting circumoral ring of water vascular system (WVS); (3) oral membrane attached to proximal edge of floor plates, each of which bears one or more downward-projecting (substrate-facing) tube feet; primary and secondary cover plates able to fold downward over tube foot basins.
Comparison of morphologic features in two cyclocystoid families recognized here. (1) Model cross section of Brechincycloididae n. fam. based on Brechincycloides stanhynei n. gen. n. sp. (2) Paratype UMMP83161, locality 1, B. stanhynei n. gen. n. sp., aboral surface of three adjacent floor plates. (3) Paratype ISGS-PAL24-1, Cyclocystoides cf. C. scammaphoris Smith and Paul, Reference Smith and Paul1982, aboral surface of four floor plates. (4) Topotype ISGS-PAL22-44, C. cf. C. scammaphoris Smith and Paul, Reference Smith and Paul1982, from Mifflin Member of Platteville Formation, Dixon, Lee County, Illinois (Kolata et al., Reference Kolata, Frank, Kaplan and Guensburg2023); proximal face of floor plate; (5) model cross section of C. cf. C. scammaphoris Smith and Paul, Reference Smith and Paul1982.
We cannot rule out that the layer of ossicles commonly associated with the lower surface of the central disk is part of an oral body wall that collapsed postmortem, compacting onto the complex of ramules and interramules of the central disk. Likewise, we are unable to ascertain if these ossicles are strictly associated with ramules or the channels that run along their oral surfaces. We have found evidence to suggest that the ossicles were more widely distributed, including in areas containing interramules or partially blocking sutural pores (see description of Brechincycloides stanhynei n. gen. n. sp.), which would preclude their interpretation as “cover plates” (Smith and Paul, Reference Smith and Paul1982). For these reasons, we refer to these elements as cryptogenic ossicles.
Localities, methods, and repositories
Locality 1
Gamebridge Quarry: single bedding plane 20.5 m above the contact of the Coboconk and Kirkfield Formations in medium- to coarse-grained, fossiliferous grainstone of the Upper Ordovician (Katian) Verulam Formation near Brechin, Ontario, Canada, 44°29′57.22″N, 79°10′11.85″W.
Locality 2
Gamebridge Quarry blast pile: Upper Ordovician (Katian) Kirkfield and basal Verulam Formations Quarry near Brechin, Ontario, Canada, 44°29′57.22″N, 79°10′11.85″W.
Locality 3
Carden Quarry blast pile: Upper Ordovician (Katian) Kirkfield and basal Verulam Formations near Brechin, Ontario, Canada, 44°34′16.92″N, 79°6′6.42″W.
Photography
All specimens were photographed with a Canon D60 digital camera. Small specimens (< 2 mm) were photographed using a Canon CA6528MP MP-E 65mm f/2.8 1–5X macro lens and larger specimens were photographed using a Canon EF-S 60mm f/2.8 macro USM lens. Focus stacking of images was obtained with an automated macro rail by StackShot, and images were processed with Helicon software. To reveal small details, specimens were stained with a wash of diluted non-waterproof black India ink, dried, and coated with ammonium chloride prior to photography. Some specimens were also photographed immersed in glycerin to enhance features of stereom elements and pore patterns.
Repositories and institutional abbreviations
Type, figured, and other specimens examined in this study are deposited in the following institutions: The University of Michigan Museum of Paleontology (UMMP); The Center for Paleontology, Illinois Natural History Survey, Prairie Research Institute, University of Illinois at Urbana-Champaign (ISGS-PAL); the Field Museum, Chicago, Illinois (PE); Institute of Geological Sciences, British Geological Survey (IGS GSM); and Geological Survey of Canada (GSC).
Systematic paleontology
Phylum Echinodermata Klein, Reference Klein1778
Class Cyclocystoidea Miller and Gurley, Reference Miller and Gurley1895
Discussion
Cyclocystoid fossils are rare and often not preserved well enough to allow complete understanding of their overall anatomy and taxonomic diversity. In part due to these difficulties, it has been customary practice to assign all cyclocystoids to the single family Cyclocystoididae Miller, Reference Miller1882. This convention was followed in the comprehensive cyclocystoid monograph by Smith and Paul (Reference Smith and Paul1982), who recognized eight genera. In addition to Cyclocystoides Salter and Billings, Reference Salter and Billings1858, and Narrawayella Foerste, Reference Foerste1920, they added six new genera including Scotiadiscus, Polytryphocycloides, Apycnodiscus, Sievertsia, Zygocycloides, and Diastocycloides. The key genus-level characters recognized by Smith and Paul (Reference Smith and Paul1982) included (1) contact versus lack of contact between marginals (floor plates) in aboral view, (2) presence versus absence of tubercles within the cupules (tube foot basins), (3) presence versus absence of interseptal plates (aboral interstitial ossicles), (4) number of cupules (tube foot basins) per floor plate, (5) four-fold versus five-fold versus six-fold symmetry of the aboral complex of radials and interradials (ramules and interramules), and (6) shape of the crests on the oral side of the marginals (floor plates). Smith and Paul (Reference Smith and Paul1982) also discussed evolutionary trends within the Cyclocystoididae and provided a possible phylogeny of the family.
Since publication of Smith and Paul’s (Reference Smith and Paul1982) monograph, 15 additional genera have been attributed to the Cyclocystoidea. Of these, nine genera are based on isolated floor plates: Apparatocycloides Boczarowski, Reference Boczarowski2001; Brutocycloides Boczarowski, Reference Boczarowski2001; Chimaerocycloides Boczarowski, Reference Boczarowski2001; Concavocycloides Boczarowski, Reference Boczarowski2001; Linguacycloides Boczarowski, Reference Boczarowski2001; Neocyclocystoides Boczarowski, Reference Boczarowski2001; Paradoxocycloides Boczarowski, Reference Boczarowski2001; Platycycloides Boczarowski, Reference Boczarowski2001; and Smithocycloides Boczarowski, Reference Boczarowski2001. Three post-1982 genera reveal only the oral or aboral surface of the central disk: Minicycloides Haude and Thomas, Reference Haude, Thomas, Hackler, Heinrich and Krause1994; Nicholsodiscus Glass et al., Reference Glass, Ausich and Copper2003; and Perforocycloides Ewin et al., Reference Ewin, Reich, Graham and Cournoyer2019. Three post-1982 genera are based on specimens that expose both the oral and aboral surfaces: Moroccodiscus Reich et al., Reference Reich, Sprinkle, Lefebvre, Rössner, Zamora and Rahman2017; Multisievertsia Müller and Hahn, Reference Müller and Hahn2019; and Brechincycloides new genus.
Based on our analysis of the new Brechin specimens and a review of the literature, we find evidence for two morphologically distinct clades of cyclocystoids based on the anatomy of the ramular facets (Figs. 2.1, 2.5). We recognize that without an outgroup designation for a phylogeny that would place cyclocystoids with more precision in the overall echinoderm tree, the description of these two clades could be subject to future honing. For now, we note that the cyclocystoids themselves form a clade, and that features different between these two clades are unique among all members of the phylum. In other words, the rest of the Echinodermata functions as the outgroup.
The first cyclocystoid clade is exemplified by the genus Cyclocystoides Salter and Billings, Reference Salter and Billings1858. This grouping is supported by several key synapomorphies, including ramular facets that form a low-profile, U-shaped protuberance on the proximal face of the floor plates that partly surrounds the openings of the facet canals (Fig. 2.3, 2.4). The distal edge of the terminal ramule is also U-shaped (Fig. 2.4) and articulates with its counterpart on the proximal face of the floor plate (Kolata et al., Reference Kolata, Frank, Kaplan and Guensburg2023). This clade also possesses crescentic facets in the form of indentations on the aboral proximal margin of each floor plate, by which the annular ossicles of the central disk are framed (Fig. 3.3). The clade includes Cyclocystoides, Scotiadiscus, Apycnodiscus, Diastocycloides, Polytryphocycloides, Zygocycloides, Sievertsia, Nicholsodiscus Glass et al., Reference Glass, Ausich and Copper2003, and Multisievertsia Müller and Hahn, Reference Müller and Hahn2019, and are here retained in the family Cyclocystoididae Miller, Reference Miller1882.
Cyclocystoides cf. C. scammaphoris Smith and Paul, Reference Smith and Paul1982, locality 2, UMMP83155. (1) Enlargement of central disk showing epispire and elliptical channels (blue) on aboral surface of ramules; (2) enlargement of central disk showing distorted annular plates (orange) centered over epispires; (3) aboral surface of central disk showing ramules/interramules and crescentic facets on proximal edge of floor plates. Blue arrows point to pentaradial distribution of floor plates possessing three tube foot basins per ossicle. All other floor plates have two tube foot basins.
The second clade is exemplified by Brechincycloides n. gen., and includes Monocycloides Berg-Madsen, Reference Berg-Madsen1987; Moroccodiscus Reich et al., Reference Reich, Sprinkle, Lefebvre, Rössner, Zamora and Rahman2017; Linguacycloides Boczarowski, Reference Boczarowski2001; Neocyclocystoides Boczarowski, Reference Boczarowski2001; Smithocycloides Boczarowski, Reference Boczarowski2001; Platycycloides Boczarowski, Reference Boczarowski2001; Apparatocycloides Boczarowski, Reference Boczarowski2001; Paradoxocycloides Boczarowski, Reference Boczarowski2001; Concavocycloides Boczarowski, Reference Boczarowski2001; Brutocycloides Boczarowski, Reference Boczarowski2001; Chimaerocycloides Boczarowski, Reference Boczarowski2001; and Minicycloides Haude and Thomas, Reference Haude, Thomas, Hackler, Heinrich and Krause1994. These genera range in age from Middle Ordovician (Darriwilian) to early Carboniferous (Mississippian) and include the oldest and youngest known cyclocystoids.
We assign the genera in this second clade to Brechincycloididae new family, whose apomorphy consists of a flat, attenuated shelf tapering away from the proximal side of each floor plate (Fig. 2.1, 2.2). Approximately one-third of the proximalmost part of the floor plate aboral surface is occupied by a ramular facet that is overlapped by, and in contact with a terminal ramule (Fig. 2.1, 2.2). As in cyclocystoidids, the facet canals extend downward through the proximal part of the floor plate, exiting through a linear series of pores positioned just above the radial ducts. Genera of the Brechincycloididae n. fam. are also unique in that the lateral edges of adjacent floor plates are not in contact aborally and in a distinct saddle shape of the marginal crests on the oral surface. We also note that the aboral surface of the type genus, Brechincycloides n. gen., is composed of distinctly broadened ramules and interramules with rounded distal edges and possesses a central aboral ramular plate rather than four, five or six primary ramules as in the cyclocystoidids.
Remarks
Boczarowski (Reference Boczarowski2001, p. 55) revised the family Cyclocystoididae to include species having a ring consisting of 28–45 marginal (floor) plates, “typically with two and rarely one or three cupules, tube foot basins.” Boczarowski (Reference Boczarowski2001) also proposed the new family Apycnodiscidae to include cyclocystoids with “(16?) 18 to 33 marginal plates, with one to seven cupules.” The number of floor plates in the disk has limited diagnostic value in distinguishing certain cyclocystoid species but has little utility above the genus level. We agree with Reich et al. (Reference Reich, Sprinkle, Lefebvre, Rössner, Zamora and Rahman2017, p. 743) that the number of floor plates is not a diagnostic family-level character, and the family Apycnodiscidae is not recognized herein.
In their description of the moldic Moroccodiscus smithi specimens from Morocco, Reich et al. (Reference Reich, Sprinkle, Lefebvre, Rössner, Zamora and Rahman2017) stated that this cyclocystoid lacks tube foot basins in the floor plates. This putative absence was presented as a diagnostic apomorphy of the new family Moroccodiscidae. However, close examination of their published photos (Reich et al., Reference Reich, Sprinkle, Lefebvre, Rössner, Zamora and Rahman2017, fig. 7.7–7.9) reveals tube foot basins in Moroccodiscus. Apparently, this was already recognized by Reich et al. (Reference Reich, Sprinkle, Lefebvre, Rössner, Zamora and Rahman2017, fig. 7.7–7.9), who stated in the caption: “Partial marginal rings [floor plates] with steinkern fillings of radial ducts and molds of cupule-like cavities [tube foot basins] and frontal plates.” In this paper, we assign Moroccodiscus to Brechincycloididae new family.
Family Cyclocystoididae Miller, Reference Miller1882
Type genus
Cyclocystoides Salter and Billings, Reference Salter and Billings1858.
Emended diagnosis
Ramular facets in lateral position forming low-profile, U-shaped protuberance on proximal face of each floor plate that partly surrounds openings of facet canals; distal edge of terminal ramule also U-shaped, tesselate contact with its counterpart on proximal face of floor plate; proximal edge of floor plate on aboral surface marked by crescentic facets into which distalmost annular ossicles of central disk fit; complete or partial contact between lateral edges of adjacent floor plates on aboral surface.
Included genera
Scotiadiscus Reich and Smith, Reference Reich and Smith2008; Apycnodiscus Smith and Paul, Reference Smith and Paul1982; Diastocycloides Smith and Paul, Reference Smith and Paul1982; Multisievertsia Müller and Hahn, Reference Müller and Hahn2019; Polytryphocycloides Smith and Paul, Reference Smith and Paul1982; Sievertsia Smith and Paul, Reference Smith and Paul1982; Zygocycloides Smith and Paul, Reference Smith and Paul1982; and Nicholsodiscus Glass et al., Reference Glass, Ausich and Copper2003.
Occurrence
Upper Ordovician (Sandbian–Katian), United States and Canada; Silurian (Llandovery–Wenlock), Scotland, England/Wales, Belgium, Sweden, Norway, United States (Ohio); Lower Devonian, Germany; Middle Devonian, Poland; lower Carboniferous, Germany.
Remarks
At least three different cyclocystoidids occur in the Brechin fauna Lagerstätte, including Cyclocystoides cf. C. scammaphoris, Zygocycloides marstoni, and Nicholsodiscus cf. N. anticostiensis.
Genus Cyclocystoides Salter and Billings, Reference Salter and Billings1858
Type species
Cyclocystoides halli Billings in Salter and Billings, Reference Salter and Billings1858, p. 86, pl. X, figs. 2–4, figs. 1, 6, 7 (lectotype Geological Survey of Canada GSC 1416a designated by Raymond, Reference Raymond1913) from the Upper Ordovician Cobourg Beds, Ottawa, Canada, by original designation.
Other species
Cyclocystoides cf. C. scammaphoris Smith and Paul, Reference Smith and Paul1982; C. tholicos Smith and Paul, Reference Smith and Paul1982; C. latus Smith and Paul, Reference Smith and Paul1982; and Cyclocystoides sp. Kolata, Reference Kolata1975.
Diagnosis
Cyclocystoidid with 28–36 floor plates in specimens judged to represent adults; floor plates typically with two tube foot basins each, interspersed pentaradially with floor plates with one to as many as five tube foot basins; six primary ramules; aboral surfaces of floor plates in contact along most of their length and conspicuously pitted; tubercles lacking in tube foot basins; annular ossicles ring-shaped, appressed to base of ramules and interramules, in lateral contact with adjacent annular ossicle and attached to crescentic facets on proximal edge of each floor plate.
Occurrence
Upper Ordovician (Sandbian–Katian); North America only, United States: Illinois, Wisconsin, Missouri, and Tennessee; Canada: Ontario.
Cyclocystoides cf . C. scammaphoris Smith and Paul, Reference Smith and Paul1982
Diagnosis
Cyclocystoides with 25 floor plates in 5-mm-diameter ring and 28–30 ossicles in 22-mm-diameter ring; tube foot basins ventrally positioned, walls parallel, not tapering proximally; floor plate crests vaulted and bearing prominent pustules; aboral surface covered with closely spaced pits.
Material examined
UMMP83155, locality 1.
Remarks
All observable features indicate that this specimen is most like Cyclocystoides cf. C. scammaphoris Smith and Paul, Reference Smith and Paul1982. Specimen UMMP83155 is unique because it reveals a network of elliptical channels on the aboral side of the ramules and interramules series into which the annular ossicles were appressed. Some annular ossicles are distorted or displaced, suggesting that the plates were, in part, supported by connective or some other type of soft tissue (Fig. 3.2).
Genus Nicholsodiscus Glass et al., Reference Glass, Ausich and Copper2003
Type species
Nicholsodiscus anticostiensis Glass et al., Reference Glass, Ausich and Copper2003.
Occurrence
Mill Bay Member of the Vaureal Formation, Upper Ordovician, Katian Stage, along the eastern bank of Oil River at its junction with Kalimazoo Creek, Anticosti Island, Quebec, Canada (NTS 12E/13, 59080:13400).
Nicholsodiscus cf. N. anticostiensis Glass et al., Reference Glass, Ausich and Copper2003
Nicholsodiscus cf. N. anticostiensis Glass et al., Reference Glass, Ausich and Copper2003, locality 1. (1–3) UMMP83166: (1) Enlargement of aboral side of central disk showing five primary ramules, epispires, annular ossicle, and elliptical channels; (2) aboral surface showing periproct; (3) enlargement of central disk edge showing tubercles within tube foot basins. (4, 5) UMMP83160 aboral surface: (4) enlargement of aboral side of disk showing aboral interstitial ossicles; (5) aboral surface showing annular ossicles.
Material examined
Two specimens available from the Brechin outcrops, Locality 1, UMMP83160 and UMMP83166.
Description
Two Brechin specimens reveal aboral surface of theca exposing ramules, interramules, and five primary ramules; both specimens have complete ring of floor plates. Aboral side of ramular/interramular complex marked by round to elliptical facets that accommodate annular plates (Fig. 4.1, 4.2). Annular ossicles round to oval in outline and ring-shaped, central pore aligns with epispire; appressed to base of ramules and interramules. Floor plates numbering 22 or 23 (UMMP83166 and UMMP83160), most floor plates have two tube foot basins, but one or three basins present. Tube foot basins possess small, elongate tubercles of low profile (Fig. 4.3). Primary cover plates articulate with floor plates and gently curve downward; secondary cover plates small, thin, scale-like, arranged in five or six irregular rows.
Remarks
As in N. anticostiensis, the Brechin specimens also have a relatively small thecal diameter (~8 mm) composed of 22 or 23 floor plates that in aboral view are separated by a narrow gap diminishing in width distally to allow contact between the floor plates at their distal edges. The gap is occupied by small, narrow, aboral interstitial ossicles. Tube foot basins were not observed by Glass et al. (Reference Glass, Ausich and Copper2003) but are visible in Brechin specimen UMMP83166, revealing two or three basins with low, elongate tubercles (Fig. 4.3). The Brechin specimens are comparable and possibly conspecific with N. anticostiensis from Anticosti Island.
Genus Zygocycloides Smith and Paul, Reference Smith and Paul1982
Type species
Zygocycloides variabilis Smith and Paul, Reference Smith and Paul1982.
Other species
Zygocycloides magnus (Miller and Dyer, Reference Miller and Dyer1878); Z. marstoni Smith and Paul, Reference Smith and Paul1982, and Z. raymondi (Foerste, Reference Foerste1920). We exclude Z. blairi Smith and Wilson, Reference Smith and Wilson1995, because this species possesses a proximal shelf on the floor plates that is more indicative of the brechincycloidid clade.
Diagnosis
See Smith and Paul (Reference Smith and Paul1982, p. 655).
Occurrence
Upper Ordovician (Sandbian–Katian); North America (United States, Canada) and Europe (Scotland, England, and Belgium).
Zygocycloides marstoni Smith and Paul, Reference Smith and Paul1982
Zygocycloides marstoni Smith and Paul, Reference Smith and Paul1982, locality 3. (1) UMMP83162, oral view showing ramular and interramular series of plates in central disk; (2) UMMP83159, photographed under glycerin, oral view of disk showing tubercles; blue arrows point to pentaradial distribution of floor plates arranged in pairs with three or four tubercles.
Comparison of epispires and annular plates in Zygocycloides Smith and Paul, Reference Smith and Paul1982, and Brechincycloides n. gen. (1) UMMP83162, locality 2, Z. marstoni showing aboral surface of five primary ramules surrounding periproct, crescentic facets on proximal edge of floor plates, annular ossicle (orange) surrounding epispires, and interstitial ossicles; (2, 3) paratype UMMP83167, locality 1, Brechincycloides stanhynei n. gen. n. sp., showing annular ossicles (orange) surrounding epispires, ramules, and central aboral ramule with periproct at center; enlargement shown in 3.
Reference Huxley and Etheridge1865 Cyclocystoides marstoni Huxley and Etheridge, p. 28 (nomen nudum).
Reference Bigsby1868 Cyclocystoides marstoni Salter; Bigsby, p. 25 (nomen nudum).
Reference Begg1939 Cyclocystoides marstoni Salter, MS; Begg, p. 22 (nomen nudum).
Reference Begg1939 Cyclocystoides caractaci Etheridge, MS [sic]; Begg, p. 22 (nomen nudum).
Reference Bassler and Moodey1943 Cyclocystoides marstoni Salter; Bassler and Moodey, p. 148 (nomen nudum).
Reference Kesling and Moore1966 Cyclocystoides marstoni Salter, MS; Kesling, p. U203 (nomen nudum).
Reference Kesling and Moore1966 Cyclocystoides caractaci Salter [sic]; Kesling, p. U203 (nomen nudum).
Reference Smith and Paul1982 Zygocycloides marstoni Smith and Paul, p. 663.
Type specimen
Institute of Geological Sciences, United Kingdom, Geological Survey Museum, IGS GSM 60303, 60304 (part and counterpart).
Diagnosis
See Smith and Paul (Reference Smith and Paul1982, p. 663).
Occurrence
The type specimens are from the Upper Ordovician (Katian) Acton Scott Beds or Cheney Longville Beds, Dicranograptus clingani zone, Shropshire, United Kingdom; Trenton Group of Ottawa, Canada; and Cincinnati, Ohio. The new occurrence reported here is from a blast pile in the Gamebridge Quarry near Brechin, Ontario, Canada. At the time of discovery, the quarry exposed beds of the upper Kirkfield and basal Verulam Formations (Paton and Brett, Reference Paton and Brett2020).
Description
Thecal diameters from 7 mm (17 floor plates) to 13 mm (20 floor plates). Preserved skeletal components include: (1) composite central disk consisting of ramules and interramules plus annular ossicles, (2) ring of floor plates, (3) primary cover plates, and (4) secondary cover plates (Figs. 5.1, 5.2, 6.1). Pentaradial symmetry expressed in arrangement of floor plates with two, three, and/or four tube foot basins (Fig. 5.2). Morphology of Brechin specimens matches the diagnosis of Zygocycloides marstoni in Smith and Paul (Reference Smith and Paul1982).
Material examined
Two slabs of shaly limestone containing at least 30 specimens, including juveniles and adults displaying oral or aboral surfaces; UMMP83159, UMMP83162, and UMMP83163.
Remarks
The Brechin specimens of Z. marstoni reveal wide variations in size of the tubercles in the cupules, commonly within a single specimen. Tubercles are poorly developed or absent in some specimens (Fig. 5.1) and fully developed in others (Fig. 5.2).
Family Brechincycloididae new family
Type genus
Brechincycloides new genus.
Diagnosis
Proximal edge of floor plates bears wedge-shaped shelf that tapers to thin edge; facet canal openings on aboral surface on proximal one-third of floor plates; facet canals curve upward through marginal ossicle in linear series of openings immediately below radial ducts; floor plates lack crescentic facets and U-shaped ramular facets; aboral surfaces of adjacent floor plates not in contact; number of floor plates variable in mature specimens; crests on oral surface of floor plates are saddle-shaped.
Included genera
The family includes, from oldest to youngest: Monocycloides Berg-Madsen, Reference Berg-Madsen1987; Moroccodiscus Reich et al., Reference Reich, Sprinkle, Lefebvre, Rössner, Zamora and Rahman2017; Linguacycloides Boczarowski, Reference Boczarowski2001; Neocyclocystoides Boczarowski, Reference Boczarowski2001; Smithocycloides Boczarowski, Reference Boczarowski2001; Platycycloides Boczarowski, Reference Boczarowski2001; Apparatocycloides Boczarowski, Reference Boczarowski2001; Paradoxocycloides Boczarowski, Reference Boczarowski2001; Concavocycloides Boczarowski, Reference Boczarowski2001; Brutocycloides Boczarowski, Reference Boczarowski2001; Chimaerocycloides Boczarowski, Reference Boczarowski2001; and Minicycloides Haude and Thomas, Reference Haude, Thomas, Hackler, Heinrich and Krause1994. We include the Late Ordovician Zygocycloides? blairi (Smith and Wilson, Reference Smith and Wilson1995) within the Brechincycloididae n. fam. because the floor plates in this species have a proximal shelf with aboral facing radial facets and floor plate crests that are saddle-shaped and wider than long. Currently Z.? blairi is represented by a single specimen revealing only the oral surface.
Occurrences
Middle Ordovician (Darriwilian), Sweden and Morocco; Upper Ordovician (Sandbian–Katian), United States and Canada; Silurian (Llandovery–Wenlock), Scotland, England/Wales, Belgium, Sweden, Norway, United States (Ohio); Lower Devonian, Germany; Middle Devonian, Poland; lower Carboniferous, Germany.
Brechincycloides new genus
Type species
Brechincycloides stanhynei n. gen. n. sp.
Diagnosis
Brechincycloidid with irregularly round to oval theca; relatively small annular ossicles confined to epispires where they form thin composite sleeve inside pore opening; epispires and annular ossicles commonly enveloped in proximal part of floor plates in gerontic specimens; central disk composed of central aboral ramule with medial pore exposing small wedge-shaped plates, plus single layer of broad, subpolygonal ramules and interramules with rounded distal edges and finely pustulose aboral surface; tube foot basin side walls commonly shared by adjacent floor plates.
Occurrence
Late Ordovician (Katian), Brechin, Ontario, Canada; locality 1.
Etymology
Named for the town of Brechin, Ontario, Canada where the specimens were found, and combined with the Greek kykloeidēs = circular.
Remarks
Brechincycloides n. gen. is unique in having relatively small annular plates that generally are not in lateral contact in the central parts of the disk, lacking crescentic facets, approximately one-third of the proximalmost part of the floor plate aboral surface is occupied by a ramular facet that is overlapped by and in contact with a terminal ramule.
Brechincycloides stanhynei new species
Figures 6.2, 6.3, 7–18
Types
Holotype: University of Michigan Museum of Paleontology UMMP83165; paratypes: UMMP83157, UMMP83158, UMMP83161, UMMP83164, UMMP83167, UMMP83168, UMMP83169, UMMP83170.1, and UMMP83170.2. Locality 1. Gamebridge Quarry: single bedding plane 20.5 m above contact of the Coboconk and Kirkfield Formations in medium- to coarse-grained, fossiliferous grainstone of the Upper Ordovician (Katian) Verulam Formation near Brechin, Ontario, Canada, 44°29′57.22″N, 79°10′11.85″W.
Diagnosis
Same as for genus.
Occurrence
Upper Ordovician (Katian Stage) near Brechin, Ontario, Canada. This brechincycloidid is represented by 10 well-preserved specimens that are complete with central disk of ramules and interramules, floor plates, and cover plates. They were discovered in the Gamebridge Quarry near Brechin, Ontario, Canada. Based on the stratigraphic section of Paton and Brett (Reference Paton and Brett2020, fig. 8) and field notes of collector JMK, the specimens were preserved on a single bedding plane 20.5 m above the contact of the Coboconk and Kirkfield Formations in medium- to coarse-grained, bryozoan- and echinoderm-rich grainstone of the Verulam Formation at Locality 1.
Description
Parts of central disk in holotype (UMMP83165, Fig. 8.1–8.3) extracted, exposing oral side of disk. Morphology of theca also revealed in series of sections cut and polished perpendicular to disk (Fig. 9.1–9.3). Theca round to irregularly oval with diameters ranging from 6.5 mm (apparent juvenile) to 38 mm. Central disk (Fig. 7.1) in holotype 73% of thecal diameter (Table 2); central disk composed of central aboral ramule with medial pore exposing small wedge-shaped plates presumed to surround periproct; distally from center disk largely consisting of ramules and interramules approximately 0.5 mm thick in holotype; in oral view plates imbricate toward center of disk; in aboral view plates imbricate away from center; calcite-cleavage faces visible along broken edge of central disk in holotype (Brechin UMMP83165); specimen cross sections (Fig. 9.1–9.3) reveal disk composed of single layer of subpolygonal ramules and interramules; these plates are distinctively broad with rounded distal edges; aboral surface finely pustulose, appears somewhat convex. Ramules with shallow channel on oral surface; bifurcate distally three or four times; terminal ramule overlapping ramular facets on distal aboral surface of floor plates (Fig. 9.1); interramules projecting distally, intersecting floor plates at contact between plates. Three specimens (UMMP83157, UMMP83158, and UMMP83170) with distalmost ramule relatively large in aboral view, convex at center, and distinct from surrounding ramules and interramules; in two specimens, this specialized plate pierced by 80-μm-diameter pore (Figs. 10.1–10.3, 11.1, 12, 13).
Thecal dimensions and number of floor plates in specimens of Brechincycloides stanhynei
Brechincycloides stanhynei n. gen. n. sp., locality 1, holotype UMMP83165. (1) Aboral surface of holotype; arrows point to arc of floor plates and central disk removed to expose adoral surface shown in Figure 8; (2) enlargement showing newly formed floor plate, cover plate system, aboral interstitial ossicles (very small ossicles) filling spaces between floor plates, and annular ossicles surrounding sutural pores.
Brechincycloides stanhynei n. gen. n. sp., locality 1, holotype UMMP83165. (1) Oral surface showing radiating channels covered with small cryptogenic ossicles, extended shelf of floor plates, primary and secondary cover plates; star indicates projected center of central disk of ramules and interramules; (2) radial ducts and linear series of pores marking facet canal openings; (3) circumferential channel and shared tube foot basin side walls.
Brechincycloides stanhynei n. gen. n. sp., locality 1, paratype UMMP83161; polished cross sections through center of theca; (1) ramular and interramular plates, ramular facet, cover plate system; (2) primary cover plate, epispires, tube foot basin; (3) circumferential channel, cover plate system.
Brechincycloides stanhynei n. gen. n. sp., locality 1. (1) Paratype UMMP83157, showing specialized ramular plate; (2) paratype UMMP83158, showing minute pore of presumed hydropore/gonopore; (3) paratype UMMP83170, second example showing minute pore of presumed hydropore/gonopore.
Brechincycloides stanhynei n. gen. n. sp., locality 1, paratype UMMP83170. (1) aboral surface of theca showing specialized ramular plate with hydropore/gonopore and associated juvenile specimen exposed in aboral view; (2) enlargement of aboral surface showing bilobed epispires within plates and bilobed epispires shared between ramular and interramular plates.
Brechincycloides stanhynei n. gen. n. sp., locality 1, paratype UMMP83158; aboral surface of theca showing specialized ramular plate with hydropore/gonopore, ramular and interramular series of plates, and central ramular plate with periproct at center.
Brechincycloides stanhynei n. gen. n. sp., locality 1, paratype UMMP83157; aboral surface of theca showing central aboral ramular plate with periproct at center; distinct pentaradial pattern marked by narrow, presumably immature, floor plates shown with blue arrows and marked A?–E; white arrows point to specialized ramular plate with hydropore/gonopore in CD interray and central aboral ramular plate with periproct at center.
Central disk penetrated by at least five types of pores differing in size, shape, and relative position within or between ramules and interramules; these best viewed on aboral surface and include: (1) relatively large, round pore up to 1.0 mm in diameter at center of central aboral ramular plate (Figs. 6.2, 6.3, 11, 12, 13); (2) round epispires approximately 0.5 mm in diameter shared by adjoining plates and lined with small annular ossicles (Fig. 11); (3) elongate, bilobed epispires up to 0.5 mm in longest dimension that penetrate plate center or are shared by adjoining plates and lined with annular ossicles (Fig. 11.1, 11.2); (4) relatively small-diameter pores 0.3 mm in longest dimension penetrating interramules (Fig. 12); and (5) small pore ~80 μm in diameter on the specialized ramular plate (Fig. 12).
Annular ossicles restricted to outer rim of epispires; composed of 2–5 small, arc-shaped ossicles surrounding interior of pore openings; annulars in contact with ramules and interramules, projecting slightly away from aboral surface (Figs. 6.2, 6.3, 7, 10). In paratypes UMMP83158 and UMMP83169, several epispires with annular ossicles encapsulated within proximal shelf of floor plates (Figs. 12, 14).
Brechincycloides stanhynei n. gen. n. sp., locality 1, paratype UMMP83169. (1) Aboral surface of theca showing epispires within or shared by ramular plates; (2) aboral surface showing small medial ossicles between primary cover plates; (3) floor plates showing facet canal openings; (4) floor plates showing encapsulated epispires with aboral opening surrounded by annular ossicles.
Oral surface of central disk in holotype (UMMP83165) covered with hundreds of microscopic calcareous cryptogenic ossicles embedded in thin, dark, reddish-brown matrix and distributed in poorly defined radial pattern; some ossicles T-shaped; some overlie and block sutural pores (Fig. 8).
Floor plate ring composed of 20–43 plates (Table 2); plate length approximately 50% of width. In holotype (specimen 40 mm wide and 20 mm long), tube foot basins 25%, crests 35%, and proximal marginal shelf with ramular facets 40% average length of floor plate. Tube foot basins oriented obliquely to crests. In oral view, floor plate crests broadly cylindrical; space between plates relatively wide on oral surface, forming V-shaped gap expanding upward (Fig. 8); crest marked by distinct median concave saddle and two lateral ridges; small pustules distributed on saddle; lateral walls oblique, marked by prominent vertical striae fanning outward. Typically, each floor plate with two tube foot basins, however, newly formed ossicles with single cupule or two small tube foot basins all spaced almost equidistant around ring in pentaradial pattern (Figs. 13, 18). Proximal edge of floor plates typically wedge-shaped in cross section and commonly deeply indented and/or possessing encapsulated epispire lined with annular ossicles (Fig. 14). Tube foot basins with relatively high side walls merging with broadly concave cup, side walls curved downward to distal edge of tube foot basin; side wall commonly shared with basins in adjacent ossicle; oral side wall flat, triangular in outline, expanding proximally beneath underlying floor plate crest and contiguous with deeply inset circumferential channel (Fig. 8.3); each tube foot basin giving rise to single radial duct approximately 100 μm in diameter with axis projecting slightly below oral surface of central disk. Most floor plates with two tube foot basins, few irregularly distributed ossicles with one tube foot basin as indicated above. Articulation surface between adjacent floor plates small and positioned near center of ossicle (Fig. 17).
In aboral view, floor plates rectangular to trapezoidal in outline, relatively flat except for slight curve along distal and proximal edges; densely covered with small pustules and wavy ridges formed by coalesced pustules (Figs. 7.2, 10–14). In well-preserved specimens, floor plate surface displays stereom microstructure. Space between adjacent floor plates, not including articulation points, filled throughout growth by microscopic aboral interstitial ossicles with surface texture like that on adjacent cover plates (Fig. 7.2). New floor plates developing as small wedge-shape ossicles, initially growing along distal edges of adjacent floor plates, eventually developing tube foot basins, radial ducts, and facet canals.
Primary cover plates tapering gradually to rounded distal edge, concave on oral side, standing erect or folded down, articulating with distal edge of tube foot basin (Figs. 8, 9). Depression between primary cover plates occupied by small medial ossicle at intersection of adjacent tube foot basin walls and adjacent primary cover plates (Fig. 14.2). Secondary cover plates consisting of numerous, small, imbricate, arrow-shaped ossicles with fine longitudinal striations. In some specimens, cover plate system folded downward to cover tube foot basins and oral crests of floor plates (Fig. 9).
Etymology
Named for Stanley G. Hyne, a long-time collector of echinoderms from the Ordovician rocks near Brechin, Ontario, who provided a key specimen in this investigation.
Remarks
Brechincycloides stanhynei n. gen. n. sp. is similar to Cyclocystoides latus Smith and Paul, Reference Smith and Paul1982 (Smith and Paul, Reference Smith and Paul1982, figs. 21, 73), both occurring in the Upper Ordovician Kirkfield Formation of Ontario, Canada. Cyclocystoides latus is known from two relatively small specimens, both exposing only the oral surface (Smith and Paul, Reference Smith and Paul1982, p. 624–625). Brechincycloides stanhynei n. gen. n. sp.is based on 10 well-preserved specimens with thecal diameters ranging from 6.5 to 38 mm (Table 2), one specimen revealing the oral surface. Characteristics shared by B. stanhynei n. gen. n. sp. and C. latus include a central disk with five primary ramules, tube foot basins lacking tubercles, and a shelf-like extension on the proximal side of the floor plates. Brechincycloides stanhynei n. gen. n. sp. differs in having (1) tube foot basins (cupules) that are approximately 25% the length of the floor plate; 40–45% in C. latus, (2) tube foot basins with curved side walls (Fig. 8.3); straight in C. latus; and (3) proximal shelf that is 40% the length of the floor plate; 20% in C. latus. We judge that B. stanhynei n. gen. n. sp. and C. latus represent two distinct species but recognize that there is a degree of uncertainty due to the small number of available specimens and variations in preservation.
Brechincycloides n. gen. is also like Moroccodiscus Reich et al., Reference Reich, Sprinkle, Lefebvre, Rössner, Zamora and Rahman2017, in commonly exhibiting tube foot basins whose side walls are shared between adjacent floor plates and a central disk composed of subpolygonal ramules and interramules (see Reich et al., Reference Reich, Sprinkle, Lefebvre, Rössner, Zamora and Rahman2017, figs. 6.5, 9.6). Brechincycloides n. gen. differs from Moroccodiscus in having a disk with fewer floor plates, lacking elongate triangular cover plates, and having epispires lined with small annular ossicles that are commonly incorporated into the proximal shelf of the floor plates. In Brechincycloides stanhynei n. gen. n. sp., hundreds of rod- or spear-shaped ossicles, 100–200 μm in length are found resting on the oral surface of the ramules and interramules. In holotype UMMP83165 (Fig. 8) the mass of these cryptogenic ossicles shows alignment, if poorly developed, with the oral complex of ramules and interramules. These cryptogenic ossicles in Brechincycloides stanhynei n. gen. n. sp. are embedded in a distinctive layer of dark reddish-brown calcitic matrix 0.5-mm thick.
Cyclocystoid anatomy
The following is an overview of cyclocystoid functional morphology based on the new specimens described herein and a review of pertinent literature. Our model of cyclocystoid anatomy (Figs. 1, 2, 15) is based on basic topologies and orientation such as those described by Nichols (Reference Nichols1969, Reference Nichols1972). In a subsequent publication, Nichols (Reference Nichols1986, p. 808) retracted his earlier interpretation, stating, “the cupules [tube foot basins] have tubercles within them, and second, they [cupules] do not connect up with the most likely seat of the water vascular system, which provides fluid for tube foot operation.” Nichols (Reference Nichols1986) did not indicate the position of the cyclocystoid WVS, although it appears that by 1986 he thought it was restricted to the central disk and did not involve the ring of floor plates. The new Brechin cyclocystoids provide compelling evidence supporting the original model of Nichols (Reference Nichols1969), in which the tube feet were positioned in the ring of marginal plates that we are asserting are floor plates.
Models of cyclocystoid anatomy. (1, 2) Brechincycloides n. gen. (1) Cross section through center of theca showing central aboral ramular plate with presumptive periproct; papula surrounded by annular ossicle (orange) over epispire; ramular and interramular plates, terminal ramular plate, ramular facet on aboral side of floor plates (yellow); presumed nerve ring and nerve plexus (red, internal facet canal dashed); cover plate system, water vascular system (WVS) (blue) including tube foot, ring canal in circumferential channel, ampulla, and radial duct; oral surface of non- or weakly calcified integument/membrane, mouth at center; cluster of cryptogenic ossicles within body cavity; (2) cross section of aboral surface showing single ramular plate (green), with epispire surrounded by relatively small annular ossicle (orange) not laterally in contact with neighboring annulars; presumptive papula (gray) mounted on epispire, dashed line showing position of lateral channel on oral side of ramule. (3–5) Cyclocystoides sp. (3) Cross section of single ramular plate (green); with epispire surrounded by relatively large annular ossicle (orange) laterally in contact with neighboring annulars; (4) cross section through center of theca showing features comparable to those in Brechincycloides n. gen., cover plate system open on left and closed on right. (5) Cyclocystoides cf. C. scammaphoris PE93328, oral view of central disk showing branched ramulars (green) with channels, interramulars between ramulars.
Floor plates
The floor plates form a dominant part of the skeletal framework and contain distinctive structures including tube foot basins, radial ducts, ramular facets, facet canals, and circumferential and lateral channels, as well as laterally positioned articulation ridges and striae. Nichols (Reference Nichols1972) envisioned the marginal ring of floor plates as housing elements of the WVS. Accordingly, he suggested that the tube foot basins held tube feet used for locomotion and a cover plate system with primary and secondary cover plates acting to protect the tube feet and associated soft tissues. He speculated that cyclocystoids lacked ampullae, further suggesting that the tube feet operated in a manner like those of modern holothuroids, in which the retraction of one foot provides hydraulic pressure for the protraction of a neighboring tube foot (Nichols, Reference Nichols1972, p. 534).
Alternatively, we suggest that ampullae were positioned internally on the proximal side of the floor plates and connected to the tube feet via the radial ducts and lateral channels between floor plates (Figs. 15.1, 15.4,16). We emphasize that each tube foot basin in all known cyclocystoids merges proximally with a single radial duct that extends through the floor plate to the interior of the body. The interior opening of each duct is positioned adjacent to many smaller openings of the facet canal network interpreted to house the nervous and/or haemal systems (Kolata et al., Reference Kolata, Frank, Kaplan and Guensburg2023). Accordingly, the ampullae would be in close proximity to these systems and connected through the radial duct to a single tube foot as well as the WVS ring canal within the circumferential channel (Figs. 1, 15.1, 15.4). Cyclocystoid anatomy is consistent with the way in which the WVS, tube feet, ampullae, and the ambulacral ossicles are arranged in other echinoderms, such as has been proposed for edrioasteroids and other early pentaradiate echinoderms (Paul and Smith, Reference Paul and Smith1984; Smith, Reference Smith1985).
Model of cyclocystoid water vascular system (blue) showing ring of floor plates (light gray), ampulla connected to tube foot through radial duct of floor plates, circumoral ring in circumferential channel of floor plates, tube feet, and hydropore within specialized ramular plate.
If tube feet were housed in the tube foot basins as we propose, then what is the function of the single tubercle present at the center of the tube foot basin in certain cyclocystoids such as Zygocycloides or Apycnodiscus? When present, tubercles vary in size from exceedingly small to prominent knob-like structures. The function of these tubercles is unclear, but the sporadic occurrence within both individuals and among taxa suggests that they were not crucial to the overall activities of the tube feet themselves. In modern echinoderms, ambulacral pores that support tube feet incorporate shelves for the insertion of soft-tissue septa that organize flow of coelomic fluids between a tube foot and its ampulla (Smith, Reference Smith1980). It is possible that the tubercles in cyclocystoid tube foot basins also supported soft-tissue structures associated with tube foot functionality.
The lateral faces of cyclocystoid floor plates exhibit a wide variety of morphological features. In cyclocystoidids such as Cyclocystoides, Apycnodiscus, and Zygocycloides, the aboral portion of the lateral surfaces of the ossicles are in contact along most of their length or touch only distally. In most of these cyclocystoidids the sides of the floor plates have extensive articulation ridges, lateral striae, and a well-developed lateral channel that extends from the proximal to the distal side of the floor plate (Fig. 15.4). Between floor plates, the channel forms a duct leading from the central disk outward to the tube foot basins. This appears to be the duct described by Ewin et al. (Reference Ewin, Reich, Graham and Cournoyer2019) in Perforocycloides nathalieae.
In contrast, the brechincycloidids tend to have lateral articulation surfaces that are relatively small and positioned near the centers of the lateral faces of the floor plates, as in Brechincycloides n. gen. (Fig. 17). Some of the most unusual cyclocystoid floor plates were described by Boczarowski (Reference Boczarowski2001) from Devonian rocks of the Holy Cross Mountains of Poland. Notable among these are Concavocycloides and Apparatocycloides (figs. 21A1, 21A2, and 25P1–P3), in which floor plates possess wing-like structures projecting laterally, suggesting restricted articulation between adjacent plates.
Brechincycloides stanhynei n. gen. n. sp., locality 1, holotype UMMP83165. Specimen photographed under glycerin; portion of aboral surface showing parts of central disk and epispires, relatively small, medial articulation points between floor plates, primary cover plates, and newly formed floor plates.
Aboral interstitial ossicles
These plates are skeletal structures intercalated between floor plates on the aboral surface of some cyclocystoids. They range in size from microscopic ossicles to prominent polygonal plates. At least four different expressions exist for aboral surfaces of adjacent floor plates: (1) floor plates are tightly appressed throughout lateral contact and lack aboral interstitial ossicles, as in Cyclocystoides (Fig. 3.3); (2) floor plates are distally appressed with a proximal gap occupied by elongate aboral interstitial ossicles, as in Nicholsodiscus (Fig. 4); (3) floor plates have polygonal aboral interstitial ossicles positioned distally between lateral faces of the floor plates, as in Zygocycloides (Fig. 6.1); or (4) floor plates are separated by a lateral gap along their entire length that is occupied by microscopic interstitial ossicles, as in Brechincycloides n. gen. (Figs. 7.2).
These aboral interstitial ossicles are not here considered to be part of the cover plate system but rather seem to resemble sesamoid bones in vertebrates, which are more or less autonomous skeletal elements situated among other mesodermal derivatives. As such, the aboral interstitial ossicles could function as “space fillers,” forming a malleable cover during relative flexure between adjacent floor plates. The aboral interstitial ossicles would have protected the musculature and other soft tissues in the spaces between floor plates that would otherwise have been vulnerable to predatory or parasitic attack. Analogies for their function can be found among extant echinoderms such as ophiuroids, in which modified spines and various lateral, dorsal, and ventral arm shields are understood to be defending ambulacral “vertebrae” (fused floor plates) while also assisting in locomotion (Byrne and Hendler, Reference Byrne, Hendler, Burke, Mladenov, Lambert and Parsley1988; Wilkie, Reference Wilkie2016).
Cover plate system
Attached to the distal edge of the floor plates are non-overlapping primary cover plates, followed distally by a series of imbricate, scale-like secondary cover plates that diminish in size distally. The primary cover plates are typically concave proximally, and in some cyclocystoids are sometimes separated from each other by small, accessory plates that are not expressed consistently among cyclocystoids. These plates show individual variation in construction, perhaps in response to damage or as auxiliary space fillers to maintain integrity of the cover plate system. The cover plate system in Brechincycloides n. gen. was capable of sufficient extension to cover the crests of the floor plates (Fig. 9) and appears to have been able to fold downward, sealing off the lower parts of the floor plates. In this way, the tube feet and circumoral ring canal of the WVS (Fig. 15) were protected, much as is seen in other early echinoderms (Paul and Smith, Reference Paul and Smith1984; Smith, Reference Smith1985).
Shape change and extension of the cyclocystoid cover plate system likely was facilitated by imbrication of skeletal elements in sheets of echinoderm tissue, whether in the body wall or otherwise. In modern forms such as cidaroids, such extension is developed in the peristomial membrane to accommodate lantern movements, suggesting adaptive reasons underlying the convergent evolution of such a configuration. In cyclocystoids, the imbrication and substantial number of secondary cover plates would have facilitated extension over the broad tube foot basins.
Large numbers or tiers of cover plates are also found in Cambrian edrioasteroid-like taxa. For example, the primary and secondary cover plate arrangements in Cambraster and Kailidiscus (Zhao et al., Reference Zhao, Sumrall, Parsley and Peng2010) bear strong similarities to those of the cover plate systems in cyclocystoids. The peripheral skirts of Cambraster and Kailidiscus, however, do not. Therefore, reference to the cyclocystoid cover plate system as a “peripheral skirt” is misleading by prompting a comparison between these two very different structures. Although the floor plate ring itself is extremely derived in cyclocystoids, it is conceivable that they inherited their complex cover plate system from a common ancestor with a Cambraster- or Kailidiscus-like early echinoderm.
Central disk
Some authors have interpreted the ramular/interramular complex of the central disk to be the skeletal framework of an ambulacral system with the mouth positioned at the center of the disk (Sieverts-Doreck, Reference Sieverts-Doreck1951; Kesling, Reference Kesling1963, Reference Kesling and Moore1966; Kolata, Reference Kolata1975; Smith and Paul, Reference Smith and Paul1982; Sprinkle et al., Reference Sprinkle, Reich, Lefebvre, Zamora and Rábano2015; Reich et al., Reference Reich, Sprinkle, Lefebvre, Rössner, Zamora and Rahman2017; Kolata et al., Reference Kolata, Frank, Kaplan and Guensburg2023). According to this interpretation, the ring canal of the WVS gave rise to a network of radial water vessels that occupied the channels in the ramules on the oral side of the central disk. In previous work, the ramules often were referred to as radial plates in this context to connote their suggested relationship to rays in other echinoderms. Concomitantly, the numerous small ossicles commonly preserved on the oral surface have been interpreted as ambulacral cover plates. However, Smith and Paul (Reference Smith and Paul1982, p. 602) recognized that “cyclocystoid cover plates [the small ossicles] are very different from cover plates found in edrioasteroids and crinoids and were apparently immobile.” Smith and Paul (Reference Smith and Paul1982, p. 607) further suggested that small food particles were collected by a ciliary epithelium lining the cupules (tube foot basins) and transmitted through the radial ducts to the ramular/interramular complex of the central disk. They left unexplained how the food particles reached a central disk covered by immobile cover plates.
The new material described herein provides several lines of evidence that the rod- and T-shaped cryptogenic ossicles on the oral surfaces of cyclocystoid fossils were not cover plates of any kind: (1) they were not associated with the WVS, which we here argue was contained within the ring of floor plates; (2) cyclocystoid plates with more typical cover plate morphology are found attached to the floor plates, just as in other echinoderms; (3) the cryptogenic ossicles appear not to have been restricted to the ramules (formerly considered “radials” by Smith and Paul, Reference Smith and Paul1982); (4) the immobility of these ossicles, as implied by Smith and Paul (Reference Smith and Paul1982), is not a characteristic of cover plates found in other echinoderms, even in reduced expressions such as those seen in modern crinoids; (5) the cryptogenic ossicles are smaller and much more poorly expressed than other known echinoderm cover plate elements; and (6) the cryptogenic ossicles are embedded within a distinctive layer lying oral to the ramules/interramules—a topology unprecedented among known echinoderm cover plates.
In our view, the suggested immobility of the cryptogenic ossicles implies a fixed protective function that did not include opening of the ossicles to allow tube feet to function. Instead, their morphology and position suggest two possible scenarios. In one scenario, the cryptogenic ossicles may have helped provide support for the ramifying nervous/haemal system associated with the central disk or for internal organs suspended by mesenteries attached to the oral surface of the disk, as seen in modern echinoderms such as echinoids. In an alternative scenario, the cryptogenic ossicles may have been part of the membrane around the mouth on the oral surface of cyclocystoids, allowing them to become taphonomically appressed to the oral surface of the ramular and interramular series. The latter situation would, in turn, explain the observations that the areal distribution of cryptogenic ossicles was not restricted to the ramular and interramular series but only loosely associated with those plate systems. In addition, the fact that cryptogenic ossicles are sometimes found preserved within epispires would make little sense if they were part of an ambulacral system in the central disk.
Smith and Paul (Reference Smith and Paul1982, fig. 9c) assumed that a thin coelomic cavity was positioned between the ramular/interramular complex and annular ossicles. The aboral surface of Brechincycloides stanhynei n. gen. n. sp. consists of a single layer of ramules and interramules with no evidence of a skeletally enclosed body cavity. The aboral surface is covered with epispires (“sutural pores” of Smith and Paul, Reference Smith and Paul1982) that are not typically an integral part of an echinoderm ambulacrum. These observations suggest that the complex of ramules and interramules did not contain an ambulacral system and that there was no WVS associated with the central disk. Moreover, the body cavity was likely positioned between the lower surface of the ramular/interramular complex and a second integument, non- or weakly calcified, positioned below the radial ducts of the floor plates in a manner like that proposed by Nichols (Reference Nichols1969, fig. 18) and shown in Figures 2 and 15 herein. Most importantly, comparisons of skeletal morphology with that of other echinoderms suggest that the cyclocystoid WVS was likely housed in the ring of floor plates as first proposed by Nichols (Reference Nichols1969, Reference Nichols1972).
Attached to the aboral surface of the ramules and interramules are annular ossicles ringing a pore aligned with the opening of an epispire. In the cyclocystoidids, including Apycnodiscus, Cyclocystoides, and Zygocycloides, the annular ossicles are taphonomically appressed to and take the shape of shallow, ovate, or polygonal depressions that surround the epispires on the aboral surfaces of the ramules and interramules (Figs. 3, 4, 6.1). Typically, the annular ossicles are largest at the disk center adjacent to the central aboral ramule (Fig. 6.1). The ossicles decrease in size distally, are laterally in contact with each other, cover most of the aboral surface of the ramular/interramular complex, and articulate with the crescentic facets on the proximal edges of the floor plates (Fig. 3.3). In some specimens, the annular ossicles are irregular in form, suggesting that they could undergo repositioning during life (Fig. 3.2).
In comparison, brechincycloidids such as Brechincycloides n. gen. possess relatively small, subcircular to oval, rigid, sleeve-like inserts lining the epispires on the aboral surface of the ramules and interramules (Figs. 6.2, 6.3). The sleeve-like inserts commonly are not laterally in contact within the central parts of the aboral surface but may be so near the floor plates. The overall size, shape, and position of the epispires in Brechincycloides n. gen. resemble the sutural pores in the cornute stylophoran Phyllocystis crassimarginata Thoral, Reference Thoral1935, and Nevadaecystis americana Ubaghs, Reference Ubaghs1963. Some pores are bilobate, resembling diplopores in certain blastozoan taxa such as Eumorphocystis (see Parsley, Reference Parsley and Sprinkle1982), and occur within or are shared by adjacent thecal plates (Fig. 11). Epispires of Brechincycloides n. gen. are surrounded by a ring of individual, sleeve-like plates that stand above the aboral surface, thus differing structurally from the raised rims of epispires in eocrinoids such as Akadocrinus jani Prokop, Reference Prokop1962 or Gogia parsleyi Zamora, Gozalo, and Liñán, Reference Zamora, Gozalo and Liñán2009 (Zamora et al., Reference Zamora, Gozalo and Liñán2009, fig. 8). It is likely that the relatively thin, sleeve-like ossicles in Brechincycloides n. gen. are homologous to the annular ossicles in the cyclocystidids such as Cyclocystoides. In two apparent gerontic specimens of Brechincycloides n. gen. (paratypes UMMP83158 and UMMP83169), several epispires with sleeve-like ossicles are encapsulated within and restricted to the proximal shelf of the floor plates (Figs. 12, 14). While individual epispires are known to share boundaries with floor plates and extraxial plates in primitive echinoderms such as Stromatocystites reduncus Smith and Jell (Reference Smith and Jell1990, fig. 4) and Vyscystis ubaghsi Fatka and Kordule, Reference Fatka and Kordule1990 (as shown in Nohejlová et al., Reference Nohejlová, Nardin, Fatka, Kašička and Szabad2019, fig. 3b, 3d), total encapsulation within the floor plates of Brechincycloides n. gen. is unique among known cyclocystoids.
At the center of the network of ramules and interramules is a central aboral ramule surrounding a medial pore (Fig. 6). Four or five small, wedge-shaped plates form a small pyramid that can be seen in the central pore on the aboral surface (Fig. 6.3). The overall structure is similar in form to the periproctal cones found in other echinoderm groups. Brechincycloides n. gen. is unique in having a single central aboral ramule rather than multiple ramules surrounding the periproct.
Three specimens of Brechincycloides n. gen. possess a unique terminal ramule that in aboral view is relatively large, convex at its center, and differentiated from surrounding ramules (Fig. 10). A single pore in this ramule, 80 μm in diameter, is visible in two specimens. The consistent occurrence of this single plate at the end of a single ramular series suggests that it may have had a specific function, most likely to contain the hydropore or hydropore/gonopore. Boczarowski (Reference Boczarowski2001, fig. 23.AG1–AG3) illustrated and briefly described a similar single isolated central disk plate in ?Concavocycloides givetiensis Boczarowski, Reference Boczarowski2001, that he suggested supported a possible hydropore. The observation in Brechincycloides n. gen. of a specialized plate in the perforate extraxial region pierced by these standard echinoderm apertures constitutes a major advance; no previous cyclocystoid study has even attempted to propose their locations. In pentaradial echinoderms, these pores occur within the CD interray between the axes of pentaradial construction. Indeed, specimen UMMP83157 seems to show the expected interray position for the specialized terminal ramule (Fig. 13), assuming that the equal-spaced narrow floor plates marking the pentaradial symmetry also mark the rays.
Pentaradial symmetry
The Brechin cyclocystoids are preserved in a wide range of sizes that reveal information about their overall morphogenesis. The availability of pertinent data is particularly notable in Brechincycloides stanhynei n. gen. n. sp. (Table 2), whose fossils have thecal diameters ranging from 6.5 mm for a floor plate ring of 20 ossicles (UMMP83170) to 36 mm for a floor plate ring of 40 ossicles (UMMP83161). These specimens illustrate that as the theca increased in size, new floor plates were added to the ring in a distinct pentaradial pattern, as demonstrated in two relatively small specimens (UMMP83167 and UMMP 83168). Incipient ossicles developed as small triangular structures at the distal margin between mature floor plates (Figs. 17, 18). Newly generated ossicles possessed a single tube foot basin. A second tube foot basin gradually developed as the ossicle grew to fill the space that otherwise would have appeared between adjacent floor plates as the circumference increased. In Brechincycloides n. gen., the regularity of the growth zones becomes less apparent in gerontic individuals. In some specimens, this may be due to old injuries along the margins of the theca that were regenerated with numerous new marginal floor plates, resulting in the irregular thecal outlines of developmentally older individuals (Figs. 11–13).
Brechincycloides stanhynei n. gen. n. sp., locality 1; specimens photographed under glycerin. (1) Paratype UMMP83168, aboral surface, blue arrows point to incipient floor plates and probable axes (rays) of pentaradial symmetry, oldest floor plates where curved arrows converge; (2) paratype UMMP83167, aboral surface, arrows point to floor plates including incipient, early, and intermediate stages of growth.
As Mooi and David (Reference Mooi and David1997, Reference Mooi and David2008) and Mooi et al. (Reference Mooi, David and Wray2005) have demonstrated, all echinoderms express growth zones centered on the perradius of the axial series, which in nearly every case is represented as a biseries of ambulacral plates. The oldest plates in the series are those proximal to the mouth and the youngest at the distal end of the perradius, forming an age gradient of these plates. The gradient is a consequence of the way in which new plates are added to the series in an alternating fashion between the a and b columns of the biseries (see also Jackson, Reference Jackson1912). This pattern, known as the ocular plate rule (OPR), operates in every echinoderm in which the pattern has been studied, suggesting that it is a hallmark of the growth of echinoderm rays. Therefore, the ability to recognize this pattern in enigmatic groups such as the cyclocystoids can be helpful in establishing the main aspects of their body plan.
The number of floor plates within the five sectors of the floor plate ring generally increased relative to thecal diameter (Table 2). The expression of the OPR in these sectors seems to serve as a strong indication that they comprise distinct growth zones (sensu Mooi and David, Reference Mooi and David1997, and Mooi et al., Reference Mooi, David and Wray2005) and that there are five such zones (Fig. 18).
In any given specimen, the clearest evidence of pentaradial symmetry depends largely on the preservation of ossicles at incipient or intermediate growth stages at the time of death. In large, gerontic specimens, pentaradiality can be less obvious (Figs. 11, 12) if new floor plates were not commonly added in late stages of growth. Functionality of the floor plate ring in cyclocystoids likely depended on uniformity in ossicle size, based on comparisons with other echinoderms with strongly developed peripheral rings of plates, such as Cambraster and certain asteroids. Newly formed floor plates would therefore quickly attain and then maintain a given size throughout the perimeter of the animal, in turn implying that plate addition events would become rarer as the animal aged.
Pentaradial symmetry also characterizes the ring of floor plates in Cyclocystoides (Fig. 3.3) and Zygocycloides (Fig. 5.2). In contrast, the ramular/interramular complex of the aboral central disk in cyclocystoids displays varied symmetries, including fourfold (Apycnodiscus, Polytryphocycloides), fivefold (Zygocycloides, Sievertsia), and sixfold (Cyclocystoides). These symmetries are not consistent with the nearly universal expression of five growth zones throughout the phylum. Blastozoans such as certain eocrinoids, carpoids, and cystoids are noted here as exceptions, but it is also clear that the stemward forms among these groups possessed pentaradial symmetry and that departures from pentaradiality were secondary.
Skeletal homologies of cyclocystoids
In cyclocystoids, the presence of epispires within the aboral part of the central disk and symmetries expressed in the ramular/interramular complex strongly support the suggestion that the central disk was extraxial body wall (specifically, perforate extraxial), as predicted by the extraxial–axial theory (EAT) (Mooi et al., Reference Mooi, David, Marchand, David, Guille, Féral and Roux1994, Reference Mooi, David and Wray2005; David and Mooi, Reference David and Mooi1996, Reference David, Mooi, Mooi and Telford1998, Reference David and Mooi1999; Mooi and David, Reference Mooi and David1997, Reference Mooi and David1998, Reference Mooi and David2008). Epispires are occasionally encapsulated by extensions from the floor plates in gerontic specimens of Brechincycloides n. gen. This hypermorphic expression, which is clearly a product of growth of the floor plates towards the center of the central disk, is insufficient to undermine the overwhelming evidence that epispires in cyclocystoids characterize the central disk of cyclocystoids as extraxial region. This region also contains a centrally positioned cone of plates, which we interpret as the site of the periproct, and a specialized terminal ramule that is most parsimoniously inferred to be the hydropore/gonopore. The placement of these openings is consistent with the determination that the central disk is perforate extraxial body wall.
Moreover, the position of the specialized hydropore/gonopore plate is consistent with the interradial position of these apertures in other echinoderms, namely in the CD interray. This in turn suggests that the hydropore-/gonopore-bearing ramule can be used to homologize the rays of other echinoderms with those of cyclocystoids, as marked by the growth zones described above. Cyclocystoids apparently lacked the imperforate extraxial region that, in Cambrian forms such as Stromatocystites and Walcottidiscus, closed the body wall on the aboral surface opposite the mouth and functioned as an attachment surface. With the atrophy of this surface, the perforate extraxial region became the sole source of body wall for the central disk.
Based on our identification of the aboral surface of the central disk as perforate extraxial region, this part of a cyclocystoid therefore becomes the expected location for extraxial structures. Furthermore, the pentaradial symmetry of the ring of floor plates and the network of internal canals, tube foot basins, cover plates, and radial ducts is consistent with an ambulacral (that is, axial) system. The level of complexity in the anatomy of cyclocystoid floor plates (“marginals”) is consistent with the complexity of ambulacral plates found in other echinoderms. This complexity includes provision for the housing of all the elements of the WVS, as well as musculature between articulation surfaces of the floor plates. Ambulacrals of other echinoderms such as asteroids typically have well-developed musculature between the ossicles in any given series (Mooi and David, Reference Mooi and David2000).
Accordingly, the floor plates of cyclocystoids are axial, and the points of insertion of new plates into the ring likely mark the positions of the axes (rays) of pentaradial construction in all cyclocystoids. In this case, the perradius of the ambulacral biseries is represented by the proximal edges of the floor plates, which have opened (‘unzipped’) along the perradial suture to make a ring (Fig. 19). This structure is what would result in the case of asteroids in which the buccal slit (sensu Mooi and David, Reference Mooi and David2000) was continued all the way to the tip of the arm, a construct also suggested to have occurred in the concentricycloids such as Xyloplax (Janies and Mooi, Reference Janies, Mooi, Candia Carnevali and Bonasoro1998; Mooi et al., Reference Mooi, Rowe, David, Mooi and Telford1998). It is important to note that the unzipping would start shortly after metamorphosis with an incipient notch just internal (i.e., opposite) to each point along the outside of the ring canal at which each radial canal joins it. This notch deepens into the perradius, thereby also splitting the radial canal. The ring plus the unzipping radial canal form a bigger ring that in Xyloplax is strongly expressed as a single structure because the division between ring and radial canal of the WVS is not apparent. In this manner, in both Xyloplax and in cyclocystoids, the WVS would be entirely confined to the marginal ring of ossicles identified as ambulacrals (or floor plates). We emphasize that the complete unzipping of a buccal slit in forms ancestral to Xyloplax, which is a crownward asteroid with no affinities to cyclocystoids (Linchangco et al., Reference Linchangco, Foltz, Reid, Williams and Nodzak2017), is not homologous in the two groups.
Model for derivation of cyclocystoid body plan. Large, bright red arrows indicate directionality from stage to stage, each of which accompanied by list of major hypothetical changes. Note that we make no claim that there will be fossils found representing these stages — these merely indicate hypothetical but necessary innovations that may have occurred very rapidly through highly altered or truncated ontogenies; (1–4) depicted in oblique perspective with oral surface upwards, (5) with aboral surface upwards. (1) Presumptive plesiomorphic morphology of cyclocystoid outgroup as exemplified by generalized early pentaradiate taxon; (2) stage at which “unzipping” along perradial suture of each ambulacrum begins; cover plate system (attached along abradial edges of floor plates) also opening outward, accompanied by contraction of aboral perforate extraxial region as axial regions push out peripherally; (3) stage in which “unzipping” process results in completely separated, now monoserial columns of ambulacra still bearing articulated but now distally (peripherally) positioned cover plate system; coelom closed on oral surface by circumoral membrane; papulae almost completely confined to constricted perforate extraxial region composing aboral surface; (4) presumptive plesiomorphic condition of cyclocystoids in which tube feet no longer shared by adjacent floor plates, but mounted wholly on single plate (subsequent evolution within the clade involves addition of tube feet to each floor plate); periproct in center of aboral ramular and interramular system of perforate extraxial region now contained within ring of floor plates; papulae entirely aboral; by this time, the animal has adopted mouth-down posture typical of all cyclocystoids, shown here with mouth upward to facilitate comparisons of changes in each stage; (5) same stage as depicted in (4), but in natural orientation with aboral surface upwards.
The mouth of cyclocystoids continues to be problematic in that it has not been positively identified in any cyclocystoid in the context of any previously published model, except that by Nichols (Reference Nichols1972, text-fig. 10). In that reconstruction, the mouth existed as a small opening in a membrane on the oral surface of the animal. The oral membrane has yet to be preserved in a way sufficient for identification in presently available fossils, although some of the Brechincycloides n. gen. material shows hints of an organic layer just below (internal to) the extraxial body wall constructed of the ramule/interramule complex. As such, the oral membrane would have been attached to the proximal rims of the floor plates, and therefore within the axial region as in other echinoderms.
The ‘unzipping’ effect described above is somewhat like the situation in living Xyloplax, but there are key differences. We emphasize that although there are similarities in general construction between concentricycloids and cyclocystoids in that they are both circular animals with a peripheral axial region enclosing a central, aboral region of extraxial body wall, we do not mean to suggest that these similarities are homologous, because cyclocystoids and concentricycloids are clearly unrelated (Linchangco et al., Reference Linchangco, Foltz, Reid, Williams and Nodzak2017). Xyloplax follows the OPR much more obviously than cyclocystoids (Mooi et al., Reference Mooi, Rowe, David, Mooi and Telford1998). In Xyloplax, each ambulacral plate (floor plate) has a single tube foot, and there is a readily identifiable, uniquely specialized terminal (or ocular) stereom plate that places Xyloplax within the asterozoan/echinozoan clade (Janies and Mooi, Reference Janies, Mooi, Candia Carnevali and Bonasoro1998). Early echinoderms lacked a calcified terminal ossicle (Mooi and David, Reference Mooi and David1997), and we find no evidence for this in cyclocystoids either.
However, other comparisons of Xyloplax with cyclocystoids can provide instructive analogies besides the one cited above concerning the position of the mouth. Such analogies help us understand features that have been selected for independently in these two otherwise unrelated forms. Interestingly, Xyloplax has convergently evolved a palisade of flattened spines to protect the downward-facing ring of tube feet, much as the cover plate system would have done in cyclocystoids. However, in Xyloplax, these spines are mounted on a series of adambulacrals in nearly one-to-one relationship with the ambulacrals (Mooi et al., Reference Mooi, Rowe, David, Mooi and Telford1998). There is no anatomy remotely like this in any cyclocystoid. In addition, the oralmost ‘blade’ that extends from the mouth angle ossicle in Xyloplax has no equivalent in cyclocystoids, and if there is a cyclocystoid homologue of the mouth angle ossicle in the form of the first ambulacral, it does not surround the peristomial membrane as do the mouth angle ossicles in Xyloplax (Mooi et al., Reference Mooi, Rowe, David, Mooi and Telford1998). Unlike cyclocystoids, Xyloplax does not express a system of channels internal to the aboral plates, which also are not specialized into ramules and interramules. Although the systems of aboral plates of Xyloplax and cyclocystoids are both extraxial, epispires are not present in the former.
The existence of tube feet in tube foot basins of preserved cyclocystoid skeletons can only be inferred by position and homology with floor plates of other echinoderms. Importantly, our interpretation strongly suggests that cyclocystoids eventually broke the ‘one tube foot per plate rule’ exemplified by other early pentaradiate echinoderms and by nearly all extant forms (Mooi et al., Reference Mooi, David and Wray2005), even those with morphologies as divergent as those of Xyloplax (Mooi and David, Reference Mooi and David1998). We do not, at present, have enough ontogenetic information for cyclocystoids to explain development of their unique arrangements and numbers of tube foot basins.
We note that breaking of the ‘one tube foot per plate rule’ among cyclocystoids does not undermine our determination that the marginal ring is made up of floor plates supporting tube foot basins. One reason for this is that departure from the ‘rule’ has precedents among other echinoderms. Irregular echinoids such as clypeasteroids are characterized by the expression of multiple tube feet in each floor plate (Mooi, Reference Mooi1990). Another reason is that the plesiomorphic expression of tube foot basins in cyclocystoids is most parsimoniously considered to be one per floor plate. Arguably early cyclocystoids such as Moroccodiscus express many floor plates in which there is only a single tube foot basin, suggesting that this state is only slightly apomorphic relative to the plesiomorphic condition exemplified by other early, non-cyclocystoid echinoderms.
Our observations strongly support not only the idea that the marginal ring consists of floor plates, but also the concept that the so-called peripheral skirt of Smith and Paul (Reference Smith and Paul1982) is actually an accompanying set of cover plates mounted on the edges of those floor plates. We appreciate that this is a radical interpretation of cyclocystoid anatomy, but we are compelled to accept this in view of its overwhelming congruences with anatomies revealed by the new material, its avoidance of hitherto unexplained inconsistencies in previous models, its consistencies with patterns of growth zones in other echinoderms, and the EAT. Nevertheless, we recognize striking similarities between the features of cyclocystoids and certain isorophid edrioasteroids, in which a peripheral skirt aided in gripping firm substrates in a limpet-like fashion. For example, the isorophid Savagella expresses laterally abutting peripheral rim plates, forming orthogonal boundaries superficially like those between floor plates of cyclocystoids (Guensburg, Reference Guensburg1988). This Savagella comparison would be visually even more convincing for cyclocystoid specimens in which the cover plate system beyond the floor plates is laid out against the substrate if it were not for the fact that the peripheral rim plates of Savagella and related forms are not homologous with floor plates of cyclocystoids. Peripheral rim plates in isorophids do not support the WVS because it is already present in the more or less conventional ray system composed of floor plates.
Along with other evidence, application of the EAT continues to support the interpretation that the plates distal to the floor plates in cyclocystoids are cover plates, not a peripheral skirt. The half ambulacrum represented by a floor plate ring formed from the axial region in the manner described above for cyclocystoids would be expected to contact the full complement of cover plates just as it actually does. That is to say, if the floor plate ring in cyclocystoids is an ‘unzipped’ biserial column of floor plates like those seen in edrioasteroids and other early pentaradial taxa (Fig. 19), then the reinterpretation espoused herein places all cyclocystoid ossicle topologies fully in line with broader echinoderm models.
Most importantly, anatomical considerations strongly indicate the existence of a coelomic cavity between the oral surface and the substrate to which flattened, early edrioasteroid-like echinoderms were attached (Smith, Reference Smith1985, text-fig. 1). In such forms, an imperforate extraxial body region closed this cavity, just above the substrate, extending from the proximal edge of the peripheral skirt across the aboral surface of the animal. This topology is not conceivable in our model of cyclocystoids because the position of the axial floor plates makes it impossible for that configuration to close the coelom with a similar sheet of extraxial body wall when the remainder of the body wall (in this case, perforate extraxial) is on the other, aboral surface of the animal.
Moreover, cyclocystoid floor plates express far more complex anatomies than the relatively simple, squared-off proximal circlet of Savagella or any other isorophid. If the axial cover plate system were homologous with the peripheral skirt of edrioasteroids, the presence of extraxial plating both oral and aboral to the floor plates would be completely unique among the echinoderms, representing extraxial aboral body wall both proximal and distal to the axial floor plates. The peripheral skirt of an edrioasteroid-like form is a continuation of extraxial body wall down to the surface to which it is attached. In sharp contrast, the taphonomic posture of the sheet of cover plates in specimens of Brechincycloides n. gen. demonstrates the ability of this marginal complex to flex downward, covering the tube foot basins in a facultative protective covering posture, a behavior impossible for the morphologies found among isorophids (Guensburg, Reference Guensburg1988).
Life mode
The new Brechin cyclocystoid specimens reveal a gross anatomy supporting a living orientation in which the tube foot basins faced the substrate (Figs. 1, 2, 15, 19.5). A related revelation bearing on this is that the cyclocystoid WVS was largely housed in the ring of floor plates in a manner like that first described by Nichols (Reference Nichols1969, Reference Nichols1972). Accordingly, the tube foot basins housed tube feet that allowed the animal to move about, feeding with the mouth facing the substrate. The epispires likely supported papulae that served in gas exchange and/or metabolic waste disposal.
Support for this orientation is particularly noteworthy in the cyclocystoid floor plates reported by Reich and Kutscher (Reference Reich, Kutscher, Harris, Böttger, Walker and Lesser2010, fig. 3) from the Silurian Hemse Group, Ludlow (Gorstian), at Tanglings, Gotland, Sweden. They illustrated floor plates of a previously unreported cyclocystoid with a prominent cusp on the aboral surface of each floor plate. If the tube foot basins were facing away from the substrate, it would be exceedingly difficult for the animal to move about because of the resistance created by the downward-projecting cusps in the ring of floor plates. Conversely, if the tube foot basins faced the substrate, as we suggest, the cusps would point upward in what would be a more optimal defensive position analogous to that seen in echinoid or asteroid spines. Our model provides conjecture as to the feeding mode of cyclocystoids (see below). If concentricycloids provide a general model, microphagy along the sediment–water interface seems a possibility.
We envision a life mode orientation like that shown in Figures 1, 2, 15, and 19.5. The tube feet were likely used for locomotion and on firm substrates were able to grip and anchor the animal in place. Notably, all 10 of the B. stanhynei n. gen. n. sp. specimens described in this report were collected from the same hardground surface with all oral surfaces facing downward. The same orientation was noted by Glass et al. (Reference Glass, Ausich and Copper2003) for the cyclocystoid Nicholsodiscus anticostiensis, preserved on a limestone hardground surface in the Upper Ordovician Vauréal Formation, Anticosti Island, Quebec, Canada. In B. stanhynei n. gen. n. sp., the hydropore/gonopore was positioned on the aboral surface adjacent to the floor plates, with the periproct at the center of the disk. The primary and secondary cover plates projected downward, apparently to protect the tube feet and oral membrane.
Conclusions
Enigmatic fossils whose nature has long been debated, the Cyclocystoidea are reexamined in light of new fossil material that greatly expands our understanding of anatomical details. These details reveal that evidence for a water vascular system (WVS) in the central disk is weak to non-existent. Channels on the lower surfaces of the ramular/interramular complex did not house elements of the WVS. Instead, these channels likely contained nervous and/or haemal systems that communicated with a nerve ring through the facet canals, which, like the ramular channels, would topologically have been situated to open inside the coelom.
The conventional understanding of the central disk elements as ‘radials’ and ‘interradials’ does not conform to empirically derived principles observed in axial regions of all other echinoderms. Moreover, the interpretation of a subset of central disk ossicles as ambulacrals in a system of rays leaves open questions concerning the remarkable ‘marginals’ (floor plates), offering them no recognizable homology with elements of any other echinoderm group. The ring of large, anatomically complex floor plates (marginals of other authors) is here revealed to be constructed of axial, ambulacral elements that are modified yet recognizable floor plates consistent with their function of supporting the WVS. This system includes the tube feet, borne by tube foot basins that, as Nichols (Reference Nichols1972) recognized, would otherwise have no plausible function (setting aside speculations of Smith and Paul, Reference Smith and Paul1982, that these were somehow involved in ciliary feeding).
This realization, supported by abundant new observations of well-preserved specimens described herein, also presents cyclocystoids as echinoderms understandable through application of the EAT. In this framing, a perforate extraxial body wall region, represented by the ramular/interramular layer, was present as the aboral surface, which faced upwards to expose the papulae, mounted on the prominent epispires, to the water column. This layer, rather than containing a thin coelom, is an anatomical and functional unit that, as cyclocystoid fossils show, could not contain a body cavity.
This, in turn, leaves the question of the position of the mouth, which we posit was situated in a membrane extending to the lower proximal edges of the floor plates, enclosing the coelom on the oral surface. The periproct was opposite the mouth, opening upward in the center of the perforate extraxial body wall on the aboral surface. For the first time, we present evidence for the existence of the hydropore/gonopore in a specialized ramule on this surface, further supporting the notion that the central disk is a perforate extraxial region in accordance with the Extraxial–Axial Theory (EAT). There is also a possibility that the cryptogenic ossicles (the “cover plates” of Smith and Paul, Reference Smith and Paul1982), seemingly appressed to the interior surfaces of the ramules and interramules, were instead part of the oral membrane. Ossicles in oral membranes are typical of other echinoderm groups such as echinoids.
This reconstruction demystifies the animals while continuing to leave open the question of the affinities of the cyclocystoids. Lacking brachioles, they cannot be considered related to the blastozoans, and the absence of arms, stem, and imperforate extraxial body wall makes it unlikely that they are exclusively related to crinoids. However, the Cyclocystoidea are derived, with many unique apomorphies that continue to render them difficult to place among other known Paleozoic taxa. The absence of an imperforate extraxial region that could be used for attachment strongly suggests that cyclocystoids were not attached. Rather, they are best pictured as dynamic animals with full motility achieved through use of their enlarged tube feet and flexure in the floor plate ring achieved by the well-developed musculature between the plates.
Therefore, cyclocystoids can be considered highly modified early pentaradiate forms that adopted a vagile lifestyle, with many of their unconventional anatomical features representing novel adaptations to this lifestyle. Specifically, the ancestors of cyclocystoids were likely similar to forms such as Stromatocystites or Kailidiscus that lived as sessile echinoderms that are conventionally interpreted to have the mouth and axial region upward so that tube feet could reach into the water column. Such an ancestor would have evolutionarily detached and ‘flipped over’ so that the mouth and tube feet faced the substrate to take advantage of changing environments with abundant benthic food sources (Fig. 19). Lacking a need for the imperforate extraxial attachment surface, this region would have been lost so that only the perforate extraxial region remained—an evolutionary change seen in many other echinoderm taxa, including stylophorans and the asterozoan + echinozoan clade. ‘Unzipping’ the rays along the perradial sutures allowed the floor plates of cyclocystoids to reposition into a distal ring, complete with cover plate systems to protect the tube feet, while leaving the mouth centered within a membrane attached to the proximal edges of the peripherally placed floor plates. Cyclocystoids would therefore represent yet another way that a specialized group of early echinoderms literally walked away from a sessile habit.
Acknowledgments
We thank P. Jell, M. Reich, and an unidentified reviewer for their thorough comments on the manuscript and for their helpful suggestions, many of which compelled us to revise and strengthen some of our observations and conclusions. We also thank editors B. Lefebvre and S. Zamora for their guidance in clarifying parts of the manuscript and A. Kaplan for editing an initial version of the paper. A. Scheer is acknowledged for providing the paratype specimen of Cyclocystoides cf. C. scammaphoris (ISGS-PAL24-1) used in Figure 2.3. J. Bauer, University of Michigan Museum of Paleontology (UMMP), provided curatorial assistance. RM was supported by his NSF grant, DEB 2036298.
Competing interests
The authors declare no competing interests.
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