Non-technical Summary
Subadult shells of several Paleozoic brachiopod species were examined. Structures of the shells show that the species studied consumed plankton in the water column, which differs from modern brachiopods that subsist on nutrients from the yolk sac in their egg. One species from Baffin Island, Canada, had a particularly large subadult shell, indicating that it spent a long time in the water before settling. It may have needed this extra time to colonize the newly opened marine ecosystem on what is now Baffin Island after a period of sea level rise. The fact that fossil brachiopods developed differently than modern ones shows that one cannot always assume that the present is a good analogue for the past.
Introduction
Brachiopods have a sessile adult stage; therefore, dispersal occurs entirely within the pelagic subadult phase. For this reason, understanding this pelagic life stage is crucial to understanding brachiopod ontogeny, dispersal, and biogeographic distribution. The small, primarily soft-bodied subadults do not readily fossilize, but the first-formed (subadult) shell is often visible in the umbonal region and in longitudinal sections of well-preserved adult shells. The study of the remnants of this first-formed shell has led to many advances in our understanding of the development of fossil brachiopod lineages including the linguliformeans (Baliński, Reference Baliński1997; Freeman and Lundelius, Reference Freeman and Lundelius1999; Popov et al., Reference Popov, Bassett, Holmer and Ghobadi Pour2009; Ushatinskaya, Reference Ushatinskaya2016; Zhang et al., Reference Zhang, Popov, Holmer and Zhang2018), craniiformeans (Popov et al., Reference Popov, Skovsted and Zuykov2010, Reference Popov, Bassett and Holmer2012), and rhynchonelliformeans (Freeman and Lundelius, Reference Freeman and Lundelius2005, Reference Freeman and Lundelius2007; Popov et al., Reference Popov, Egerquist and Holmer2007; Madison, Reference Madison2009; Bassett and Popov, Reference Bassett and Popov2017; Madison and Kuzimina, Reference Madison and Kuzmina2020).
Study of fossil brachiopod development is complicated by a history of inconsistent terminology, although attempts have been made to stabilize this terminology by Williams et al. (Reference Williams, Brunton and Carlson1997) and more recently by Madison and Kuzmina (Reference Madison and Kuzmina2020). Many of these inconsistencies are due to disagreement on the distinction between the larval and juvenile stages. After fertilization of the egg, the brachiopod embryo develops within a fertilization membrane and the puncturing of this membrane is considered the point at which an embryo becomes a larva (Williams et al., Reference Williams, Brunton and Carlson1997). The larval stage was defined by Williams et al. (Reference Williams, Brunton and Carlson1997) to be the entire pelagic stage of the brachiopod life cycle, and the juvenile as the early settled stage that undergoes metamorphosis. Madison and Kuzmina (Reference Madison and Kuzmina2020) define a true larval stage as lacking a shell, and a shelled pelagic stage as a juvenile, with the organism becoming an adult when it settles and metamorphoses. In this conception, brachiopod groups such as modern lingulides, which emerge from the fertilization membrane with a shell already formed, lack a true larval stage (Zhang et al., Reference Zhang, Popov, Holmer and Zhang2018; Madison and Kuzmina, Reference Madison and Kuzmina2019; Madison et al., Reference Madison, Kuzmina and Temereva2021). Groups such as modern rhynchonelliformeans, which only begin to biomineralize a shell after settling on a substrate, lack a juvenile stage in this classification scheme (Madison et al., Reference Madison, Kuzmina and Temereva2021).
This disagreement on the division of life stages has implications for the terminology that describes the parts of the first-formed shell because the terms are related to the growth stage in which each part formed. The protegulum is consistently defined as the initial shell; it lacks growth markings because the whole protegulum is secreted by the mantle simultaneously rather than in intervals as the shell grows. The protegulum is surrounded by the brephic shell during the juvenile stage. It may form either in the pelagic stage or after settlement depending on the definition of the juvenile stage used. In work that considers the shelled pelagic stage to be the larval stage (e.g., Williams et al., Reference Williams, Brunton and Carlson1997; Freeman and Lundelius, Reference Freeman and Lundelius2005, Reference Freeman and Lundelius2007), any shell growth that happens in the pelagic larval stage is referred to as the larval shell or larval protegulum; shell growth that happens upon settling but before metamorphosis is the brephic shell. In papers where the shelled pelagic stage is considered to be the juvenile stage (e.g., Madison and Kuzmina, Reference Madison and Kuzmina2019, Reference Madison and Kuzmina2020), this stage of shell growth is the brephic shell. The present study follows the terminology of Madison and Kuzmina (Reference Madison and Kuzmina2020).
Regardless of which mode of life the brephic shell is thought to have formed in, the protegulum and brephic shell together comprise the first-formed shell. In some groups, such as lingulides, the protegulum and brephic shell are separated by a pronounced growth line (Madison et al., Reference Madison, Kuzmina and Temereva2021). However, these stages are more difficult to distinguish in many rhynchonelliformeans that lack such a boundary. Previous work has noted a difference in the microstructure of first-formed and adult shells in strophomenides (Madison and Kuzmina, Reference Madison and Kuzmina2020), but this has not been studied in other rhynchonelliformeans. The term “metamorphic shell” is sometimes used to refer to the subadult shell up until metamorphosis into an adult, making it equivalent to the first-formed shell (Bassett and Popov, Reference Bassett and Popov2017).
The life cycles of brachiopods and their corresponding first-formed shell growth patterns vary (Madison et al., Reference Madison, Kuzmina and Temereva2021; Malakhov et al., Reference Malakhov, Kuzmina and Madison2021). Lingulides and discinides (linguliformean brachiopods) are thought to be planktotrophic during their larval stage based on modern studies (Collin et al., Reference Collin, Venera-Pontón, Driskell, Macdonald and Boyle2018), although Baliński (Reference Baliński1997) showed that modern lingulides may have had different patterns of early development from fossil lineages. Modern rhynchonelliformean brachiopods have an entirely lecithotrophic (non-feeding) larval stage and only develop a shell upon metamorphosis into an adult (Chuang, Reference Chuang1996; Kuzmina, Reference Kuzmina2021). Because there is no true juvenile stage, the portion of shell that might be termed the brephic shell is biomineralized simultaneously with the protegulum, therefore the two cannot be distinguished (Madison et al., Reference Madison, Kuzmina and Temereva2021). The first-formed shells in these extant groups are generally less than 0.25 mm in width, a measurement chosen based on egg sizes of extant brachiopods (Freeman and Lundelius, Reference Freeman and Lundelius2005).
Conversely, in modern lingulides, the protegulum is formed in the embryonic stage and the brephic shell begins to grow after puncture of the fertilization membrane (Madison et al., Reference Madison, Kuzmina and Temereva2021; Malakhov et al., Reference Malakhov, Kuzmina and Madison2021). There is a distinct boundary between the protegulum and brephic shell in this group and the first-formed shell is larger, greater than 0.25 mm. Modern discinides also have a large first-formed shell; these brachiopods have both a larval stage with a protegulum, which lacks growth lines and is biomineralized simultaneously across the entire cuticle of the mantle, and a juvenile stage with a brephic shell, which has growth lines indicating a shift to shell growth at the anterior edge of the mantle. Radial ornamentation (i.e., ribs) first forms in the adult stage (Fig. 1). These modern groups serve as examples of how the brachiopod life cycle is preserved on the first-formed shell, therefore they provide guidelines for examining the first-formed shells of fossil brachiopods.
Simplified line drawing of a brachiopod dorsal valve showing idealized differences in ornamentation among protegulum (no ornamentation), brephic shell (growth lines only), and adult shell (both growth lines and radial ornamentation). Both the protegulum and brephic shell are included in the first-formed shell.
The size and structure of the first-formed shell can also provide some insight into the life cycles of fossil brachiopods. Freeman and Lundelius (Reference Freeman and Lundelius2005) measured the first-formed shells of many fossil species and compared them in size to modern brachiopods to determine whether different extinct brachiopod lineages were planktotrophic or lecithotrophic. Lecithotrophic brachiopod larvae depend wholly on the yolk of the egg for their nutrition, so are constrained in how much they can grow in their larval stage, producing only a small first-formed shell before metamorphosis into an adult. Planktotrophic larvae and juveniles, on the other hand, are not so limited given that they can feed within the water column and grow to a larger size before settling. This also allows for greater variation in the size of the first-formed shell within a species (Freeman and Lundelius, Reference Freeman and Lundelius2007). Whether the protegulum and brephic shell are distinct from each other informs whether there is a major change during development, such as metamorphosis from a lecithotrophic larva into a planktotrophic juvenile as in discinides, or development from a shelled embryo directly into a juvenile as in lingulides (Madison et al., Reference Madison, Kuzmina and Temereva2021). The broad scope of the Freeman and Lundelius (Reference Freeman and Lundelius2005) study was informative but did not focus on individual groups, so more detailed analysis of individual brachiopod lineages is warranted.
The development of orthide larvae remains unclear, despite orthides being one of the most common brachiopod orders of the early Paleozoic (Freeman and Lundelius, Reference Freeman and Lundelius2005; Madison, Reference Madison2009). Madison et al. (Reference Madison, Kuzmina and Temereva2021) suggested that many types of Paleozoic brachiopods, including orthides, had true planktotrophic larvae and only began biomineralizing a shell after settlement and lack distinctive protegula and brephic shells, but noted preserved impressions of larval setal sacs, which they considered indicative of planktotrophy. Orthides are among the earliest and most primitive of the rhynchonellate brachiopods but diversified considerably during the Great Ordovician Biodiversification Event (GOBE) (Harper et al., Reference Harper, Popov and Holmer2017; Stigall et al., Reference Stigall, Edwards, Freeman and Rasmussen2019) so it would be reasonable to expect some variability in life cycle within this group. This study focuses on one of the most prominent families of orthides in the Ordovician of North America, the Dalmanellidae.
The Dalmanellidae were found around the world in the Ordovician. They were common in both in equatorial intracratonic tropical basins and carbonate platforms and in the pericratonic basins in eastern North America (Jin, Reference Jin2012). Several lineages emerged and can be differentiated primarily on the basis of the size and distribution of their punctae, the size and shape of their cardinal processes, and the shape of their muscle scars. The present study focuses on the genera Cincinnetina Jin, Reference Jin2012; Diceromyonia Wang, Reference Wang1949; and Paucicrura Cooper, Reference Cooper1956; which represent one such lineage (Jin and Bergström, Reference Jin and Bergström2010; Jin, Reference Jin2012). Freeman and Lundelius (Reference Freeman and Lundelius2005) examined dalmanellid first-formed shells, including Cincinnetina meeki (Miller, Reference Miller1875) (there listed as Onniella Bancroft, Reference Bancroft1928), Diceromyonia storeya (Okulitch, Reference Okulitch1943), and Paucicrura corpulenta (Sardeson, Reference Sardeson1890).
The objective of this study is to quantify and describe the morphology of the first-formed shells of some of the most common North American dalmanellids. Detailed measurements of both the first-formed shell stages and the fully grown shells can provide insight into the development of this common and widespread brachiopod lineage. This could have implications for our understanding of brachiopod dispersal and, by extension, paleobiogeography.
Materials and methods
Measured specimens are detailed in Table 1. Species measured include: Cincinnetina multisecta (Meek, Reference Meek1873), Diceromyonia storeya (Okulitch, Reference Okulitch1943), Diceromyonia tersa (Sardeson, Reference Sardeson1890), Paucicrura corpulenta (Sardeson, Reference Sardeson1890), Paucicrura rogata (Sardeson, Reference Sardeson1890), and Paucicrura sillimani (Roy, Reference Roy1941). Specimens of Cincinnetina meeki (Miller, Reference Miller1875) were examined but not measured. Taxonomic assignments of specimens from collections have been updated to conform to current nomenclature, but no detailed reassessment of the taxonomy of this lineage was undertaken for this study.
Species and provenance of specimens measured.
Specimens were examined under a stereo microscope. First-formed shells were distinguished based on shell ornamentation in that the first-formed shell was presumed to lack the radial ornamentation of the adult shell (Figs. 1, 2). On specimens in which the tips of the umbonal regions were visible and undamaged, length and width of first-formed shells of both valves were measured using the Olympus CellSens imaging software (v. 3.2). First-formed shells were discernible on at least one specimen of all species examined, except Cincinnetina meeki, of which the three specimens examined all had abraded posterior regions.
Dorsal and ventral first-formed shell of Paucicrura sillimani (Roy, Reference Roy1941), with length (vertical line) and width (horizontal line) measurements shown.
Either type specimens (when available) or specimens of each species with well-preserved first-formed shells were selected for photos and prepared using a tungsten carbide needle and water. Specimens were coated with ammonium chloride and photographed using the CellSens microscope software.
Two specimens each of D. storeya and P. rogata were selected for lateral sectioning. Specimens were ground to the midline using 320-mesh carborundum powder. The polished surface was treated with dilute HCl before being covered in acetone and then acetate film. This created a reproduction of the shell in cross-section. Acetate peels were made and photographed under a light microscope to examine internal structure of specimens.
Repositories and institutional abbreviations
Types, figured, and other specimens examined in this study are deposited in the following institutions: the Cincinnati Museum Center (CMC), Cincinnati, USA; the Field Museum of Natural History (FMNH), Chicago, USA; the Geological Society of Canada (GSC), Ottawa, Canada; the Manitoba Museum (MM), Winnipeg, Canada; and the Royal Ontario Museum (ROM), Toronto, Canada.
Results
Dorsal and ventral first-formed shell widths differed on most specimens (Table 2; Fig. 3). The single largest first-formed shell (dorsal width of 1.36 mm) belonged to P. sillimani, and the smallest first-formed shell (dorsal width 0.12 mm) belonged to C. multisecta. Paucicrura sillimani and C. multisecta also have the largest and smallest average dorsal first-formed shell widths, respectively. All species except for P. sillimani had average dorsal first-formed shell widths less than 0.5 mm and more than 0.25 mm, although some individuals had measurements outside this range.
Mean and Median first-formed shell measurements of species examined. VW = ventral width; DL = dorsal length; DW = dorsal width. All measurements in millimeters.
Bivariate plot comparing dorsal and ventral width measurements, in millimeters, of first-formed shells. Linear regression through all datapoints indicated by dotted line.
Each species studied forms a cluster in bivariate plots based on the size of the first-formed shells (Fig. 3). The range in size of most species overlaps considerably, indicating similarly sized first-formed shells. Paucicrura sillimani has a consistently larger and more variable first-formed shell than other species in this study, while C. multisecta has a significantly smaller first-formed shell. Diceromyonia first-formed shells tend to be larger than those of Paucicrura and Cincinnetina, but the shells are also generally larger overall (Fig. 4). There is much less variation in the full (adult) width of all species examined in this study, including P. sillimani (Fig. 4).
Bivariate plot comparing adult width measurements and first-formed dorsal shell width measurements (both in millimeters). Polynomial regression through all datapoints indicated by dotted line.
On all specimens in which the features of the first-formed shell could be distinguished, the dorsal first-formed shell was more distinct from the surrounding shell than the ventral first-formed shell. The dorsal first-formed shell was elliptical in outline and slightly raised, and the ventral first-formed shell was higher and conical in shape. On most specimens of C. multisecta, D. storeya, D. tersa, P. corpulenta, and P. rogata (Figs. 5–9), the first-formed shell was only distinguishable by the lack of ornamentation. On all specimens of P. sillimani (Fig. 10) and on some well-preserved specimens of P. corpulenta and P. rogata, the protegulum, present as a raised median area on the dorsal first-formed shell, could be distinguished from the surrounding brephic shell. On P. sillimani, the protegulum appeared to be narrower at the mid-length and split into an anterior and posterior region.
Cincinnetina multisecta (Meek, Reference Meek1873) from the Cincinnatian at Cincinnati, Ohio. FMNH UC1099A. (1) Dorsal view; (2) posterior view; (3) posterior close-up showing first-formed shells. Arrow points to dorsal first-formed shell. Scale bars are (1, 2) 5 mm, (3) 0.5 mm.
Diceromyonia storeya (Okulitch, Reference Okulitch1943) from the Stony Mountain Formation, Gunn Member (Richmondian) at Stony Mountain, Manitoba. GSC 1362. (1) Dorsal view; (2) posterior view; (3) MM I-6276, posterior close-up showing first-formed shells. Arrow points to dorsal first-formed shell. Scale bars are (1, 2) 5 mm, (3) 0.5 mm.
Diceromyonia tersa (Sardeson, Reference Sardeson1890) from the Maquoketa Shale (Richmondian) at Spring Valley, Minnesota. CMC IP 88655A. (1) Dorsal view; (2) posterior view; (3) posterior close-up showing first-formed shells. Arrow points to dorsal first-formed shell. Scale bars are (1, 2) 5 mm, (3) 0.5 mm.
Paucicrura corpulenta (Sardeson, Reference Sardeson1890) from the Maquoketa Shale (Edenian–Richmondian) at Spring Valley, Minnesota. CMC IP 89840A. (1) Dorsal view; (2) posterior view; (3) posterior close-up showing first-formed shells. Arrow points to boundary of dorsal first-formed shell. Scale bars are (1, 2) 5 mm, (3) 0.5 mm.
Paucicrura rogata (Sardeson, Reference Sardeson1890) from the Verulam Formation (Chatfieldian) at Lake Simcoe, Ontario. ROM IP67553. (1) Dorsal view; (2) posterior view; (3) posterior close-up showing first-formed shells. Arrow points to dorsal first-formed shell. Scale bars are (1, 2) 5 mm, (3) 0.5 mm.
Paucicrura sillimani from Amadjuack Formation at Silliman's Fossil Mount (Edenian) on Frobisher Bay near Iqaluit, Nunavut. FMNH P28265. (1) Dorsal view; (2) posterior view. (3) GSC 143338 from GSC locality O-104516; posterior close-up showing first-formed shells. Larger arrow points to boundary of dorsal first-formed shell; smaller arrow points to boundary between protegulum and brephic shell. Scale bars are (1, 2) 5 mm, (3) 0.5 mm.
Internal shell structure
The first-formed shells of the dorsal valves are visible on all acetate peels, differentiated from later stages based on changes in the shell fabric (Figs. 11, 12). There is an abrupt change in the growth pattern of shell fibers between the first-formed shell and the adult shell. The fabric of the first-formed shell also differs in being granular, as opposed to the fibrous structure of the adult shell. The ventral first-formed shells are less apparent, but still visible in the peels of P. rogata and D. storeya.
Light-microscope photo of acetate peel taken from lateral section of Paucicrura rogata. ROM IP67554. C = cardinal process, DV = dorsal valve, FFS = first-formed shell, VV = ventral valve. (1) Photo without labels or overlay; (2) photo with shell sections labeled and given colored overlay.
Light-microscope photo of acetate peel taken from lateral section of Diceromyonia storeya. MM I-6277. C = cardinal process, DV = dorsal valve, FFS = first-formed shell, VV = ventral valve. (1) Photo without labels or overlay; (2) photo with shell sections labeled and given colored overlay.
The lengths of the first-formed shells measured through peels fit within the ranges of the external measurements (Table 3). Ventral valves measured on the peels were smaller than ventral valves measured externally, perhaps due to the difficulty of measuring their conical shape.
Length of first-formed shells measured on acetate peels of cross-sections.
Cross-sections of the shells in the acetate peels are less affected by abrasion and may be more accurate than external measurements or photographs in that they are true measurements of the dimensions of the shells and not subject to the difficulties of measuring a three-dimensional curved surface from a two-dimensional photograph. Acetate peels made in this manner may also be useful when examining lineages with less-prominent exterior expressions of this feature. However, the process destroys much of the shell, limiting the utility of this method when studying rare taxa or historical collections.
The granular nature of the first-formed shell likely reflects simultaneous biomineralization of the protegulum and brephic shell in the water column. This was suggested to explain the granular appearance of the pedicle sheath in the strophomenates (Madison and Kuzmina, Reference Madison and Kuzmina2020), although the sheath would have been formed by the pedicle lobe rather than the mantle lobe as the first-formed shell would have been. The onset of continuous biomineralization as the mantle lobe grew towards the anterior would be marked by the transition to fibrous shell biomineralization.
Sources of variation in measurements
The results here apparently show dorsal and ventral valves to be slightly different sizes on average (Fig. 3). This discrepancy may represent a real biological signal but also could be partially affected by the imperfect preservation of first-formed shells and the inaccuracy of making linear measurements of curved surfaces (especially in the case of the cone-shaped ventral shell). This should affect the length measurement most significantly due to the slight curve of the first-formed shell towards the anterior, but width measurement may also have been affected to a minor degree. However, the overall shell shape within this lineage is relatively consistent, which suggests that any interspecific variation represents real variation in the shell rather than inaccuracy introduced due to variations in convexity. This is especially the case for Paucicrura sillimani where the difference between it and other species is too significant to be explained by minor differences in shell shape.
The umbonal region of brachiopod shells is susceptible to abrasion during the life of the brachiopod, before burial, and after exhumation. Its location near the posterior makes first-formed shells susceptible to damage. Abrasion may obscure the point from the posterior at which ribs originate (where the onset of adult shell growth occurred). Given that this process would only increase the possible size of the first-formed shell, the measurement still provides an upper boundary for its size. The anomalously large first-formed shells of P. sillimani in particular were very well preserved, so this likely is not influencing our results to a large degree.
Despite the variation shown in the measurement data between dorsal and ventral valves, each species does cluster together in bivariate charts of first-formed shell width and length (Fig. 3). This is particularly true for C. multisecta, D. storeya, and P. rogata, including most measured specimens. This suggests that the variation from shell to shell within a collection is likely not significantly affecting the results in a way that would bias our conclusions. The application of 3-dimensional morphometric techniques could better account for the effects of shell curvature in future studies, but these techniques are not yet feasible for large datasets.
Discussion
Evidence for a planktotrophic juvenile stage
There is no correlation between the size of the measured species’ first-formed shells and the size of the adult shell either across species or within samples of the same species (Fig. 4). Thus, different factors must govern the growth of the first-formed shell and the adult shell.
Paucicrura sillimani, the species with the largest first-formed shell, has a mean dorsal first-formed shell width more than 0.5 mm greater than the next largest species, P. corpulenta (Table 2). Despite this, there is no significant morphological difference between adult P. sillimani shells and adult shells of the other species studied. The nature of the boundary between the protegulum and brephic shell of P. sillimani differed from other species as well in being more distinct, even when compared to the other species of Paucicrura examined (Fig. 10).
These differences in the size and structure of the first-formed shells suggest differences in the life cycles of the brachiopods. Paucicrura sillimani may have undergone a prolonged planktonic juvenile stage in comparison to other species within this lineage. Another possibility is that P. sillimani was capable of growing more rapidly in the water column during its juvenile stage in comparison to other species. Paucicrura corpulenta and P. rogata had smaller first-formed shells than P. sillimani, but the distinction between protegulum and brephic shell suggests that they also had planktotrophic juvenile stages, albeit shorter than those of P. sillimani. Other species seem to have lacked significant juvenile stages. Cincinnetina multisecta had the smallest first-formed shell on average, but it was still above the 0.25 mm length suggested by Freeman and Lundelius (Reference Freeman and Lundelius2005) to indicate planktotrophy. The lack of distinction between the protegulum and brephic shell suggests that this species only had a planktotrophic larval stage and lacked a juvenile stage.
Large first-formed shells have been identified in other lineages such as lingulides (Cherns, Reference Cherns1979; Baliński, Reference Baliński1997) where they likely indicated an exceptionally long planktonic larval stage. This interpretation is supported by the documented presence of lingulide larvae at bathyl and abyssal depths (Mileikovsky, Reference Mileikovsky1971) despite only one genus of discinide being known to live in the bathyl zone and modern lingulide brachiopods only being known from water depths of less than 47 m (Emig, Reference Emig, Williams, Brunton and Carlson1997). If the dalmanellids studied here have larger larval shells, they too must have had a longer planktonic larval period, although other factors such as food availability and water temperature can influence shell size (Freeman and Lundelius, Reference Freeman and Lundelius2005). The eventual adult size would have been controlled by other factors affecting the shell after it has settled, such as hydrodynamic energy, substrate, and nutrient availability at the settlement location (Gordillo et al., Reference Gordillo, Muñoz, Bayer and Malvé2018).
Paleobiogeographic work on brachiopods sometimes will invoke the lecithotrophy of modern rhynchonelliformeans to explain the generally endemic nature of Paleozoic rhynchonelliforms (e.g., Harper et al., Reference Harper, Rasmussen, Liljeroth, Blodgett, Candela, Jin, Percival, Rong, Villas, Zhan, Harper and Servais2013), but this likely was not the case for every lineage. Studies have shown that many fossil rhynchonelliformeans likely also had planktotrophic larvae (e.g., Popov et al., Reference Popov, Egerquist and Holmer2007; Bassett and Popov, Reference Bassett and Popov2017), and Baliński (Reference Baliński1997) underscored that caution should be taken when interpreting the development of fossil brachiopod lineages based on modern observations. A planktotrophic life cycle lacking a juvenile stage is now thought to be ancestral for orthides (Madison et al., Reference Madison, Kuzmina and Temereva2021), and that C. multisecta, D. tersa, and D. storeya, all shared this ancestral life cycle. In modern marine ecosystems, planktotrophy is more common in the tropics than lecithotrophy is (Valentine and Jablonski, Reference Valentine and Jablonski1983; Fernández et al., Reference Fernández, Astorga, Navarrete, Valdovinos and Marquet2009), so it follows that Paleozoic brachiopods that dominated the tropics (as in equatorial Ordovician Laurentia) would be more likely to have planktotrophic subadults if larval development is so variable, even within a single lineage as shown by the large larval shell of P. sillimani versus other species of Paucicrura.
Difference in size of first-formed shell between dorsal and ventral valves
The dorsal first-formed shell is consistently more readily discernable than the ventral first-formed shell in all species studied. This may have been due at least in part to a difference in shape because the dorsal valve is low, elliptical, and rounded, while the ventral valve is higher, conical, and thus more prominent in profile but less prominent when looking at the surface of the shell. The higher ventral valve would lead to subadults having a globular or cone-shaped silhouette as suggested for juvenile strophomenides (Madison and Kuzmina, Reference Madison and Kuzmina2020, fig. 9). This form is common in planktonic organisms (e.g., foraminifera, pteropods, and agnostids), perhaps reinforcing the idea that these brachiopods had significant planktonic life stages.
The unequal size of the first-formed shells may reflect an important aspect of the early development of dalmanellids. Brachiopod larvae typically possess a mantle lobe between an apical lobe and pedicle lobe during their planktonic phase (Williams et al., Reference Williams, Brunton and Carlson1997), but how these lobes develop during metamorphosis varies between groups. In modern terebratulides, thecideides, and rhynchonellides, the mantle lobe continues to grow posteriorly over the pedicle lobe during the planktonic phase before undergoing a reversal upon settling, where the mantle lobe folds over the apical lobe due to contraction of muscles that insert into the pedicle and mantle lobes (the brachiopod fold hypothesis of Cohen et al., Reference Cohen, Holmer and Lüter2003; see also Williams et al., Reference Williams, Brunton and Carlson1997, and Freeman and Lundelius, Reference Freeman and Lundelius2005). The protegulum then develops on the exterior surface of the mantle (that formed the interior prior to folding), with the pedicle emerging between the mantle lobes. The protegula in these groups are similar sizes, reflecting the common origin of each larval shell. The ancestors of modern brachiopod lineages are assumed to have developed the same way. Freeman and Lundelius (Reference Freeman and Lundelius2005) and Williams and Carlson (Reference Williams, Carlson, Williams, Brunton and Carlson2007) suggested that this was a plesiomorphic character to most of the Rhynchonellata, including ancient pentamerides, rhynchonellides, atrypides, and spiriferides that typically have small protegula of equal sizes.
Orthides and protorthides both have large protegula that likely grew from a mantle that, rather than folding, grew towards the anterior to envelop the apical lobe more like the Strophomenata creating protegula that are larger, but of unequal size of the dorsal and ventral valves (Freeman and Lundelius, Reference Freeman and Lundelius2005, Reference Freeman and Lundelius2007). This was explained by Freeman and Lundelius (Reference Freeman and Lundelius2007) as being the result of an extended planktotrophic period in the orthides in comparison to the early atrypide lineage that they examined that not only had a smaller, but generally less variable shell. Our results support their conclusions, although here we show that there can be significant variation in both shells in different species of even the same genus in different geographic regions. Where they found that the ventral valve tended to be larger in width than the dorsal valve, here we see the opposite in most species, with D. storeya having a consistently wider first-formed dorsal shell relative to the first-formed ventral shell. Perhaps this reflects differences in the development of different brachiopod lineages, even within a single brachiopod order.
Latitudinal trends in size of first-formed shells
Latitudinal gradients can be found throughout the modern living world, in both terrestrial and aquatic ecosystems. They can be seen in the modern global latitudinal diversity gradient, which has been established since the Miocene and shows an increasing number of taxa towards the tropics and away from the poles (Zhang et al., Reference Zhang, Song, Zhang, Wang, Su, Huang, Meng and Li2022; Fenton et al., Reference Fenton, Aze, Farnsworth, Valdes and Saupe2023). Latitudinal effects also can be seen within lineages, such as changes in the size of individuals of the same species shifting with latitude (e.g., Chauvaud et al., Reference Chauvaud, Patry, Jolivet, Cam and Le Goff2012). This type of gradient also has been reported in the fossil record, such as in the changing sizes at settlement of Pliocene bivalves in Japan (Kazushige and Zushi, Reference Kazushige and Zushi1988).
The dalmanellids studied show a gradient in larval shell size that varies with latitude (Figs. 13, 14). Other than the outlier P. sillimani, the average first-formed shell size of the specimens in this study increased towards the equator. In modern oceans, planktonic larval stages decrease in duration towards the equator as sea surface temperatures increase and cause an increase in the rate of development (O'Connor et al., Reference O'Connor, Bruno, Gaines, Halpern, Lester, Kinlan and Weiss2007). Higher temperatures also have been shown to increase the rate of development of modern brachiopods (Pennington et al., Reference Pennington, Tamburri and Barry1999). This may allow species found closer to the equator to biomineralize more rapidly, especially given the supersaturation of bicarbonate in warm, shallow, equatorial waters, producing larger first-formed shells.
Relative sizes of dorsal first-formed shells of species under study, located on map of Late Ordovician Laurentia (after Cocks and Torsvik, Reference Cocks and Torsvik2011). Ages of specimens used in the study are indicated by color.
Mean widths of first-formed dorsal shells of each species (in millimeters) compared to approximate paleolatitude (in degrees south).
Another factor noted in modern marine invertebrates with planktotrophic subadults is an increase in food availability resulting in a larger size at settlement (Giménez, Reference Giménez2010). If more food were available towards the equator, then species living there may have been able to grow larger in the water column and thus be larger in size at settlement. Although modern tropical oceans have lower chlorophyll concentration than temperate oceans do (Gregg et al., Reference Gregg, Casey and McClain2005), chlorophyll concentration is higher at shallower depths (Sauzède et al., Reference Sauzède, Lavigne, Claustre, Uitz, Schmechtig, D'Ortenzio, Guinet and Pesant2015), making it difficult to say whether modern latitudinal patterns would apply to the relatively shallow Ordovician epicontinental seas, which have no true modern analogue. Regional differences in this environment may explain the exceptional subadult shell size of P. sillimani, whose large first-formed shell size contradicts the overall latitudinal trend.
Adaptive advantage of an extended juvenile stage in Paucicrura sillimani.—The large size of the first-formed shell of P. sillimani may indicate an extended time spent in the water column during the juvenile stage. Longer planktonic phases in benthic marine invertebrates allow for larger dispersal distances and greater connectivity between populations of benthic marine invertebrates with a pelagic phase in their life cycle (Treml et al., Reference Treml, Halpin, Urban and Pratson2008). This may also have been the case in the Paleozoic, as during the Richmondian Invasion in the Upper Ordovician of the Cincinnati region most invaders belonged to groups with planktotrophic larvae, which allowed long-distance dispersal (Lam and Stigall, Reference Lam and Stigall2015).
The longer planktotrophic stage in P. sillimani may have enabled greater dispersal across the shelf in comparison to other populations of Paucicrura and Diceromyonia in Laurentia. The true extent of the Ordovician epicontinental sea in Laurentia remains unclear, although conodont evidence and carbonate outliers suggest that by the Richmondian it covered much of what is now the Precambrian Shield (Dix et al., Reference Dix, Coniglio, Riva and Achab2007; Zhang, Reference Zhang2011; Kang and Dix, Reference Kang and Dix2021). As the epicontinental sea grew rapidly in size through the early Katian due to elevated sea level (Haq and Schutter, Reference Haq and Schutter2008), new living environments would have become accessible, including what is now Baffin Island. Modeling of oceanic circulation through the Ordovician has shown that northeastern Laurentia may have been a region of low primary productivity relative to southwestern Laurentia during the Middle to Late Ordovician (Pohl et al., Reference Pohl, Harper, Donnadieu, Le Hir, Nardin and Servais2018). A longer juvenile stage may have enabled P. sillimani to survive in the water column long enough to spread to newly opened continental shelf settings in what is now northeastern North America to access new, productive shallow-marine ecosystems. An inconsistent nutrient supply in the area also may have resulted in a patchy distribution dependent on currents, as seen in the modern brachiopod-dominated Brazilian Bight (Kowalewski et al., Reference Kowalewski, Simoes, Carroll and Rodland2002) and Patagonian continental shelf (Gordillo et al., Reference Gordillo, Muñoz, Bayer and Malvé2018).
In addition to the ability to colonize a new area, a longer juvenile stage may have allowed P. sillimani more time to locate advantageous settlement locations. Modern brachiopod larvae in laboratory settings have been shown to exhibit preferences for certain settlement locations, such as low-light conditions or on conspecific shells (Pennington et al., Reference Pennington, Tamburri and Barry1999; Passamaneck et al., Reference Passamaneck, Furchheim, Hejnol, Martindale and Lüter2011). Less-ideal settlement locations, such as on unfavorable substrates, have been shown to interfere with metamorphosis (Percival, Reference Percival1960). It is difficult to determine the preferences of fossil species for particular temperatures, salinities, or light levels. If P. sillimani had a narrow range of tolerances and required a particular set of conditions within its ecosystem, such as a preference for lower light levels only found in shaded areas or a particular type of substrate, then an extended juvenile period may have provided more time to find a suitable settlement location. This also could explain the variation seen in size at settlement, with individuals that found a suitable settlement location faster may have metamorphosed earlier, moving more quickly on to the adult stage of their life cycle.
The GOBE marks an increase in prevalence of suspension feeders in the benthos (Stigall et al., Reference Stigall, Edwards, Freeman and Rasmussen2019), so P. sillimani subadults that spent more time in the water column may have better avoided benthic planktotrophs and a substantial shell in this stage may have protected them from smaller nektonic planktotrophs. This factor may have influenced the evolution of planktotrophy in multiple invertebrate lineages at this time, playing at least some role in driving the rapid evolution across marine ecosystems during the Ordovician (Servais et al., Reference Servais, Perrier, Danelian, Klug and Martin2016). Staying in the water column might also have allowed subadults to avoid competition for food and living space in a crowded benthic ecosystem full of other filter feeding organisms until they were larger and more competitive. These benefits would also apply, to a lesser extent, to other species of Paucicrura with large first-formed shells that were not so large and prominent as those of P. sillimani.
Conclusion
The size and structure of dalmanellid first-formed shells vary, even within genera. While all species studied likely had planktotrophic larval stages, the length of this stage and the presence or absence of a shelled juvenile stage differed between species. Paucicrura likely had a juvenile stage, while Cincinnetina and Diceromyonia did not. Dalmanellid life cycles were plastic, varying even between species within the same genus, suggesting physical or ecological factors may have played a more important role than evolutionary relationships. Differences in temperature or productivity along latitudinal gradients may have contributed to general trends in size at settlement, but most species studied overlap in their range of sizes. Paucicrura sillimani resembles other members of its genus in all respects except for its first-formed shell, which was significantly larger. This indicates it spent an extended period in the water column or was able to biomineralize a larger initial shell more quickly than other species. This may have indicated that colonization of the area that is now Baffin Island necessitated an extended period in the water column, or it may have been an adaptation that allowed individuals to find suitable settlement locations in a less broadly habitable environment or defend from zooplankton predators.
The results of this study underscore that fossil brachiopods may not have lived like their modern rhynchonelliformean analogues, especially in lineages only known from the Paleozoic. The lecithotrophic larvae of modern lineages may not be as universal among fossil brachiopod groups as once thought. This may have similar implications for the study of the life cycles of other invertebrates that also lack true modern analogues, such as rugose and tabulate corals, ammonites, and early Paleozoic arthropods.
Acknowledgments
The authors thank J. Jin (Western University), C. Schwalbach (CMC), P. Mayer (FMNH), and M. Coyne (GSC) for kindly arranging for loans of brachiopods for this study. The manuscript benefitted from careful reviews by J. Jin and C.M.Ø. Rasmussen. We thank M. Rychel for help with the high-magnification photography and proofreading the manuscript. This work was funded by an NSERC Discovery Grant to Sproat and scholarship support to Rogal from the University of Saskatchewan.
Declaration of competing interests
The authors declare none.
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