An edrioasteroid from the Silurian Herefordshire Lagerstätte of England reveals the nature of the water vascular system in an extinct echinoderm

Abstract

Echinoderms are unique in having a water vascular system with tube feet, which perform a variety of functions in living forms. Here, we report the first example of preserved tube feet in an extinct group of echinoderms. The material, from the Silurian Herefordshire Lagerstätte, UK, is assigned to a new genus and species of rhenopyrgid edrioasteroid, Heropyrgus disterminus. The tube feet attach to the inner surface of compound interradial plates and form two sets, an upper and a lower, an arrangement never reported previously in an extant or extinct echinoderm. Cover plates are absent and floor plates are separated creating a large permanent entrance to the interior of the oral area. The tube feet may have captured food particles that entered the oral area and/or enhanced respiration. The pentameral symmetry of the oral surface transitions to eight columns in which the plates are vertically offset resulting in a spiral appearance. This change in symmetry may reflect flexibility in the evolutionary development of the axial and extraxial zones in early echinoderm evolution.

1. Introduction

The water vascular system is a defining feature of echinoderms which, via the tube feet, performs a diversity of functions in living forms including feeding, locomotion and respiration. Here, we present evidence of tube feet in an edrioasteroid, representing one of the most basal groups of pentaradial echinoderms [1,2]. Edrioasteroids appeared in the Cambrian and persisted until the Permian [3], occurring worldwide, mostly in shallow-water settings. They are characterized by a disc-like to globular theca with five ambulacra and do not possess erect plated feeding appendages (i.e. arms or brachioles). Rare examples, such as the rhenopyrgids, have an elongate conical peduncle and lived on soft substrates [4]. Here, we report a new genus and species, Heropyrgus disterminus, from the lower Silurian Wenlock Series Herefordshire Lagerstätte (approx. 430 Ma) of England [5,6].

Fossil echinoderms rarely preserve soft tissues, and the only other records of tube foot preservation are confined to representatives of the extant classes, which has limited our understanding of the evolutionary history of the water vascular system. These include asteroids from the Upper Ordovician of Kentucky [7] and of Shropshire, England [8,9], as well as ophiuroids, a crinoid, and a holothurian from the Lower Devonian Hunsrück Slate of Germany [10–12]. The only other echinoderm described from the Herefordshire Lagerstätte to date, the asteroid Bdellacoma sp., also revealed evidence of tube feet [13]. Heropyrgus disterminus gen. et sp. nov., like the other exceptionally preserved fossils from Herefordshire ([14] and references therein), is preserved as three-dimensional calcite in-fills in nodules in a volcaniclastic ash [15]. Select specimens were studied through serial grinding and computer reconstruction [16–18].

2. Material and methods

Three specimens (figure 1a–h,k–s) were chosen from approximately 20 available examples and serially ground at 30 µm intervals (20 µm for the coriaceous sac of OUMNH C.36003). Each surface was captured digitally and the resulting tomographic datasets were reconstructed with the SPIERS software suite and studied as three-dimensional virtual fossils [16,18]. This destructive approach is necessary as the calcite void fill that preserves fossils from the Herefordshire Lagerstätte is very similar in composition to the host rock [15], and the density contrast is insufficient to allow X-ray-based imaging techniques to yield the high fidelity results required. Interpretation of the virtual fossils was facilitated on screen by variable magnification, rotation, virtual dissection, and stereoscopic viewing. Specimens were also examined using screen-captured images and three-dimensional prints. Full details of the locality and datasets from serial-grinding tomography of the specimens are housed in the Oxford University Museum of Natural History (OUMNH). Serial-grinding datasets and triangle-mesh models in VAXML/STL format are also available from the Dryad Digital Repository: http://dx.doi.org/10.5061/dryad.7005f [19]. The tube feet of a modern asteroid in the collections of the Yale Peabody Museum of Natural History (YPM) were studied for comparative purposes.

Figure 1.

Heropyrgus disterminus (a–h,k–s) and other echinoderms (i,j). (a,c–g,i,k–q,s) ‘Virtual’ reconstructions (a,c–f,k,n,o,q,s are stereo-pairs), (b,h,r) specimen in rock, (j) photograph. (a) OUMNH C.36003 lateral view showing division of theca into oral surface, collar, peduncle and coriaceous sac. (b) OUMNH C.36003, section through the oral surface, collar and proximal peduncle showing crystalline calcite filling the void. (c) OUMNH C.36043, oral surface. (d) OUMNH C.36044, oral surface. (e) OUMNH C.36043, oral surface showing tentacle-like structures and compound interradial plate CD (other interradial plates removed). (f) OUMNH C.36043, oral surface in oblique view showing compound interradial plate CD and associated tentacle-like structures (all other features removed). (g) OUMNH C.36043, oral view with compound interradial plates removed to show 2–1–2 symmetry revealed by the larger angle in ambulacrum A. (h) OUMNH C.36043, section through oral area showing tentacle-like structures interpreted as tube feet. (i) OUMNH C.29573, tube feet in the fossil asteroid Bdellacoma sp. from the Silurian of Herefordshire (from [13]). (j) YPM IZ 008378.EC, tube feet in the extant paxillosid asteroid Luidia barbadensis. (k) OUMNH C.36043, lateral view facing interradial plate EA showing suboral constriction, collar and proximal part of peduncle. (l) OUMNH C.36043, lateral view of oral surface showing thread-like structure attached to compound interradial plate AB. (m) OUMNH C.36043, lateral view of oral surface showing thread-like structure attached to compound interradial plate CD. (n) OUMNH C.36043, lateral view showing junction of collar and peduncle, and the spiral arrangement of the plates on the latter. (o) OUMNH C.36043, compound interradial plate BC. (p) OUMNH C.36043, lateral view showing hydropore/gonopore. (q) OUMNH C.36003, coriaceous sac showing spine-like plates and central depression. (r) OUMNH C.36003, coriaceous sac in oblique section showing evidence of lateral projections. (s) OUMNH C.36044, base of collar showing two ridges on a single collar plate. Abbreviations: AB–EA, interradial plates; co, collar; cs, coriaceous sac; fp, floor plates; h/g, hydropore/gonopore; op, oral plate; os, oral surface; pe, peduncle; pr, periproct; rc, ridges on collar plate; ri, ridges on inner surface of floor plates; sc, suboral constriction; tf, tube feet; th, thread-like structure; ts, tentacle-like structures interpreted as tube feet. Scale bars: (a) is 2 mm; (b,l–n,p,s) are 1 mm; (c–h,o,q,r) are 0.5 mm; (i,j) are 5 mm.

3. Systematic palaeontology

Phylum Echinodermata [20] (ex [21])

Class Edrioasteroidea [22]

Order Edrioasterida [23]

Suborder Edrioblastoidina [24]

Family Rhenopyrgidae [25]

Genus Heropyrgus gen. nov.

Type species: Heropyrgus disterminus sp. nov.

Other species: None.

(a). Etymology

Herefordshire, for the locality where the taxon occurs; pyrgos (Greek) = tower, referring to the long erect peduncle. Disterminus (Latin) = separated, referring to the permanent gape between the floor plates.

(b). Diagnosis of genus (monotypic) and species

Rhenopyrgid lacking cover plates; oral plates fringed by nine floor plates with narrow ridges on their inner surface; floor plates separated by permanent gape; oral and floor plates fused into compound interradial plates; constricted elongate zone of imbricate plates between oral surface and suboral collar; long peduncle composed of numerous imbricate plates organized into eight columns.

(c). Material

Holotype: OUMNH C.36043 (figure 1c,e–h,k–p). Paratypes: OUMNH C.36044 (figure 1d,s), OUMNH C.36003 (figure 1a,b,q,r). Other (unground) specimens: OUMNH C.36045–36058, C.29683, C.29685, C.29687, C.29688.

(d). Locality and horizon

Herefordshire, England, UK; Wenlock Series, Silurian.

(e). Description

OUMNH C.36003 (figure 1a) reveals the complete morphology of Heropyrgus disterminus. The theca is 27 mm long, and the oral surface ranges from 2.4 mm (OUMNH C.36044) to 4.2 mm (OUMNH C.36043) in maximum width. The oral surface sits atop a suboral constriction, which is irregularly plated and transitions into the collar. There is a pronounced gutter where the collar inserts into the plated peduncle, which terminates distally in a holdfast structure, the coriaceous sac.

The oral surface is highly domed and comprises five large compound interradial plates (figure 1c,d), each consisting of a central oral plate and several marginal floor plates fused into a single structure (figure 1o). The oral plates are subtriangular in outline, with a wide base. The floor plates are rectangular in outline and are oriented at an angle to the oral plate such that the compound interradial plates are highly concave with a scalloped margin (figure 1o). The axial floor plate is the longest and those lateral to it are successively shorter. High narrow ridges run along the length of the inner surface of the floor plates, decreasing in height from axial to lateral (figure 1c,d). Although the boundaries between the floor plates and the adjacent oral plate are not distinct, linear traces on the external surface (e.g. BC interradial plate in OUMNH C.36043: figure 1o), the arrangement of indentations in the scalloped margin (figure 1k–o), and the spacing of the ridges on the inner surface (figure 1f), demonstrate that nine floor plates surround each oral plate, one median, the others flanking it; the outermost floor plates are evident where the oral surface meets the suboral constriction (e.g. BC interradial plate in OUMNH C.36043: figure 1o). There are five straight ambulacra, which are apparently arranged into a slight 2–1–2 symmetry (figure 1c,d,g): the largest angle subtended by the oral surface is in ambulacrum A (approx. 116°; figure 1g). Cover plates are absent and the floor plates are separated resulting in a wide permanent gape (figure 1c,d).

OUMNH C.36043 preserves elongate tentacle-like structures situated on the inner surface of the compound interradial plates (figure 1e–g). These structures are widest at their base, becoming narrower distally until they reach a pointed tip. They are arranged in two sets: an upper set attaches about half-way up each compound interradial plate (near the top of the oral plate), and a lower set attaches close to the base. Both sets of structures extend upwards along the inside of the interradial plates; those in the upper set are generally longer than those in the lower and are roughly aligned with the slots bounded by the narrow ridges on the inner surface of the floor plates (figure 1f). Based on the best-preserved examples associated with the CD interradial plate, there appear to be nine structures in each set, i.e. one upper and one lower corresponding to each floor plate.

In specimen OUMNH C.36043, two elongate branching thread-like structures attach to two different interradial plates, but are not part of Heropyrgus disterminus. The first of these structures is attached to the exterior surface of a floor plate (AB interradius) and extends well above the oral surface (figure 1l,n). The second is much shorter and attaches to the inner surface of a floor plate (CD interradius), adjacent to one of the internal ridges (figure 1m).

The arrangement of plates in the collar is essentially fivefold (figure 1k,n). The plates alternate in position in successive rows which overlap proximally. There are at least six rows but the margins of the plates adjacent to the oral surface are difficult to discern. Smaller plates are occasionally intercalated in a row. Three smaller plates are evident between the five large ones that make up the most distal row in OUMNH C.36043 (figure 1k,n), for example, presumably filling in spaces (two others, making up the complement of five, may be concealed where the larger plates overlap laterally). This roughly symmetrical arrangement breaks down in the CD interradius towards the oral surface. Here, there is a somewhat disorganized configuration, including an elongate medial plate that slightly overlaps the oral plate and likely marks the position of the periproct (figure 1n). A small circular notch to the right of this plate presumably indicates the position of the hydropore and/or gonopore (figure 1n,p). The specimens available show no evidence of contraction or expansion of the collar.

A series of widely spaced, narrow short ridges is present at the base of the larger plates that form the distalmost row of the collar, where it inserts into the peduncle (figure 1s). These ridges are eight in number, corresponding to the number of columns in the peduncle itself. Thus, three of the collar plates bear two ridges and two others just one, reflecting their alignment with the peduncle columns. These ridges are clearly evident in OUMNH C.36044 (figure 1s) but more subdued in OUMNH C.36043. They are not evident on OUMNH C.36003 but this may be because the slices are oriented along the length of the specimen.

The peduncle is subcircular in cross-section, and its surface is covered by regularly spaced plates arranged in eight columns (figure 1a,b,n). The plates within each column overlap proximally (i.e. toward the oral surface) and are offset vertically resulting in a spiral appearance. The complete specimen, OUMNH C.36003, shows that the columns may consist of up to 25 plates (figure 1a). The peduncle of this specimen is gently curved (figure 1a). Sections through OUMNH C.36003 (e.g. G148, H172 in [19]) suggest that the peduncle was a hollow structure (figure 1b).

Beyond a slight constriction at its distal termination the peduncle transitions abruptly into the holdfast (‘basal coriaceous sac’ in [26]) (figure 1a,q,r). OUMNH C.36003 reveals spine-like ‘plates’ embedded in the dermis of this bulbous structure, projecting normal to its surface (figure 1q,r). The holdfast accommodates a deep circular depression in the centre into which the spines project (figure 1q,r). These spines become less densely spaced proximally until they are no longer present near the boundary with the plated peduncle. The holdfast is anchored by eight laterally projecting lobes (figure 1q,r).

4. Discussion

(a). Systematic position

The family Rhenopyrgidae includes several species that have been assigned to the genus Rhenopyrgus. Following Sumrall et al. [27], we consider R. coronaeformis, R. flos, R. piojensis and R. whitei the only unambiguous members of this genus. Heropyrgus gen. nov. shares a number of characters with Rhenopyrgus including a domed oral surface, differentiated suboral collar, long peduncle, and holdfast (coriaceous sac) composed of numerous small plates; these features clearly identify it as a rhenopyrgid edrioasteroid. A major difference between Heropyrgus and Rhenopyrgus, however, is the absence of cover plates, which distinguishes the Herefordshire taxon as a new genus. The remarkable preservation of the Herefordshire material, including the non-biomineralized tentacle-like structures (figure 1e–g), indicates that the specimens were buried alive and were not significantly impaired by decay. There is no evidence of cover plates, either in place, separated and lying within the gape, or otherwise associated with any of the three specimens that were serially ground [19]. The scalloped margin of the compound interradial plates would not have readily accommodated the articulating margin of a series of cover plates (compare, for example, with the straight proximal margins of cover plates in species of Rhenopyrgus illustrated in [27], figure 1). Thus, the available evidence indicates that cover plates were absent in life as opposed to lost and not preserved.

The assignment of rhenopyrgids to the Edrioasteroidea has never been in doubt and they are generally acknowledged to lie closest to cyathocystids and edrioblastoids. Holloway and Jell [25] erected the family Rhenopyrgidae to accommodate Rhenopyrgus, but did not assign it to either of the edrioasteroid orders defined by Bell [23], designating it as order uncertain. Smith and Jell's [4] cladistic analysis of Cambrian edrioasteroids and related taxa grouped Rhenopyrgus with the Cambrian genera Totiglobus and Cambroblastus. Guensburg and Sprinkle [28] revised the formal classification of Edrioasteroidea, placing Rhenopyrgus in a subfamily Rhenopyrginae of the family Cyathocystidae (together with cyathocystids), suborder Edrioblastoidina, order Edrioasterida. Sumrall et al. [27] favoured the same scheme, based on a cladistic analysis, but resurrected Holloway and Jell's [25] family Rhenopyrgidae alongside the family Cyathocystidae. We assign Heropyrgus to the Rhenopyrgidae as it differs from other members of this family only in the (secondary) loss of the cover plates. Sumrall et al.'s ([27], figure 2a) cladogram grouped Rhenopyrgus in a polytomy with Cyathotheca and Lampteroblastus (i.e. a clade equivalent to the suborder Edrioblastoidina).

Figure 2.

Reconstruction of the water vascular system in Heropyrgus disterminus. (a) Upper view. (b) Angled view. Abbreviations: lc, lateral canals; ra, radial canals; rg, ring canal; st, stone canal; tf, tube feet.

(b). The water vascular system

The tentacle-like structures evident on the interior of the compound interradial plates of Heropyrgus disterminus in OUMNH C.36043 (figure 1e–g) have never been described in any edrioasteroid. These structures are elongate with pointed tips, similar morphologically to the tube feet of many extant echinoderms including the knob-ending tube feet in certain asteroids (figure 1j) [29,30]. They are also similar to structures interpreted as non-suckered tube feet in the Herefordshire asteroid Bdellacoma sp. (figure 1i) [13]. Moreover, the structures in H. disterminus are situated on either side of each ambulacrum, as are the tube feet of all other echinoderms. For these reasons, we interpret the structures in H. disterminus as tube feet.

The tube feet of H. disterminus are arranged into upper and lower sets and roughly aligned with the floor plates (figure 1f). No other elements of the water vascular system are preserved, but we infer that it was similar to that in extant echinoderms. Thus, the tube feet were presumably joined by lateral canals to five radial canals that were aligned with the ambulacra in a 2–1–2 pattern [31] and connected by the ring canal [32]; if the circular notch at the bottom right of the CD interradius (figure 1n,p) represents a hydropore, this was presumably connected to the ring canal by the stone canal (figure 2). The placement of the tube feet indicates that the lateral canals were longer toward the centre and gradually reduced in length toward the periphery of the oral surface (figure 2).

The arrangement of the tube feet into upper and lower sets is radically different from anything previously documented in echinoderms. It also contrasts with all previous reconstructions of the edrioasteroid water vascular system, which inferred a one-to-one correspondence between tube feet and floor plates (e.g. [26,33,34]), whereas there are two tube feet per floor plate in H. disterminus. We find no evidence that the tube feet were closely associated with pores between adjacent floor plates [26,33,34]; the tube feet in H. disterminus are roughly aligned with ridges on the inner surface of the floor plates (figure 1f) and are not close to the floor plate margins. However, our material provides some support for Bell's [33] inference that the radial canals were internal. There is no evidence of grooves to accommodate canals on the exterior surface of the theca of H. disterminus and the floor plates could not have supported the radial canals because they are separated. We infer that the radial canals were suspended within the thecal cavity, where they would have been protected in the absence of overlying cover plates. It is not clear whether a similar arrangement was present in other edrioasteroids.

The position of the narrow ridges on the inner surface of the floor plates would have prevented the compound interradial plates from meeting. The remarkable preservation of the soft tissues (tube feet), never previously seen in any edrioasteroid, strongly suggests that the absence of cover plates and the spacing between the floor plates are real features, rather than artefacts of taphonomy. Thus, the large star-shaped opening onto the interior of the oral area was a permanent feature in life. The attachment of a thread-like structure, which we interpret as an epibiont, to the inner surface of a floor plate (figure 1m) is consistent with the absence of cover plates and a permanent gape. The tube feet are short and, even when fluid filled, almost certainly did not extend beyond the margin of the interradial plates. Consequently, it is unlikely that they could have captured food particles directly from the water column, as in crinoids. It seems more likely that H. disterminus captured suspended food particles that entered the oral area. The tube feet may have served to sort and transport food particles towards the mouth, as do the knob-ending tube feet in paxillosid asteroids [30]. The tube feet may also have played a role in respiration; the flow of water over tube feet in H. disterminus was facilitated by the large permanent opening onto the oral area, and would have enhanced gas exchange.

(c). Symmetry

Edrioasteroids originated in the Cambrian and the majority lived on the sediment surface during the early Cambrian before transitioning to hard substrates [35] or developing a peduncle for anchoring in soft sediment, the strategy adopted by Rhenopyrgus [4] and Heropyrgus. H. disterminus offers an opportunity to consider the evolution (and evolutionary development) of symmetry changes in echinoderms. The oral surface is pentameral and shows a slight 2–1–2 symmetry (figure 1c,g). The arrangement of plates in the collar is less regular, but essentially fivefold, particularly where it inserts into the peduncle. The plates of the peduncle are arranged in eight columns; adjacent plates are offset laterally resulting in a spiral appearance. An eightfold arrangement is also evident in projecting swellings at the end of the coriaceous sac. The most distal row of plates in the collar, which is dominated by five large plates, is marked by ridges, probably for muscle attachment [26]. Three of the five large plates bear two widely spaced ridges each, and the other two large plates bear just one, yielding a total of eight, which correspond in position to the eight columns in the peduncle. In this way the symmetry shifts from pentameral in the crown to eightfold in the peduncle.

Following the model of Mooi & David [36] we can posit the origins of the three regions in the body of rhenopyrgids. The oral surface belongs to the axial zone, and the collar and peduncle are extraxial. The axial zone of Helicocystis, the most primitive pentaradial echinoderm known [1], includes a spiral arrangement. In rhenopyrgids, the ambulacra are pentaradial but the plates of the extraxial peduncle form eight columns which are offset laterally, resulting in a spiral appearance. This illustrates the persistence of developmental flexibility in edrioasteroids.

Data accessibility

Serial-grinding datasets and triangle-mesh models in VAXML/STL format are available from the Dryad Digital Repository: http://dx.doi.org/10.5061/dryad.7005f [19].

Authors' contributions

D.E.G.B., D.J.S., D.J.S. and M.D.S. designed the research and carried out fieldwork. I.A.R. reconstructed the water vascular system and prepared the figures. D.E.G.B. wrote the paper with scientific and editorial input from all the other authors.

Competing interests

We have no competing interests.

Funding

This study was supported by the Natural Environment Research Council (Grant NE/F018037/1), the Leverhulme Trust (Grant EM-2014-068), the Yale Peabody Museum of Natural History Invertebrate Paleontology Division, the Oxford University Museum of Natural History, the John Fell Oxford University Press Research Fund and English Nature.