Non-technical Summary
Crinoids, the group known today as the sea lilies, were a major constituent of ocean environments from the late Carboniferous (323–299 million years ago). However, crinoid fossil-forming potential is poor, and they typically fell apart quickly after death. This limits our ability to study much about their life histories, including how they would have grown. Through the discovery of an area of exceptional fossil preservation in the Barnsdall Formation of Oklahoma, we have a rare chance to learn about the growth of one of these species of crinoids, Erisocrinus typus. Here we perform a growth analysis of a well-preserved series of fossils and discuss the patterns that it showed from its juvenile stage to adulthood.
Introduction
Although crinoids were a major component of Paleozoic marine communities (Sepkoski, Reference Sepkoski1981; Simms, Reference Simms, Hess, Ausich, Brett and Simms1999), there are gaps in our knowledge of a number of species’ systematics, morphology, and ontogeny due to a differential preservation potential among different crinoid clades, causing many taxa to have few complete, well-preserved specimens across multiple growth stages. Crinoid skeletons are composed of numerous calcareous plates that are connected by soft tissues (i.e., muscles and ligaments); after death, the crinoid is prone to rapid disarticulation as the muscles and ligaments decay (Brett et al., Reference Brett, Moffat and Taylor1997; Thomka et al., Reference Thomka, Lewis, Moscher, Pabian and Holterhoff2011). As a result, there is a distinct lack of articulated crinoid skeletons in the fossil record, which has hampered investigations regarding ontogeny (Meyer, Reference Meyer1971; Liddell, Reference Liddell1975; Thomka et al., Reference Thomka, Lewis, Moscher, Pabian and Holterhoff2011). However, not all crinoids have the same disarticulation potential due to differences in their construction. Camerate crinoids have tight suturing of the plates of the calyx, and the arms are incorporated into the cup by interradial and interbrachial plates, which results in a relatively high percentage of crown preservation (Brower, Reference Brower1974; Brower and Venous, Reference Brower and Venous1978). Compared with the camerates, cladid crinoids have looser suturing of the plates of the calyx and a lack of interradial and interbrachial plates, allowing the arms to fall away from the cup soon after death as the muscles and ligamentary tissues holding them together begin to decay (Liddell, Reference Liddell1975; Ubaghs, Reference Ubaghs and Moore1978; Ausich and Baumiller, Reference Ausich and Baumiller1993; Kammer and Ausich, Reference Kammer and Ausich2007; Brower, Reference Brower2010; Thomka et al., Reference Thomka, Mosher, Lewis and Pabian2012). Cladid taxa are often represented by single specimens (e.g., Sheffield, Reference Sheffield2015) and complete, preserved growth series are much scarcer compared with other subclasses of the class Crinoidea (Brower, Reference Brower1974; Ausich and Wood, Reference Ausich and Wood2012).
The lack of well-preserved collections of cladids places limitations on what can be learned from them. However, the discovery of crinoid-bearing Lagerstätten, fossil deposits of exceptional preservation (Seilacher, Reference Seilacher1970), can often provide a more complete picture of fossil crinoids than is usually seen. The Barnsdall Formation, exposed near Copan, Oklahoma, USA (Fig. 1), is a Koncentrat-Lagerstätte with a rich diversity of Late Pennsylvanian crinoids (Oakes, Reference Oakes1951; Lewis et al., Reference Lewis, Holterhoff, Mosher and Pabian1998; Thomka, Reference Thomka2010; Thomka et al., Reference Thomka, Lewis, Moscher, Pabian and Holterhoff2011). The crinoids in the Barnsdall Formation were preserved largely via rapid burial from distal storm events in an area that essentially lacked background sedimentation. In such deposits, burial allows organisms to be shielded from natural processes that actively degrade them. Rapid burial by storm events heightens the chances of exceptional fossil preservation because the organism is protected from scavenging and destruction by macro- and microorganisms due to the depth and anaerobic conditions (McMahon et al., Reference McMahon, Anderson, Saupe and Briggs2016; Muscente et al., Reference Muscente, Schiffbauer, Broce, Laflamme and O'Donnell2017; Parry et al., Reference Parry, Smithwick, Nordén, Saitta, Lozano-Fernandez, Tanner, Caron, Edgecombe, Briggs and Vinther2018).
Figure 1. Map of the location of the Barnsdall Formation (black square), a crinoid-bearing Lagerstätte near Copan, Oklahoma, USA (modified from Thomka et al., Reference Thomka, Lewis, Moscher, Pabian and Holterhoff2011).
The Barnsdall Formation has yielded more than 1,000 cladid crinoid fossils across a number of species and genera, providing a rare look into Pennsylvanian crinoid diversity. While many of these specimens are preserved as simple cups, there are a number of complete crowns from a full ontogenetic range. In this study, we examine one such ontogenetic range from Erisocrinus typus Meek and Worthen, Reference Meek and Worthen1865 (Fig. 2), a Pennsylvanian cladid crinoid with a dicyclic cup, mild basal concavity, smooth cup surface, and small, circular stem facet (Sheffield, Reference Sheffield2013). As noted in the preceding (Ubaghs, Reference Ubaghs and Moore1978; Thomka et al., Reference Thomka, Mosher, Lewis and Pabian2012), cladid crinoids are less likely to be fossilized due to their weak suturing, but Erisocrinus has a significantly higher preservation potential compared with other cladid crinoids. This is shown in studies performed at the genus level using bulk samples of the Wann and the Barnsdall formations (Lewis, Reference Lewis1986; Thomka, Reference Thomka2010). Higher preservation potential, combined with ideal preservation conditions, has yielded a series of 10 crowns belonging to Erisocrinus recovered from the Barnsdall Formation (Oklahoma, USA), which provides insight into the ontogeny of late Paleozoic crinoids that are rarely found in high enough numbers to study in such detail. It is notable that the series includes an ontogenetic sequence with multiple juvenile specimens, which are even less common than the typical cladid specimen, considering their small size, thin plates, and typically poorly sutured calyx plates (Strimple, Reference Strimple1977; Ausich and Göncüoglu, Reference Ausich and Göncüoglu2020).
Figure 2. Growth series of Erisocrinus typus. The fossils are organized from most juvenile (1) to adult (10). In its juvenile stage, E. typus (1, 2) had uniserial brachial plates and a rounded cup; as the crinoid matured, the brachial plates became biserial and the infrabasal plates became invaginated, which are obscured from view in these specimens due to lateral compaction of the theca. Specimens whitened with ammonium chloride sublimated. (1) UNSM 36189. (2) UNSM 36190. (3) UNSM 36191. (4) UNSM 36192. (5) UNSM 36193. (6) UNSM 36194. (7) UNSM 36195. (8) UNSM 36196. (9) UNSM 36197. (10) UNSM 36198. Scale bars = 10 mm.
Background
Barnsdall Formation
The Upper Pennsylvanian (Missourian) Barnsdall Formation is exposed in northeastern Oklahoma near the small town of Copan in Washington County (36°55′24.58″N, 95°54′56.51″W; Fig. 1). The Barnsdall Formation, with its exceptional preservation of the delicate, multi-element crinoid skeletons, allows for unique insight into the variability of crinoids at low taxonomic levels. The 10 crinoid specimens studied in this paper were retrieved from a mudstone-dominated interval measuring approximately 50 cm in thickness (Thomka, Reference Thomka2010). This interval's paleoenvironment is characterized by muddy substrates, oxygenated bottom waters, and slow sedimentation rates (Holterhoff, Reference Holterhoff1997; Lewis et al., Reference Lewis, Holterhoff, Mosher and Pabian1998; Thomka et al., Reference Thomka, Lewis, Moscher, Pabian and Holterhoff2011). After rapid burial from obrution events (Thomka et al., Reference Thomka, Lewis, Moscher, Pabian and Holterhoff2011), many crinoids within the unit were also preserved through post-depositional compaction, which encapsulated these crinoid communities into sequential layers.
Within the Barnsdall Formation, the majority (approximately 91%) of the preserved crinoids are cladids and within that area a number of cladid genera, dominated by Erisocrinus, Apographiocrinus, Stellarocrinus, Stenopecrinus, Galateacrinus, and Exocrinus (Thomka et al., Reference Thomka, Lewis, Moscher, Pabian and Holterhoff2011). Taphonomic processes can help explain both the distribution of each of these genera (i.e., how commonly each of them is preserved) and the likelihood of their complete preservation. While a full description of the genus-level taphonomic variation can be found in Thomka et al. (Reference Thomka, Lewis, Moscher, Pabian and Holterhoff2011), the major controls can be explained first by the flexibility the cup would have had during life and second by the type of compaction it experienced. Genera with more tightly sutured cups would likely have rotated slightly during compaction (oblique compaction). The rotation would have allowed the cup to have been preserved, commonly unaltered, but would have caused a separation of the cup from the arms and subsequent loss of the arm. In contrast to that, those genera with more flexible suturing between the thin cup plates, such as Erisocrinus, were more often found laterally compacted, parallel to the long axis of the crown, which resulted in a greater possibility of arm-plate retention (Thomka, Reference Thomka2010; Thomka et al., Reference Thomka, Lewis, Moscher, Pabian and Holterhoff2011). This lateral compaction allows the study of ontogenetic trends as the majority of plates and arms are well preserved and not distorted in two dimensions, although measurements involving cup width are unreliable due to cup distortion during compaction.
Previous studies concerning cladid ontogeny
There are few studies concerning the ontogeny of cladid crinoids from the Middle or Late Pennsylvanian (Peters and Lane, Reference Peters and Lane1990), and many of them are limited by a lack of specimens from the smallest sizes (Strimple, Reference Strimple1977). While studies on cladids have generally been more limited, some ontogenetic studies have been published over the past 50 years (e.g., Strimple, Reference Strimple1977; Pabian and Strimple, Reference Pabian and Strimple1979; Lewis and Strimple, Reference Lewis and Strimple1990; Peters and Lane, Reference Peters and Lane1990; Ausich and Wood, Reference Ausich and Wood2012). These studies provided a range of qualitative and quantitative growth studies. Strimple (Reference Strimple1977) described rare juvenile specimens of Pennsylvanian crinoids in the genus Stenopecrinus, where even an extremely limited number of specimens showed clear differential rates of growth in plates of the cup. Pabian and Strimple (Reference Pabian and Strimple1979) found that Cibolocrinus conicus Strimple, Reference Strimple1951 showed clear anisometric change in the shape of the cup as it grew, with some changes in the number of plates in the circlets. Lewis and Strimple (Reference Lewis and Strimple1990) qualitatively described ontogenetic changes in the shape of the cup and in arm branching patterns in Sciadiocrinus. Peters and Lane (Reference Peters and Lane1990) performed an ontogenetic study of a series of five moderately well-preserved Erisocrinus typus specimens from the Millersville Limestone of eastern Illinois, USA (although the arms were incomplete). Through their analysis, Peters and Lane (Reference Peters and Lane1990) concluded that E. typus grew with virtually no change in the shape of either the plates of the cup or the cup itself (i.e., it grew isometrically), with the exception being the arms, which grew much taller first and then widened later. Peters and Lane (Reference Peters and Lane1990) also found that Apographiocrinus grew in a similar manner. Other work found that cladid species grew with a combination of allometry and isometry, with the isometry being limited to the plates of the cup and allometry in the feeding arm structures, such as in the Mississippian crinoid Hypselocrinus hoveyi (Ausich and Wood, Reference Ausich and Wood2012).
Materials and methods
Materials
The specimens of Erisocrinus typus discussed here are part of a larger group of 1,200 specimens of cladid crinoids collected from the middle portion of the Barnsdall Formation (Pabian et al., Reference Pabian, Mosher, Lewis and Holterhoff1995). The growth series comprises 10 well-preserved crowns and ranges from juvenile (1.0 cm in height) to adult (7.6 cm in height) (Fig. 2).
Methods
Both sides of each Erisocrinus typus specimen were used in this study. Each side was whitened using ammonium chloride sublimated to highlight plate suture boundaries and then photographed with scale using a Nikon D850 camera. Images of each specimen were imported into ImageJ (Rasband, Reference Rasband2016); units were scaled to match the scale bar in the photograph before any measurements were taken to ensure consistency between measurements. The measurement parameters were determined on the basis of the maximum distance between the top and bottom, for height, and the maximum width possible for each plate of the cups and of the arms (Fig. 3). Only those plates that were complete and nondistorted were used in this study; due to lateral compaction, cup width was not a reliable measurement, and some radial and basal plates that sit on the sides of the cup could not be reliably measured. Due to the basal concavity in adult specimens of Erisocrinus, the infrabasals and the stem facet diameter were also not available for measurement as the lateral compaction caused distortion in the majority of the specimen's infrabasal plates. In addition, due to taphonomic features such as jumbling of the plates and loss of the distal tips of the arms (common taphonomic patterns documented by Thomka et al., Reference Thomka, Lewis, Moscher, Pabian and Holterhoff2011), some plates of the arms were also not measurable. The measurements taken include the following: the length and width of basal and radial plates; primibrachial length and width; brachial length, width, and area; and arm width and length (see Supplemental Material for all measurements).
Figure 3. Measurement parameters for each plate as done in this study. Line drawing is based on UNSM 36193). (1) Basal plate width. (2) Basal plate height. (3) Radial plate width. (4) Radial plate height. (5) Primibrachial height. (6) Primibrachial width. (7) Secundibrachial height. (8) Secundibrachial width. (9) Arm width. (10) Arm length. Modified from Sheffield (Reference Sheffield2013).
The averages of the radial, basal, primibrachial, and secundibrachial plates for each specimen were used to measure allometric growth. We used a Reduced Major Axis (RMA) model in the software PAST (Hammer et al., Reference Hammer, Harper and Ryan2001, Reference Hammer, Harper and Ryan2006), applied to the log-transformed data of the averaged measurements.
Repository and institutional abbreviation
All specimens for this study are reposited at the University of Nebraska State Museum (UNSM).
Results
Here we report statistics related to the growth of the basal, radial, primibrachial, and secundibrachial plates to determine whether there are changes in the proportions of the morphological features of the specimens through ontogeny. Following Ausich and Wood (Reference Ausich and Wood2012), we report the following statistics: the correlation coefficient r2; the probability of no correlation (p(uncorr.)), the probability of no correlation based on a permutation test (permut p); and the probability that the slope of the line is one (p(a) = 1). We use these statistics to differentiate isometric (a slope of one) from allometric growth patterns and determine whether allometric growth is positive (a slope greater than one) or negative (a slope less than one).
Due to compaction and disarticulation, changes in the cup width and growth of the infrabasals could not be measured in this study. However, we can clearly see the cup outline change from a shape with a rounded bottom to a cup that is bowl shaped with basal concavity (Fig. 4). This is a common anisometric change within cladid crinoid growth (e.g., Mirantsev and Arendt, Reference Mirantsev and Arendt2012).
Figure 4. A simplified outline of five benchmark specimens (as imaged in Fig. 2.1, 2.2, 2.5, 2.8, 2.10) of the growth series of E. typus. Note the shape change of the primibrachial plates, which are taller than wide in juvenile stages and become wider than tall in the adult stages, likely to support the increased weight of the arm. The arms also transitioned from uniserial to biserial from juvenile to adult. Shape changes of the plates of the cup (i.e., the basal and radial plates) is subtle.
We find that E. typus grew anisometrically in both the plates of the cup and in the arm structures, with a mixture of positive and negative allometric growth; the RMA analysis indicates that these results are significant and clearly distinguishable from isometric growth in nearly all of the measurements (Table 1).The basal plate width and height grew with positive allometry with respect to the height of the aboral cup. The basal plate width grew with slightly negative allometry with respect to basal plate height. The radial plate height and width grew with slight positive allometry with respect to cup height. The radial height grew with slight positive allometry with respect to radial width. The slight allometric growth means that the shape change of the overall plates is subtle (Fig. 4). All of these measurements are statistically significant, indicating that the growth is very unlikely to be isometric (Table 1).
Table 1. Results from the RMA analysis in PAST. H = height; W = width; L = length; RP = radial plate; Cu = cup; BP = basal plate; PB = primibrachial plate; SB = secundibrachial plate; AR = arm.
In each of the specimens, one of the primibrachials is taller than the others in the cup. This taller primibrachial is interpreted as belonging to the A ray, which was added first in other related crinoids (Peters and Lane, Reference Peters and Lane1990) and is therefore larger. Study of the specimens shows that the primibrachial plates grew in height faster than in width in young crinoids and then grew more wide than tall as the crinoid aged (Fig. 4). The growth of the primibrachial plate height and width as compared with the cup height is significantly anisometric; the primibrachial height grew with negative allometry with respect to the cup height, and the width grew with positive allometry. The growth of the primibrachial width with respect to primibrachial height indicates positive allometric growth, and this is statistically significant.
The secundibrachials began as uniserial in the most juvenile specimen and became biserial as the crinoid aged (Fig. 4). The first secundibrachial height grew with negative allometry with respect to cup height. The first secundibrachial width grew with positive allometry with respect to cup height. Both of these results are statistically significant. The first secundibrachial width with respect to the first secundibrachial height grew with positive allometry but is statistically insignificant and may not be distinguishable from isometric growth.
The total arm length also grew with positive allometry and changed from approximately four times to eight times the cup height. Arm width grew with negative allometric growth with respect to cup height.
Discussion
Previous studies of cladid crinoids, including Erisocrinus typus, have been limited due to the small number of well-preserved specimens (Lewis and Strimple, Reference Lewis and Strimple1990), especially in juvenile samples; this means that many growth studies that have been performed have not been able to utilize a substantial ontogenetic sequence. Peters and Lane (Reference Peters and Lane1990) conducted a similar study to the one presented here on a smaller growth series of E. typus from five specimens of the Millersville Limestone of eastern Illinois, USA. They concluded that the plates of the cup in E. typus grew isometrically, and the primibrachials of the arms grew anisometrically. However, with the broader range of ontogenetic stages in this study, the interpretation of E. typus growth changes. With the addition of more juvenile specimens, which were unavailable in the Peters and Lane (Reference Peters and Lane1990) study, the data show that the growth of the plates in both the cup and arms was anisometric. The plates of E. typus exhibited a mixture of positive allometric growth strategies, which is a similar growth strategy noted in other cladid crinoids and some disparid crinoids (Strimple, Reference Strimple1977; Peters and Lane, Reference Peters and Lane1990; Ausich and Wood, Reference Ausich and Wood2012).
The primibrachial plates grew anisometrically, with the height and width increasing at different rates, indicating both negative and positive allometry, respectively. The primibrachials in the youngest specimens of E. typus are much higher than wide at first and then become much wider than tall through the ontogenetic sequence. This growth strategy is likely related to its paleoecology and possible evidence that the species described here could have employed limited mucus-net feeding (Ausich, Reference Ausich1980). Peters and Lane (Reference Peters and Lane1990) hypothesized that this pattern could be related to the establishment of the filtration fan mode; by having the height become established more quickly, this would allow for faster gains in the volume of water that the arms would have been able to filter. Later, the width increased, likely for higher strength of the arm. The fact that E. typus arms also shift from uniserial to biserial could be an indication of increasing surface area for greater feeding structures through growth. Growth patterns such as these have been documented in other late Paleozoic cladids as well (Peters and Lane, Reference Peters and Lane1990; Ausich and Wood, Reference Ausich and Wood2012). This shift from uniserial to biserial arm elements has implications for understanding skeletal element origins and homologies, as well (Sumrall et al., Reference Sumrall, Sheffield, Bauer, Thompson and Waters2023). Early crinoid arms are composed of axial floor plates and extraxial brachial elements (Guensburg et al., Reference Guensburg, Blake, Sprinkle and Mooi2015); however, in more-derived crinoids, such as Erisocrinus, the axial plates are lost. When the extraxial arm elements become biserial, they mimic the ocular plate rule (where plates are added at the growing tip of a plate series, immediately proximal to a terminal ossicle or ocular plate; this type of terminal growth is typically recognized as evidence for presence of axial skeleton) and become nearly indistinguishable from axial skeleton (Kammer et al., Reference Kammer, Sumrall, Zamora, Ausich and Deline2013). This indicates that the definitions of axial and extraxial skeleton in echinoderms, typically treated as separate entities, may be more complex (Sumrall et al., Reference Sumrall, Sheffield, Bauer, Thompson and Waters2023).
The total arm length also exhibits positive allometry: the arm length increases from four times the cup height in the juvenile specimens to nearly eight times in the adult specimens. The increase in width occurs far less dramatically, and the width of the arm maintains relatively similar proportions from juvenile to adult. While the change in width is less dramatic, it does indicate, as Peters and Lane (Reference Peters and Lane1990) also stated, that individuals of E. typus may have fed on slightly differently sized food particles, and juveniles and adults were likely not in direct competition with one another.
Similar patterns of arm growth can be found in different cladid taxa across the early and later Paleozoic; in particular, one pattern that can be noted, shared between Erisocrinus typus and some Ordovician crinoids, is in the growth pattern of the first arm plate. Brower (Reference Brower2007) noted that in the Middle Ordovician cladid Cupulocrinus plattevillensis Kolata, Reference Kolata1975 that the width of the primibrachials exhibited positive allometric growth with respect to the height of the primibrachials, a pattern also seen in the growth of the primibrachials of E. typus, as discussed. Similar growth trajectories are also uncovered in the positive allometric growth observed in arm length throughout ontogeny (Brower, Reference Brower1992), as seen in E. typus and in Ordovician cladids, such as Cupulocrinus crossmani Brower, Reference Brower1992 and Praecupulocrinus conjugans (Billings, Reference Billings1857). These growth patterns, shared between crinoids that had quite different morphologies (e.g., C. crossmani has branching arms, unlike E. typus), can likely provide further study into paleoecological trends in evolutionary history. Unfortunately, without complete stems of E. typus in the growth series presented in this study, full comparisons of how these crinoids across ontogenetic stages and geologic time may have subdivided niches in the water column cannot be fully explored at this time.
Quantifying the growth of crinoids can inform us of the feeding strategies that these organisms may have used. Research has shown that different arm morphologies can shed light on niche differentiation and community structures (e.g., Ausich, Reference Ausich1980; Kitazawa et al., Reference Kitazawa, Oji and Sunamura2007; Baumiller, Reference Baumiller2008; Cole et al., Reference Cole, Wright and Ausich2019), which can certainly be used to better explore evolutionary paleoecological questions (Macurda, Reference Macurda1968; Lamsdell, Reference Lamsdell2021). In this study of the ontogeny of E. typus, we find that arms grew taller first and then wider, likely to increase its food gathering surface first and then wider to support the arm structure. The change in width of the arms also indicates that there was possibly some niche differentiation, and thereby reduced competition, in food resources, where juveniles and adults of E. typus may have preferentially accepted different sizes of food particles.
Conclusion
Lack of a detailed, well-preserved growth series of crinoids hampers our ability to fully quantify the growth trajectories used by extinct organisms. Juvenile specimens, which are less commonly preserved, add important information about these growth trajectories. A pristine growth series of Pennsylvanian-age Erisocrinus typus from the Barnsdall Formation (Oklahoma, USA) is an example of how adding new fossil data from a broad ontogenetic range can change interpretations of their growth patterns. Earlier studies of E. typus found that the plates of the cup grew isometrically; by contrast, this study shows that the cup grew anisometrically with a combination of positive and negative allometry. The arms of E. typus, whose arm elements begin as uniserial and transition to biserial, increased in height at a rate far faster than the increase in width, which is an indication that the growth pattern would have allowed quicker establishment of a food-gathering surface and then a subsequent width increase to support the weight of the arm itself, a pattern seen in other crinoids. The change in width of the arms also indicates that there was possibly some niche differentiation, and thereby reduced competition, in food resources, where juveniles and adults of E. typus may have preferentially accepted different sizes of food particles. Many of these growth patterns are also seen in earlier Paleozoic cladid crinoids, as well. Ontogenetic data such as this can be added to the growing conversations of crinoid paleoecology and to studying overall phylogenetic ontogenetic and paleoecological trends in Paleozoic crinoids.
Acknowledgments
We thank R. Diffendal and G. Corner at the University of Nebraska State Museum for access to specimens. These specimens were originally collected by D. Mosher. Helpful comments on earlier drafts of this work were made by J. Bauer, B. Deline, L. Zachos, J. Bright, and D. King. We thank S. Zamora, J. Botting, V. Syverson, and an anonymous reviewer for their comments that improved this paper. This study was partially funded by a Geological Society of America student research grant awarded to S. Sheffield.
Declaration of competing interests
The authors declare none.
Data availability statement
All measurements of the specimens can be found in Supplementary Material 1. Alternative text of images can be found in Supplementary Material 2. Supplementary material available from the Dryad Digital Repository: http://doi.org/10.5061/dryad.h18931zrx.
Open access
