Introduction
Silurian-age diploporitan echinoderms are relatively scarce in the fossil record (Witzke et al., Reference Witzke, Frest and Strimple1979; Thomka and Brett, Reference Thomka and Brett2014). The Holocystites Fauna, however, is an important exception to this paucity of fossil material and presents a rare window into unusual middle Silurian echinoderm communities. This fauna is an abundant and diverse collection of middle Silurian diploporitan taxa from the midcontinental region of North America (i.e., Wisconsin, Illinois, Indiana, Kentucky, Ohio, Tennessee) (Frest et al., Reference Frest, Strimple and Paul2011) and possibly Australia (Jell, Reference Jell2011) that provides a unique opportunity to study paleoecology, taphonomy, and phylogenetics of this enigmatic clade. This study focuses on the generic classification of holocystitids, the dominant component of this fauna.
Understanding the systematics of Holocystitidae has been complicated by a number of issues. First, holocystitids have a plastic thecal morphology that shows wide variation within populations, resulting from irregular plating of the theca, allometric changes, and ecophenotypic variation, making species identification based on thecal morphologies unreliable (Sheffield and Sumrall, Reference Sheffield and Sumrall2015a). Some work has been done to identify holocystitids from preserved holdfasts attached to hardgrounds (e.g., Thomka et al., Reference Thomka, Brett, Bantel, Young and Bissett2016). However, thecae are disassociated from these holdfasts, so the taxonomic affinity is based on preserved aboral plating and general size of the holdfast. However, when found attached to large bioclasts, holocystitid holdfasts in softground settings can be extremely plastic, taking on the size and morphology of the underlying attachment surfaces, casting some doubt on the reliability of holdfast morphology for discriminating taxa across holocystitid-bearing localities. Second, many holocystitid species are based on extremely poorly preserved internal molds in sugary dolomite that are difficult to reconcile with more pristine specimens preserving external morphologies as original calcite. Third, species and genera were described with a poor understanding of the plating of the oral and summit structures, emphasizing presumed differences (often preservational) while overlooking fundamental similarities.
Fossils from the Holocystites Fauna were first published over a century and a half ago (e.g., Hall, Reference Hall1861, Reference Hall1864, Reference Hall1870). At that time, Holocystites Hall, Reference Hall1861 was the only proposed genus within the fauna, encompassing a wide variety of morphologies; a multitude of later studies (e.g., Miller, Reference Miller1878, Reference Miller1879; Miller and Gurley, Reference Miller and Gurley1888, Reference Miller and Gurley1894, Reference Miller and Gurley1895) proposed over 50 species assigned to this genus alone. Frest et al. (Reference Frest, Strimple and Paul2011) noted that the number of species proposed by Miller correlated closely with the number of specimens found within the formations being studied. These initial papers sought to document the wide disparity of morphologies present within holocystitids primarily via describing the differences noted across the thecae. Detailed descriptions of a large majority of these specimens were complicated by poor preservation that erased important information concerning thecal ornamentation and the oral area morphology.
More recent studies (Tillman, Reference Tillman1967; Paul, Reference Paul1971; Frest et al., Reference Frest, Mikulic and Paul1977, Reference Frest, Strimple and Paul2011) recognized the high morphological disparity within the numerous species of Holocystites and divided known taxa among multiple genera, including Holocystites Hall, Reference Hall1861; Trematocystis Jaekel, Reference Jaekel1899; Triamara Tillman, Reference Tillman1967; Pentacystis Paul, Reference Paul1971; Pustulocystis Paul, Reference Paul1971; Brightonicystis Paul, Reference Paul1971; Osgoodicystis Frest and Strimple, 2011; and Paulicystis Frest and Strimple, 2011 in Frest et al., Reference Frest, Strimple and Paul2011 (taxa used within this study are listed in Table 1). These genera were based on major variations in the morphology of the pore systems and observed differences within the plating of the oral area (Paul, Reference Paul1971). However, issues of taphonomy, especially concerning the preservation of the oral area, were interpreted taxonomically in these studies, leading to some species being based on state of preservation rather than phylogeny (Sheffield and Sumrall, Reference Sheffield and Sumrall2015a).
Table 1 Holocystitid taxa were delineated largely according to the inferred numbers of plates within each of the two circlets. The number of oral plates ranged from zero in Pentacystis to six in Holocystites. A revised analysis asserts that the changes in plate numbers are solely a taphonomic artifact. Brightonicystis was excluded from this study because of a lack of available material.
The systematics of Holocystitidae has been continuously revised and subdivided according to inferred differences in thecal and oral area morphology but in the absence of a unifying plating model of the oral area. Although two circlets of plates around the peristome were recognized (periorals, herein interpreted as orals sensu Sumrall, Reference Sumrall2010) forming the mouth frame and facetals bearing large facets for feeding appendages (Paul, Reference Paul1971), it was not realized that each of the holocystitid genera has the same complement of plates. This paper aims to review the Holocystites Fauna in a modern context by reinterpreting morphologies of the oral area through universal elemental homology (Sumrall, Reference Sumrall2010; Sumrall and Waters, Reference Sumrall and Waters2012; Kammer et al., Reference Kammer, Sumrall, Zamora, Ausich and Deline2013) and emending the generic diagnoses.
Holocystitid plate morphologies
Until recently, it was not recognized that a highly conserved set of axial skeletal elements—referred to as universal elemental homology (UEH)—was common to all derived blastozoan echinoderms. These taxa share a peristome that is bordered by seven interradially positioned oral plates (Sumrall, Reference Sumrall2010, Reference Sumrall2015). The CD interray is divided into three plates: O1, O6, and O7; O1 and O6 form the peristomial border, and O7 sutures distally to them and is associated with the hydropore and gonopore (Fig. 1.1). Plates O2–O5 are positioned clockwise in the remaining four interradii, forming the bifurcation points of the proximal ambulacra. In holocystitids, these oral plates were recognized as periorals except for O7, which was thought to belong to the facetal circlet (see the following).
Figure 1 (1) Typical peristomial border plating of holocystitids. The peristome (M) is bordered by seven oral plates (gray). The facetal circlet (white) lies distal to the oral plates and comprises seven plates; five generally bear facets for stout appendages and are associated with ambulacral rays (labeled A–E), and two lateral facet plates do not bear lateral scars (labeled L). The gonopore (black circle) is typically situated on O7; O7 is situated in the CD interray, in contact with the periproct (P) and is precluded from the peristome by O1 and O6. Modifications to this basic pattern are the basis for the identification of different taxa within the holocystitids. Modified from Sheffield and Sumrall (Reference Sheffield and Sumrall2015a). (2) Brightonicystis has been described as having ten oral plates, which is inconsistent with the model presented for Holocystitidae. It is unclear whether this taxon bears a defined facetal circlet. Illustrations in Paul (Reference Paul1971) do not unequivocally document the presence of ten oral plates, which has not been observed in any other echinoderm; more likely, each oral plate has been interpreted as two separate plates due to ambiguous plate sutures. Modified from Paul (Reference Paul1971). (3) Pustulocystis was previously described as having six facetal plates, although the plate in contact with O1 and O6 is here interpreted as O7 and not a facetal. This taxon has five facetal plates and seven oral plates; the lateral facet plates that do not bear facets are not present, leaving only facetal plates A–E. Note the loss of A ambulacrum. Line drawing of Pustulocystis pentax Paul, Reference Paul1971 (MUMG-T 226).
Oral plates are present in all holocystitids, but their recognition is complicated by two factors. First, in Holocystites, there is a slight clockwise rotation of the ambulacra system with respect to the theca (Fig. 1.1). This results in the ambulacral food grooves being positioned radially on the oral plates rather than along the sutures of the ambulacral system as is typical for most pentaradiate echinoderms (Sumrall, Reference Sumrall2015). The identity of the oral plates is straightforward because the compound oral plate complex, O1, O6, and O7, is positioned in the CD interray, based on 2-1-2 ambulacral symmetry and the position of the hydropore, gonopore, and anus (Sumrall, Reference Sumrall2010). Similar rotations are seen in other diploporitans such as Glyptosphaerites Müller, Reference Müller1854 and Eucystis Angelin, Reference Angelin1878.
Second, an open circlet of differentiated plates, called facetals, lies immediately distal to the oral plate circlet (Fig. 1.1). This facetal circlet normally includes seven plates; five are radially positioned and generally bear facets for stout appendages associated with each of the five main ambulacral rays (Paul, Reference Paul1971; Frest et al., Reference Frest, Strimple and Paul2011) and labeled here A–E depending on which ambulacrum they support (Fig. 1.1). In taxa bearing four ambulacra, the A ambulacrum is undeveloped, and consequently the A facetal plate lacks a facet. Two additional lateral facetals (labeled L) do not bear facets for appendages and are positioned between the B and C facetals to the right and the C and E facetals to the left in most taxa (Fig. 1.1). The facetal circlet is open between the C and D facetals because of the placement of O7 (Fig. 1.1). The facetal plate series is not part of the ambulacral system; rather, they are thecal plates that have ambulacra supported upon them epithecally (Sheffield and Sumrall, Reference Sheffield and Sumrall2015a). This is a common theme among diploporitans (e.g., Glyptosphaerites and Eucystis).
The plating of the oral area of Brightonicystis is inconsistent with the model presented for Holocystitidae (Paul, Reference Paul1971; Frest et al., Reference Frest, Strimple and Paul2011; Fig. 1.2). It was described as having 10 periorals (=orals), and it was unclear whether it had a defined facetal circlet. The specimen is unavailable for study, but according to the illustrations in Paul (Reference Paul1971), the presence of 10 orals cannot be confirmed, and there is no suggestion that this is the case. Indeed, if 10 orals are present, it would be unique not only to holocystitids, but to all stemmed echinoderms. It is possible that deep, angular food grooves mimic plate sutures as there are no indentations for three plate junctions on the appendage facets as illustrated (Fig. 1.2). Furthermore, the placement of additional non-facet-bearing facetals in between the A and B and between the D and E ambulacra, coupled with the wide geographic separation of this taxon, cast doubt on Brightonicystis sharing a close relationship with other holocystitids.
Pustulocystis (Fig. 1.3) also appears to vary from this holocystitid model. Although few specimens were available for analysis, previous authors (Paul, Reference Paul1971; Frest et al., Reference Frest, Strimple and Paul2011) have indicated that the oral plates bordering the peristome are in the standard configuration, and the lateral facetal plates are absent, leaving only facetals A–E. In addition, most specimens suggest loss of the A ambulacrum.
Taphonomy
North American holocystitids have two distinct taphonomic trends based on the formation in which they were deposited (Paul, Reference Paul1971). First, many holocystitid diploporitans are preserved as internal and external molds in coarsely crystalline dolomite (Fig. 2.1, 2.2). Typically, in older collections, only the poorly preserved internal mold of the specimen was recovered; the taxonomically important external mold counterparts of the specimens were left behind. On occasion, these internal molds can be used to describe generalized plating of the theca, but the combination of coarse crystallization and the preservation of only the internal morphology make interpretation of the oral area and respiratory pores nearly impossible. Consequently, most of the moldic specimens cannot be confidently diagnosed beyond holocystitid because of the significant loss of thecal morphologies.
Figure 2 Two common taphonomic preservation types found in holocystitids. (1) Lateral view of typical holocystitid mold (‘Racine Formation,’ Wisconsin). (2) The internal mold preserved as coarse crystalline dolomite does not usually preserve plating of the oral area, and often of the theca, in enough detail to study (Holocystites winchelli Hall, Reference Hall1868; CMCIP 26438). (3) Oral view of specimen preserved as original calcite; thecal plates are typically well preserved (Massie Formation, Indiana). (4) Lateral view of well-preserved specimen (Paulicystis sparsus; SUI 48164). These two very dissimilar preservational types make it difficult to reconcile the systematics of specimens found across holocystitid-bearing localities. Scale bar=1 cm.
The other dominant mode of preservation for holocystitids is preservation as original calcite showing external morphology in easily weathered mudstone (Fig. 2.3, 2.4). Consequently, the preservation is generally quite good and the only problems are that: (1) specimens are most often isolated from their holdfast structures; (2) many of the specimens are slightly compressed; and (3) many of the best-preserved specimens have been aggressively cleaned with air abrasion. In addition, Thomka et al. (Reference Thomka, Brett, Bantel, Young and Bissett2016) noted that a significant percentage of diploporitan specimens are encrusted to some degree, with some overgrowth of the oral area. Regardless, the plating of the oral area and thecal morphologies are much more readily identifiable in fossils preserved as original calcite than in those with moldic preservation. Unfortunately, associated free feeding appendages are not preserved with specimens of either preservation type in current collections. External morphologies of specimens preserved as original calcite are often difficult to reconcile with internal morphologies of those preserved as molds because of the inability to identify thecal morphologies and oral plating in the latter.
While holocystitid thecae are thick and heavily plated, the oral plates seem to be easily disarticulated and often become disassociated from otherwise well-preserved thecae, presumably due to some amounts of reworking after initial burial. This has taphonomically produced a variety of oral–facetal plate configurations described among specimens (Paul, Reference Paul1971; Frest et al., Reference Frest, Strimple and Paul2011). When fully articulated, the peristomial opening is bordered by six oral plates, O1–O6. Oral 7 and the seven facetal plates are in contact with this proximal oral circlet and are not in contact with the peristomial opening (Fig. 3.1). In some specimens, O2–O5 have become disarticulated from the peristome, making it appear as if the seven facetals, O1, and O6 (but not O7) border the taphonomically enlarged peristomial opening (Fig. 3.2). In other cases, O1–O6 have become disassociated with the theca, leaving a taphonomically enlarged peristomial border bordered by seven facetals and O7 (Fig. 3.3). Taphonomic effects are often exacerbated by aggressive use of air abrasion during specimen preparation that has worn away oral plates either in part or in whole. This situation formed the basis for the identification of Osgoodicystis, which is only distinguishable from Pentacystis by the lack of oral plates.
Figure 3 Common disarticulation patterns of holocystitid oral plating. (1) All seven oral plates associated with the theca, bordering the peristome. Schematic line drawing of Holocystites scutellatus (SUI 48183). (2) O2–O5 become disarticulated from the peristome, giving the appearance of an enlarged peristome being bordered by the facetal circlet and O6 and O7. Schematic line drawing representative of the oral area of Holocystites spangleri Miller, Reference Miller1891 (SUI 48197). (3) O1–O6 have been disarticulated, giving the appearance of a greatly enlarged peristomial opening being bordered by the facetal plate circlet. This plating pattern has been used to separate Pentacystis Paul, Reference Paul1971 (those without most oral plates) and Osgoodicystis Frest and Strimple, 2011 in Frest et al., Reference Frest, Strimple and Paul2011 (those with oral plates); because the only significant difference between these two proposed genera is taphonomic, Osgoodicystis is rejected as a junior synonym of Pentacystis. Schematic line drawing of Pentacystis gibsoni Frest and Strimple, 2011 (SUI 46316). M=mouth; P=periproct; L=lateral facet.
Non-holocystitid Silurian diploporitans from North America
Holocystitids are typified by a number of features that appear to be unique to this clade. The thecae are typically large (compared to other diploporitans), with some specimens reaching 15 cm in thecal height. With the possible exception of diplopore-bearing Triamara (which may or may not be a holocystitid; see discussion in the following), holocystitids bear humatipores that lie solely within individual thecal plates and have numerous coelomic canals covered by a bulbous, lightly skeletonized covering. Other diploporitan groups typically have simple diplopores composed of a single, uncalcified thecal canal that is rarely preserved. In fossils, these structures are expressed as two pores contained within a depression on the external portion of the thecal plate (for further information regarding diploporitan respiratory structures, see Paul, Reference Paul1972).
The ambulacra of holocystitids are also morphologically different from other diploporitans. They have highly reduced proximally recumbent ambulacral systems that are restricted to the summit on the orals and facetals, and erect appendages (recumbent and epithecally positioned in Paulicystis) of unknown affinities; the oral areas of holocystitids do not bear floor plates incorporated into the theca as do most blastozoans (Sumrall, Reference Sumrall2010, Reference Sumrall2015). Erect appendages, either erect ambulacral floor plates presumably bearing brachioles or more likely greatly enlarged terminal brachioles borne on facets that are positioned on the facetal circlet, are unique to holocystitids. Judging from the size of the facets and plating scars on Paulicystis, these appendages are biserial and proportionately exceptionally large for a blastozoan.
Other occurrences of diploporitans from the Silurian of North American are morphologically highly dissimilar to holocystidids, and until recently, the only described taxon was Gomphocystites Hall, Reference Hall1864 (Fig. 4.1). Gomphocystites occurs slightly earlier than the holocystitids, with the earliest undoubted occurrence in the Llandovery-age Hopkinton dolomite of Iowa (Witzke, Reference Witzke1976) and persists as a common faunal component in strata containing the Holocystites Fauna (which are largely restricted to Wenlock age). Gomphocystites also has a greater biogeographic range than holocystitids, with fossils known from New York, USA (Brett, Reference Brett1985a), and the Baltic Celtacystis (Gomphocystites) gotlandicus (Angelin, Reference Angelin1878), which has been proposed to be very closely related to Gomphocystites (Bockelie, Reference Bockelie1979, Reference Bockelie1984). The morphology of Gomphocystites deviates strongly from holocystitids. It has a typical oral plate–bearing oral area but lacks O7, and plates O2 and O5 are not in contact with the peristomial opening. The recumbent ambulacra are long and spiraling and wrap around the theca, but they bear brachiole facets only on the left side and seem to be borne on floor plates that are restricted to the left side. They also bear true diplopores instead of the humatipores of holocystitids.
Figure 4 (1) Gomphocystites indianensis Miller, Reference Miller1889, a nonholocystitid diploporitan from the Silurian of North America. Note the long, spiraling ambulacra. Brachiole facets are borne from the left side of the ambulacra only. True diplopores situated within shallow, elliptical peripores are clearly seen in this image (FMNH 19708). (2) Middle Silurian Eucystis specimen from the Bainbridge Formation of Missouri. Oral area pictured shows five multibranching ambulacra extending across the orals and proximal thecal plates and ending in various numbers of large brachiole facets (CMCIP 53630). Scale bars=1 cm.
The only other known Silurian diploporitan from North America is a recently discovered and undescribed species of Eucystis from Wenlock-age strata of the Bainbridge Group of Missouri (Sheffield and Sumrall, Reference Sheffield and Sumrall2015b). These specimens (Fig. 4.2) share strong morphological similarities with Eucystis from the Ordovician Baltican and peri-Gondwanan faunas. Like their Baltican and peri-Gondwanan counterparts, these specimens have five multibranching ambulacra extending across the orals and proximal thecal plates without underlying floor plates. These food grooves each end in a brachiole facet. The diplopores are simple, and the theca bears an unusually large holdfast that flares slightly at the attachment surface (whether this flaring is characteristic of this taxon or was formed around an unusually large bioclast is unclear). However, these specimens share a similar, slightly clockwise rotation of the oral plates with respect to the ambulacra with Holocystites and Glyptosphaerites. It is clear, from strong morphological deviations, that neither Gomphocystites nor these recently discovered eucystitid specimens are closely related to members of Holocystitidae. Details of the relationships between these taxa are pending phylogenetic analyses that are currently in progress.
Previous phylogenetic analysis
An evolutionary hypothesis of the Holocystitidae was proposed by Frest et al. (Reference Frest, Strimple and Paul2011), based on assumed trends in peristomial morphology. A second analysis based on a stratocladistic model is not discussed here. The resulting phylogeny (Fig. 5) shows a complicated evolutionary history with drastic changes in the oral area of the diploporitans from an inferred hypothetical ancestor to the more derived taxa (Table 1). Holocystites and Trematocystis are depicted as grades of organization at nodes rather than as monophyletic groupings of taxa. Frest et al. (Reference Frest, Strimple and Paul2011) drew the conclusion that more-derived holocystitids trended toward a reduced number of plates within the oral area. As mentioned in the preceding, the number of plates observed was affected by taphonomy and specimen preparation and is, therefore, not based on the evolutionary history of the taxa involved. Further, Paul (Reference Paul1971) and Frest et al. (Reference Frest, Strimple and Paul2011) misidentified an oral plate (O7) as a facetal plate, which influenced their interpretations. Some of the characters within their analysis were based on counting the numbers of plates present in proposed taxa. However, characters based on the number of plates present in the absence of a clear understanding of which homologous elements are present and absent among taxa are not properly constructed because the alternate states are not derived from a single character transformation.
Figure 5 A proposed evolutionary hypothesis proposed by Frest et al. (Reference Frest, Strimple and Paul2011), based on changes within peristomial morphology; note that Holocystitinae, Holocystites, and Trematocystis are all paraphyletic. This analysis interpreted a trend toward a reduction in oral plates in advanced holocystitids, such as Pentacystis, whose species were described as having vestigial or absent oral plates. Figure modified from Frest et al. (Reference Frest, Strimple and Paul2011).
Materials and methods
Repositories and institutional abbreviations
All taxa studied for this analysis, along with their locality and age information, are listed in Table 2. All specimens are housed in research collections from the following museums or institutions: Cincinnati Museum Center (CMCIP), Field Museum of Natural History (FMNH; UC), The University of Iowa (SUI), Miami University (MUMG), and Yale Peabody Museum (YPM). Brightonicystis was not examined for this study because of a lack of available material.
Table 2 Specimens utilized in this study. SUI=University of Iowa; YPM=Yale Peabody Museum; CMCIP=Cincinnati Museum Center; AMNH=American Museum of Natural History; FMNH=Field Museum; UC=University of Chicago (note: all University of Chicago specimens are now reposited at The Field Museum); MUMG=Miami University Museum of Geology. Age and locality information are provided.
Systematic paleontology
Subphylum Blastozoa Sprinkle, Reference Sprinkle1973
Class Diploporita Müller, Reference Müller1854
Superfamily Sphaeronitida Neumayr, Reference Neumayr1889
Family Holocystitidae Miller, Reference Miller1889
Type genus
Holocystites Hall, Reference Hall1861
Other genera
Trematocystis Jaekel, Reference Jaekel1899; Pentacystis Paul, Reference Paul1971; Pustulocystis Paul, Reference Paul1971; Brightonicystis Paul, Reference Paul1971; Paulicystis Frest and Strimple, 2011 in Frest et al., Reference Frest, Strimple and Paul2011.
Emended diagnosis
Large diploporitans with peristomial border plating pattern comprising two distinct circlets of plates, oral plate series and facetal series; O1–O6 surround peristome; O1 and O6 preclude O7 from the peristomial border; O7 is in contact with the periproct. Facetal plate series distal to oral plate series. Five facetal plates lie radially and bear large facets for feeding appendages (some facets missing in taxa bearing fewer than five ambulacra). Two lateral facetal plates positioned between B and C, and the D and E ambulacra lack facets; these lateral facetal plates are lacking in Pustulocystis. Facetal plate series open, being interrupted by O7. Floor plates not incorporated into oral surface, either absent or restricted to unknown erect ambulacra. Stem absent. Holdfast present at distal end of theca.
Remarks
The plating of the oral area with the orals bordered by facetals is unique to Holocystitidae and is the primary distinguishing feature of the clade. The large facets on the facetal series connect to food grooves extending from the peristome without underlying floor plates. The nature of the appendages that arise from these facets remains unknown. Two scenarios are thought to be possible. First, erect ambulacra in the form of biserial ambulacral floor plates likely bearing biserial brachioles arise from the facets. Their biserial nature is supported by the facet having scars for two perradially positioned plates. Further, the scars on Paulicystis where the appendages are not preserved but recumbent show them to be biserial. The second option is that these facets are for extremely stout terminal brachioles. If these are brachioles, they would be among the most robust brachioles known, being an order of magnitude larger in diameter than those typically found in blastozoans. Only material preserving these appendages will elucidate the nature of these appendages and add more data to the diagnosis.
Previously proposed subfamilies within Holocystitidae include Holocystitinae Miller, Reference Miller1889 (comprising Holocystites and Brightonicystis), Trematocystinae Frest and Strimple, 2011 in Frest et al., Reference Frest, Strimple and Paul2011 (comprising Trematocystis, Pustulocystis, and Paulicystis), and Pentacystinae Frest and Strimple, 2011 in Frest et al., Reference Frest, Strimple and Paul2011 (comprising Pentacystis and Osgoodicystis). These subfamilies were identified by the previous phylogenetic analysis and differentiated from one another largely on the basis of numbers of facetal and oral plates. Frest et al. (Reference Frest, Strimple and Paul2011) interpret Holocystitinae as being a paraphyletic grade with respect to Trematocystinae and Pentacystinae (Fig. 5). Furthermore, the Pentacystinae were partially designated on taphonomic features (Sheffield and Sumrall, Reference Sheffield and Sumrall2015a). These subfamilies are not discussed here further pending phylogenetic analysis of the taxa in question.
Triamara was separated from Holocystitidae and placed within Aristocystitidae Neumayr, Reference Neumayr1889, on the basis of Triamara having simple diplopores and not humatipores (Tillman, Reference Tillman1967). As blastozoan respiratory structures have been shown to appear more than once in evolutionary history (Sumrall and Gahn, Reference Sumrall and Gahn2006), it is not clear that using respiratory structures is valid for defining higher-level taxonomy. Triamara and Holocystitidae share some similar features concerning the peristomial border plating system, but there are also some strong deviations (see the following discussion of Triamara for further details); unfortunately, the oral areas of the studied specimens of Triamara were insufficiently preserved to be interpreted in detail. Pending better material, we retain Aristocystitidae for species of Triamara.
Genus Holocystites Hall, Reference Hall1861
Figures 6.1, 6.2, 7.1, 7.6, 7.7, 7.8
Figure 6 (1) Holocystites scutellatus (SUI 48183) oral view. (2) Interpretation of oral area of Holocystites scutellatus; note that facet-bearing facetal plates are loosely positioned on more than one facetal. (3) Pentacystis gibsoni (SUI 46316) oral view. (4) Interpretation of oral area of Pentacystis gibsoni; note five facetal scars lying atop facet-bearing plates and semiprotuberant summit. Attachment scars on the oral area of Pentacystis (SUI 46316) clearly show where O1–O6 were attached before they were disarticulated. (5) Osgoodicystis bissetti Frest and Strimple, 2011 in Frest et al., Reference Frest, Strimple and Paul2011 (SUI 48166) oral view. (6) Interpretation of oral area of Osgoodicystis bissetti shows a plating pattern identical to that of Pentacystis, with the exception that the oral plates are still intact. (7) Trematocystis magniporatus (SUI 48198) oral view. (8) Interpretation of oral area of Trematocystis; note absence of A ambulacrum and firm positioning of facets on one facetal plate. (9) Paulicystis sparsus (48164) oral view. (10) Interpretation of oral area of Paulicystis sparsus; note absence of A ambulacrum and presence of recumbent ambulacral scars on the theca. OO indicates disarticulated oral plates of this specimen. Open circles on O7 indicate position of gonopore. O=oral plate; P=periproct; M=mouth. Scale bars=1 cm. Modified from Sheffield and Sumrall (Reference Sheffield and Sumrall2015a).
Figure 7 (1) Holocystites scutellatus (SUI 48183). Theca squat, globular with numerous tumid plates with moderately impressed sutures. Distal end tapers considerably into holdfast. (2) Trematocystis magniporatus (SUI 48198). Theca squat, with large and flat plates, without impressed sutures. Theca narrows slightly into holdfast. (3) Paulicystis sparsus (SUI 48164). Theca squat, globular with numerous small, tumid plates with deeply impressed sutures. Theca widens distally into holdfast. (4) Pentacystis gibsoni (SUI 46316). Theca elongate to globular with relatively large, flat plates without impressed sutures. Theca narrows moderately into holdfast. (5) Osgoodicystis bissetti (SUI 48166) is highly morphologically similar to Pentacystis; theca elongate with relatively large, flat plates without impressed sutures. Theca narrows moderately into holdfast. Note that circular depressions on theca are attributed to parasitic embedment structures, Oichnus Bromley (Tremichnus sensu Brett, Reference Brett1985b). (6) Holocystites sp. (YPM 34764). Theca is relatively large and narrows considerably distally. Plates are highly disorganized and of multiple generations. (7) H. cylindricus (YPM 19175). Theca is elongated and cylindrical without distal constriction. Plates are organized and of one generation. (8) Holocystites sp. (YPM 519465). Theca is squat and globular and narrows distally into holdfast. Plates are disorganized and of multiple generations. Scale bar=1 cm.
Type species
Caryocystites cylindricum Hall, Reference Hall1861
Emended diagnosis
Five ambulacra present, extending from peristome to facet scars that straddle distal edges of oral plate series and facetal plates, typically positioned on more than one facetal plate (Fig. 6.1, 6.2). Oral plate series slightly rotated clockwise with respect to ambulacra. Thecal plates tumid with sunken sutures (Fig. 7.1).
Remarks
This diagnosis is based on preserved oral areas of multiple Holocystites species. Holocystites bears the stereotypical peristomial plate arrangement of holocystitids. All five ambulacra lead to facetal scars that are partly positioned between the oral plate series and the facetal circlet (Fig. 6.1, 6.2). The positioning of the facets is looser than other taxa spread across the edges of more than one facetal.
Holocystites species show wide morphological variability, suggesting that more than one clade may be represented (Fig. 7.6, 7.7, 7.8). Proposed species show wide variation in the organization of the theca, ranging from moderately well-organized plate circlets to disorganized, irregularly plated thecae and species with large plates and relatively small plates. Holocystites species also encompass a wide range of thecal body shapes, ranging from long and elongate to very globose. Further, ontogenetic sequences for most holocystitids are not understood; therefore, changes in plating patterns and thecal shape that occurred during ontogeny of species are likely adding to confusion concerning holocystitid systematics. Holdfasts can range from tapering to an almost stem-like projection to robust forms that lack noticeable narrowing. Unfortunately, many of the species currently assigned to Holocystites do not have oral areas preserved. Because the features of the theca and holdfast are so highly variable, they cannot be used to determine genus-level placement of species.
Genus Trematocystis Jaekel, Reference Jaekel1899
Type species
Holocystites subglobosus Miller, Reference Miller1889 (H. globosus Miller, Reference Miller1878)
Emended diagnosis
Four ambulacra, B, C, D, and E, extend from peristome to facet scars that lie on top of facetal plates (Fig. 6.7, 6.8); the A ambulacrum not developed; B–E facets centered on facet-bearing facetal plates. Lateral facetals and A facetal plate depressed; O7 proportionally small. Thecal plates large and flat without sunken sutures (Fig. 7.2). Theca globular and squat, with relatively wide cementation disk.
Remarks
Trematocystis bears the stereotypical holocystitid peristomial border plating (Fig. 6.7, 6.8). It is unusual because the A ambulacrum is not developed, likely resulting from paedomorphic reduction, a phenomenon seen in other blastozoan groups (Sumrall and Wray, Reference Sumrall and Wray2007). Among holocystitids, this reduction is also seen in Paulicystis, but there the appendages are recumbent, as evidenced by biserial scars extending a short way down the thecal plating near the summit. Large facets for the B–E ambulacra are centered on the facetal-bearing plates, and the presence of facets that do not cross the facetal plate boundaries serves to separate this taxon from Holocystites. The lateral, non-facet-bearing facetal plates and the A facetal plate are depressed with respect to others within the facetal plate series as seen in Pentacystis.
Genus Paulicystis Frest and Strimple, 2011 in Frest et al., Reference Frest, Strimple and Paul2011
Type species
Paulicystis densus Frest and Strimple, 2011 in Frest et al., Reference Frest, Strimple and Paul2011
Emended diagnosis
Four ambulacra, B, C, D, and E, extend from peristome to facet scars that lie on top of facetal plates. The A ambulacrum not developed. Ambulacra epithecally recumbent upon theca (Fig. 6.9, 6.10). Lateral facetals and A facetal plate depressed. Periproct relatively large. Theca squat and globular (Fig. 7.3). Plates small, tumescent, with deeply depressed sutures. Relatively wide cementation disk.
Remarks
Paulicystis bears the stereotypical plate arrangement for the peristomial border (Fig. 6.9, 6.10). As with Trematocystis, the A ambulacrum is absent, likely resulting from paedomorphic ambulacral reduction as seen commonly among blastozoans (Sumrall and Wray, Reference Sumrall and Wray2007). The B–E ambulacra are not erect, as in the other genera, but instead lie recumbently on the thecal surface, beginning with the facet scars on the facetal plates. This shows the appendages to be biserial (Fig. 6.9) but adds little information about whether they are floor plates or brachiolar plates. Large facets for the B–E ambulacra are centered on facetal-bearing plates, and the presence of facets that do not cross plate boundaries serves to separate this taxon from Holocystites. The non-facet-bearing facetal plates and the A facetal plates are depressed with respect to others within the facetal plate series.
Genus Pentacystis Paul, Reference Paul1971
Type species
Pentacystis simplex Paul, Reference Paul1971
Emended diagnosis
Five ambulacra extend from peristome to very large facet scars that lie on top of facetal plates. Facetal plates large and elevated to form a low spout-like protuberant summit structure (Fig. 6.3, 6.4). Plates of the oral series narrow and confined to peristomial depression, except for relatively large O7. Theca elongate, narrows slightly toward the base without a constricted distal portion. Plates large and flat, without depressed sutures (Fig. 7.4).
Remarks
Pentacystis bears the stereotypical holocystitid peristomial border plating. All five ambulacra extend to very large facets that bear erect feeding appendages. These facets are wholly supported on the facet-bearing plates and do not cross facetal plate boundaries. This serves to separate this taxon from Holocystites; the presence of a facet on the A facetal serves to separate Pentacystis from Trematocystis and Paulicystis. The oral plates within the oral plate circlet are proportionally narrow compared to O7. The facetals form a spout-like protuberant summit structure unlike the rounded summits of other holocystitids. The non-facet-bearing lateral plates are not depressed with respect to other plates within the facetal series, adding to the spout-like appearance of the summit area. Humatipores are present on the thecal plates.
Pentacystis was proposed as a separate genus within Holocystitidae on the basis of the oral plates being greatly reduced or absent (Paul, Reference Paul1971). Species within this genus were delineated by the presence or complete absence of oral plates; specimens with present or reduced (herein interpreted as partially disarticulated) oral plates were used to describe P. wykoffi (Miller, Reference Miller1891), whereas specimens with absent oral plates were assigned to P. simplex and P. sphaeroidalis (Miller and Gurley, Reference Miller and Gurley1895; Fig. 8).
Figure 8 Species of Pentacystis were previously proposed according to whether oral plates were present, reduced, or absent. (1) P. simplex (Paul, Reference Paul1971) was described as having no oral plates. (2) P. wykoffi (Miller, Reference Miller1891) was described as having six oral plates (O7 was misidentified as a facetal plate). P. wykoffi was later reassigned to Osgoodicystis to reflect the presumed systematic differences of those without oral plates (Pentacystis) and those with oral plates (Osgoodicystis). Oral plates of P. wykoffi are outlined in gray. Gonopore position indicated as black circles. P=periproct; M=mouth. Modified from Paul (Reference Paul1971).
Osgoodicystis Frest and Strimple, 2011 in Frest et al., Reference Frest, Strimple and Paul2011 (Figs. 6.5, 6.6, 7.5) was erected within the same subfamily as Pentacystis (Pentacystinae) because of the presence of the oral plates observed in some specimens. Species of Pentacystis with preserved oral plates, such as P. wykoffi, were reassigned to Osgoodicystis to reflect this. Osgoodicystis closely resembles Pentacystis in thecal shape, and outside of the differences in size and number of the oral plates, they are nearly identical in terms of major morphological features (Figs. 6.3, 6.4, 6.5, 6.6, 7.4, 7.5).
Reinvestigation of these specimens shows that the differences previously noted in the oral areas are based on taphonomy and preparation. Attachment scars from O1–O6 are clearly visible upon all the specimens in question, though in many cases they are obscured by aggressive preparation with air abrasion. Oral 7 is contained within the CD interray, as is typical for all holocystitid specimens. As the only major difference between Pentacystis and Osgoodicystis is taphonomic, Osgoodicystis Frest and Strimple, 2011 in Frest et al., Reference Frest, Strimple and Paul2011 is reassigned as a junior synonym of Pentacystis Paul, Reference Paul1971.
Genus Brightonicystis Paul, Reference Paul1971
Type species
Brightonicystis gregarius Paul, Reference Paul1971
Remarks
The oral area plating of Brightonicystis (Paul, Reference Paul1971; Frest et al., Reference Frest, Strimple and Paul2011) is inconsistent with the model presented for Holocystitidae. It was described as bearing 10 periorals (=orals), and it was unclear whether it had a defined facetal circlet. Plates consistent with the facetal series suggest the presence of additional plates between the A and B and between the D and E ambulacra, unlike any other holocystitid (Fig. 1.2). Furthermore, the illustrations in Paul (Reference Paul1971) do not adequately document the presence of ten orals (Fig. 1.2), which seems highly unlikely as this condition is unknown in any other echinoderm. It may be that each of the oral plates is being interpreted as a pair of plates and the food grooves interpreted as sutures because of rotation of the oral plates. However, due to a lack of available material, Brightonicystis will not be rediagnosed in this study.
Pustulocystis Paul, Reference Paul1971
Figure 9 (1) Pustulocystis pentax (MUMG-T 266). Oral area shows the normal holocystitid oral area, with O1–O7 in the standard configuration. However, the lateral non-facet-bearing facetal plates are absent, leaving only facetals A–E. Gonopore visible on O7; hydropore slit straddles the suture between O1 and O6. (2) Side view. Theca elongate. Plates numerous and flat without depressed sutures. Theca narrows into holdfast. (3) Triamara ventricosa (UC5997). Oral area potentially shows a peristomial border-plating pattern similar to that of holocystitids, but due to poor preservation, this cannot be confirmed. A ambulacrum absent; shared ambulacrum BC present, as well as D and E. D ambulacrum food groove bifurcates distally and terminates in two separate facets on top of facetal bearing plates. The position and number of the facets cannot be determined from this specimen. A crinoid holdfast is growing around the border of the periproct, which is separated from O7 by a thecal plate. (4) Side view. Theca proportionally large and elongate. Plates numerous and appear to represent two generations. Plates flat without impressed sutures. Theca narrows considerably into holdfast. Scale bar=1 cm.
Type species
Holocystites ornatissimus (Miller, Reference Miller1891)
Remarks
One specimen of Pustulocystis, Paul, Reference Paul1971 was examined as part of this study. This taxon has the normal holocystitid oral area with seven oral plates in the standard configuration bordered by a facetal series. The primary difference is the absence of the lateral facetal plates, leaving only facetals A–E (Figs. 1.2, 9.1). The lateral facetal plate absence serves to diagnose this taxon. Species within Pustulocystis are largely differentiated by the number of ambulacra present; some proposed species within this taxon are diagnosed by the absence of the A ambulacrum, whereas others have no reduction of ambulacra. Because of a lack of available material, the diagnosis for this taxon is not herein emended.
Superfamily Aristocystitidae Neumayer, 1889
Remarks
Members of Aristocystitidae are characterized by very short and unbranched ambulacra (Kesling, Reference Kesling1967). All other genera within Aristocystitidae are placed within subfamilies, except for Triamara, due to uncertainty about its placement (Paul, Reference Paul1971).
Genus Triamara Tillman, Reference Tillman1967
Type species
Triamara cutleri Tillman, Reference Tillman1967
Emended diagnosis
Three ambulacra, likely shared BC, D, and E because of their relative positions with respect to oral plates, extend from peristome to facet scars that lie on top of a facetal plate (Fig. 9.1). The D ambulacrum bifurcates and leads to two distinct facets on the D facetal plates. Facetal plates not clearly diagnosable from other plates in summit area, slightly elevated to form a moderately high spout-like protuberant summit. Oral plates relatively large. Theca narrows into constricted distal holdfast (Fig. 9.2). Diplopores present on thecal plates.
Remarks
Triamara appears to bear most aspects of the stereotypical holocystitid peristomial border plating pattern. Unfortunately, heavy taphonomic disarticulation has affected the oral areas of most curated specimens, and details concerning the number and placement of the facetals cannot be determined at this time. Orals 1–6 surround the ovate peristome. Orals 1, O6, and O7 are within the CD interray, with O1 and O6 precluding O7 from the peristome. Facetals D and E are in the expected position, but the position of the facetal in association with shared B and C ambulacrum is unclear due to taphonomic overprinting (i.e., disarticulation and breakage of plates in the oral area, along with noticeable thecal compaction). In some specimens of Triamara (e.g., Triamara ventricosa Paul, Reference Paul1971), a plate appears to separate O7 from the periproct, unlike holocystitids (Fig. 9.3). It is unclear whether this is common to Triamara or unique to T. ventricosa. Both oral plates and facetal plates are extremely large, even when considering that Triamara is relatively larger than most holocystitids. Theca plates are relatively large and appear to have two generations of plates, primary and secondary (Fig. 9.4). Diplopores, as opposed to humatipores, are densely and evenly spread across the thecal plates.
The peristomial border plating pattern of Triamara bears strong similarities to Holocystitidae, as does the makeup of the theca. However, due to dissimilarities in the sizing of the oral and facetal plates, the presence of diplopores, the different positioning of the periproct with respect to O7, and the poor preservational detail of the oral area that pervades curated specimens, it is unclear whether Triamara is a member of the holocystitid clade. As such, it will not be reassigned until new data can be collected.
Conclusions
Previous studies of the Holocystites Fauna were problematic because of oversplitting of poorly preserved species and a misinterpretation of the peristomial border plate system resulting in a complicated and unparsimonious evolutionary history. Careful analysis of numerous well-preserved specimens shows that the peristomial border plate system among holocystitid taxa is much more conservative than previously described. Many of the ascribed differences proposed by previous authors were based on taphonomic differences or a lack of understanding of the homologous elements of the oral plating system. Consequently, Osgoodicystis Frest and Strimple, 2011 in Frest et al., Reference Frest, Strimple and Paul2011 is a junior synonym of Pentacystis, Paul, Reference Paul1971. The systematic placement of Triamara Tillman, Reference Tillman1967 is unclear due to poor preservation. While it bears many peristomial border similarities to holocystitids, there are also many differences in the size and placement of these oral area plates. Numerous examples of blastozoan respiratory structures re-evolving suggests that delineating higher-level systematics solely on the basis of the presence of humatipores or diplopores is likely not valid. However, these other differences in Triamara, in combination with the presence of simple diplopores, suggest the possibility that it is not a member of the holocystitid clade. Pending new data, we retain Aristocystitidae for species of Triamara.
The oral area of blastozoan echinoderms is the key to delineating systematic relationships, as evidenced by the plastic nature of the theca in the holocystitids. While it is very likely that a number of species proposed within the remaining genera of the Holocystites Fauna should be synonymized or reassigned to other genera, a lack of preserved oral areas that pervades a significant number of type specimens makes it is impossible to assess the systematic placement of many species.
Acknowledgments
We are grateful to the following for their assistance with museum specimens: T. Adrain, The University of Iowa; S. Butts, Yale Peabody Museum; K. Hollis, U.S. National Museum of Natural History; B. Hunda, Cincinnati Museum Center; B. Hussaini, American Museum of Natural History; P. Mayer, The Field Museum; K. Hauer, Miami University. K. B. Gibson collected the specimens of Eucystis from the Bainbridge Formation. This work was supported by grants awarded to SLS from The Paleontological Society, The Dry Dredgers, SEPM, and the Schuchert and Dunbar Grants-in-Aid Program, as well as NSF Assembling the Echinoderm Tree of Life project, DEB-1036260 awarded to CDS. We are grateful to T. Kammer, J. Waters, and J. Thomka for reviews that strengthened this manuscript.
