1. Introduction
Xiphosurans (commonly referred to as horseshoe crabs) are aquatic chelicerate arthropods with an extensive fossil record stretching back to the Ordovician (Rudkin et al. Reference Rudkin, Young and Nowlan2008) but a seemingly low standing diversity with only 76 species described to date throughout the entirety of their 445 Ma evolutionary history (Lamsdell, Reference Lamsdell2020). Despite being rare components of aquatic ecosystems, the four extant horseshoe crab species have long been recognized as being biomedically important for vaccine production (Das et al. Reference Das, Bal, Mahapatra, Carmichael, Botton, Shin and Cheung2015) and keystone components of their ecosystems in need of active conservation (Karpanty et al. Reference Karpanty, Fraser, Berkson, Niles, Dey and Smith2006), and are the focus of extensive research (Lamsdell, Reference Lamsdell2022 a). Fossil horseshoe crabs have also been the subject of numerous evolutionary studies, mostly related to the notion that horseshoe crabs are quintessential ‘living fossils’ exhibiting low rates of evolutionary change manifesting in long-term bradytely and morphological stasis (Fisher, Reference Fisher, Eldredge and Stanley1984, Reference Fisher, Briggs and Crowther1990; Kin & Błażejowski, Reference Kin and Błażejowski2014), potentially driven by a generalist ecology. This traditional narrative has been overturned in recent years, with extinct horseshoe crabs shown to have greater ecological and morphological diversity than modern forms (Lamsdell, Reference Lamsdell2016) and a number of xiphosuran clades exhibiting marked shifts in morphology linked to heterochronic shifts in development as they occupy non-marine environments (Lamsdell, Reference Lamsdell2021 a, b). Despite these morphological and ecological changes, horseshoe crabs are thought to have maintained a consistent post-embryonic developmental trajectory (Lamsdell, Reference Lamsdell2021 a; Bicknell et al. Reference Bicknell, Kimmig, Budd, Legg, Bader, Haug, Kaiser, Laibl, Tashman and Campione2022) and exhibit a neuroanatomy conserved at least since the Carboniferous (Bicknell et al., Reference Bicknell, Ortega-Hernández, Edgecombe, Gaines and Paterson2021 b), making xiphosurans an important group for studying the patterns and drivers of mosaic evolution (Hopkins & Lidgard, Reference Hopkins and Lidgard2012; Hunt et al. Reference Hunt, Hopkins and Lidgard2015).
Our understanding of horseshoe crab diversity trends has changed drastically in the last decade. The removal of synziphosurines – a polyphyletic grouping of stem and crown euchelicerates (Lamsdell, Reference Lamsdell2013; Lamsdell et al. Reference Lamsdell, Briggs, Liu, Witzke and McKay2015) – from Xiphosura reduced early Palaeozoic horseshoe crab diversity to a rump, while the synonymy of some 15 species of Belinurus (Lamsdell, Reference Lamsdell2022 b) severely depleted the recognized acme of xiphosuran diversity during the Carboniferous. Conversely, the trough in diversity during the Jurassic has been somewhat ameliorated with the description of two new species from the Hettangian (Bicknell et al., Reference Bicknell, Hecker and Heyng2021 a) and Sinemurian (Lamsdell et al. Reference Lamsdell, Teruzzi, Pasini and Garassino2021). One trend that has remained consistent, however, is the paucity of horseshoe crab species early on in their evolutionary history, with only a single species currently described from the Ordovician (Rudkin et al. Reference Rudkin, Young and Nowlan2008) and none known from the Silurian. With the early evolution of the group so poorly represented in the fossil record, any new early Palaeozoic discoveries have the potential to provide critical information on horseshoe crab origins. Here, we describe three horseshoe crab specimens from the Upper Ordovician of Ontario, Canada, as a new species congeneric to Lunataspis aurora, the only other previously described Ordovician xiphosuran. Critically, this new species is represented by multiple instars and as such affords a view into xiphosuran ontogeny at the very start of their known fossil record, permitting exploration of whether the conserved xiphosuran developmental trajectory has been maintained since the origins of the clade.
2. Material and methods
2.a. Lunataspis material and specimen visualization
Lunataspis borealis sp. nov. is described from three specimens, all housed in the collections of the Royal Ontario Museum (ROM), Toronto, Canada, and recovered from Kingston, Ontario, Canada. The holotype specimen (ROM IP 64616) is a mostly complete adult individual while the two paratypes (ROM IP 64617 and 64618) are juveniles or subadults preserving the prosoma and thoracetron along with parts of the postabdomen. The fossil material was photographed using a Canon EOS 5D Mark IV digital camera with a Canon EF 100 mm Macro lens. All specimens were imaged immersed in ethanol under polarized light.
2.b. Geological setting
All specimens of Lunataspis borealis sp. nov. are derived from the Upper Member of the Gull River Formation, Simcoe Group, Upper Ordovician (Late Sandbian), where it is exposed in the north face of an inactive quarry on the east side of Division Street, south of Benson Street, Kingston, Ontario. Specimens were excavated from a shaly limestone interval c. 4 cm in thickness, immediately below a massive micritic unit in turn located 70–80 cm beneath the top of the exposed section. There is considerable historical controversy regarding the nomenclature of Upper Ordovician lithostratigraphic units in the Kingston area, with some authors having applied terminology based on that of correlative Black River Group strata in New York State (McFarlane, Reference McFarlane1992; Cornell, Reference Cornell2000), while others employ the formational names established or modified by Liberty (Reference Liberty1969, Reference Liberty1971) for the Lake Simcoe and Kingston areas in Ontario (Carson, Reference Carson1982; LeBaron & Williams, Reference LeBaron and Williams1990; Mitchell et al. Reference Mitchell, Adhya, Bergström, Joy and Delano2004). Mapping by Carson (Reference Carson1982) shows the discovery quarry located in his middle member (3B) of a tripartite Gull River Formation. Subsequent revision (LeBaron & Williams, Reference LeBaron and Williams1990) resulted in a local twofold division of the Gull River, with the discovery site falling within a redefined upper member. Following NYS terminology, McFarlane (Reference McFarlane1992) placed the uppermost portion of the discovery quarry section (approximately the top 6 m) in the Lowville Formation. Cornell (Reference Cornell2000) showed what appears to be the same section high in the Lowville, equivalent to the upper Gull River Formation (Moore Hill beds of Okulitch (Reference Okulitch1939)). More recently, revised regional identification of key K-bentonite horizons and of biostratigraphically significant conodont faunas (Mitchell et al. Reference Mitchell, Adhya, Bergström, Joy and Delano2004) suggests the discovery section falls in the M3 sequence of Holland and Patzkowsky (Reference Holland, Patzkowsky, Witzke, Ludvigson and Day1996), correlative with the Belodina compressa Chronozone. We herein follow the scheme in use by the Ontario Geological Survey (Armstrong & Carter, Reference Armstrong and Carter2010).
Late Ordovician strata in the Kingston area form part of a broad, warm-water carbonate shelf succession within the St Lawrence Platform tectonic province (Sanford, Reference Sanford1993). Deposition took place along the southern margin of equatorial Laurentia at c. 20° S latitude (Mac Niocaill et al. Reference Mac Niocaill, Van der Pluijm and Van der Voo1997). Near Kingston, gently southeastward-dipping Ordovician rocks are bounded to the north and east by the Frontenac Arch which brings underlying Proterozoic (Grenville Province) basement to the surface (Hewitt, Reference Hewitt1964). The main expression of the arch lies less than 10 km from the discovery locality, but because the Precambrian surface has an irregular topographic relief, at several sites within 3–7 km of the quarry, granitic and metamorphic basement rocks come very close to the surface or are exposed as outliers. These Precambrian topographic highs represent small islands or shoal areas within the shallow Gull River sea, just offshore of the fully emergent arch. At some of these locations, so-called basal beds of the Shadow Lake Formation contain large angular fragments of Proterozoic crystalline rocks incorporated into high-energy beach sands, which is compelling evidence of an island shoreline probably within a few metres laterally. Gull River carbonates lie just above these basal beds. Fossil-bearing beds of the Upper Member of the Gull River Formation near the top of the discovery quarry were likely formed under oscillating but only slightly deeper (shallow subtidal/peritidal) and quieter water (lagoonal) conditions in a protected area amidst shoals and small islands. Bathyurine trilobite sclerites were found at the same shaly horizon and in direct association with one of the xiphosurid specimens. The thicker micritic beds above and below this horizon yielded a sparse normal marine fauna of isoteline and bathyurine trilobite sclerites, leperditiid valves, tetradiid fragments and strophomenate brachiopods.
It is unclear whether the xiphosuran fossils represent moults or carcasses. Trace fossils are present on the bedding surface immediately below the thin shaly interval in which the three specimens were found, but there is no obvious bioturbation within the shale itself. The available evidence suggests the specimens were buried rapidly in fine-grained sediment under relatively low-energy conditions, with minimal compaction and no subsequent physical or biological disturbance, resulting in unique preservation of the small, relatively intact, non-mineralized xiphosuran exoskeletons.
3. Systematic palaeontology
Chelicerata Heymons, Reference Heymons1901
Xiphosura Latreille, Reference Latreille1802
Xiphosurida Latreille, Reference Latreille1802
Lunataspis Rudkin, Young and Nowlan, Reference Rudkin, Young and Nowlan2008
Lunataspis borealis sp. nov.
Etymology. The species name borealis is Latin for ‘northern’ and refers to the northerly latitude from which the species is known.
Holotype. ROM IP 64616 (Fig. 1a, d), complete adult specimen in dorsal view preserving the dorsal prosomal carapace, thoracetron, postabdomen and telson.
Fig. 1. Lunataspis borealis sp. nov. specimens and interpretive drawings. (a) ROM IP 64616. (b) ROM IP 64617. (c) ROM IP 64618. (d) Interpretive drawing of ROM IP 64616. (e) Interpretive drawing of ROM IP 64617. (f) ROM IP 64618. Grey indicates preservation of organic cuticular material. All scale bars = 1 mm. Abbreviations: AN, axial node; CL, cardiac lobe; CN, cardiac node; FT, free tergites; LE, lateral eye; MR, marginal rim; OR, ophthalmic ridge; PT, pretelson.
Additional material. Paratypes ROM IP 64617 (Fig. 1b, e), incomplete juvenile or subadult specimen in dorsal view preserving dorsal prosomal carapace and thoracetron, and ROM IP 64618 (Fig. 1c, f), incomplete juvenile or subadult specimen in dorsal view preserving the dorsal prosomal carapace, thoracetron and postabdomen.
Localities and horizon. Upper Member of the Gull River Formation, Simcoe Group, Upper Ordovician (Late Sandbian), in Kingston, Ontario, Canada (44° 15′ 52.7″ N, 76° 29′ 46.3″ W).
Diagnosis. Lunataspis with cardiac node positioned at base of cardiac lobe; lateral eyes located along middle of prosomal carapace length.
Description. ROM IP 64616 comprises the prosomal carapace, thoracetron, postabdomen and telson in dorsal view preserved in positive relief. Maximum preserved length 37.0 mm, missing the very tip of the telson. Prosomal carapace 11.6 mm long, 18.8 mm wide, semicircular in outline. Cardiac lobe indistinct. Cardiac node, 1.0 mm long by 1.0 mm wide, located centrally at carapace posterior. Reniform lateral eyes faintly visible, 1.4 mm long by 0.5 mm wide, located 3.6 mm from carapace lateral margin and 5.6 mm from carapace posterior. Marginal rim indistinct. Genal spines extending 4.8 mm beyond prosomal carapace posterior, narrowing distally from width of 4.0 mm proximally. Thoracetron 7.7 mm long, 14.1 mm wide anteriorly narrowing to 10.1 mm wide posteriorly, broadly rectangular in outline. Number of tergites in thoracetron unknown. First two thoracetron tergites freely articulating, first tergite 0.9 mm long, second tergite 1.0 mm long. Flattened pleural region, potentially corresponding to the ventral doublure, extends around the thoracetron margin posterior to the freely articulating segments and is 1.3 mm wide. Axial region of thoracetron indistinct. Vestigial differentiation of final thoracetron segment axis in line with thoracetron pleural region. Postabdomen composed of three freely articulating segments and pretelson. First postabdominal segment 1.0 mm long and 5.7 mm wide, second 0.9 mm long and 4.9 mm wide, third 0.8 mm long and 4.0 mm wide. Pretelson elongated, 3.2 mm long and 3.4 mm wide. Axial nodes, 0.8 mm long and 0.8 mm wide, present at thoracetron anterior and each postabdominal segment. Telson long, styliform, preserved length 12.5 mm, 0.9 mm wide.
ROM IP 64617 comprises the prosomal carapace, thoracetron, and proximal postabdominal segments in dorsal view preserved in negative relief. Maximum preserved length 13.7 mm, missing the posterior postabdominal segments and telson. Prosomal carapace 5.8 mm long, 13.1 mm wide, lunate in outline. Cardiac lobe 2.0 mm wide at base. Cardiac node, 0.4 mm long by 0.4 mm wide, located centrally on cardiac lobe. Reniform lateral eyes, 1.7 mm long by 0.5 mm wide, located 2.2 mm from carapace lateral margin and 1.9 mm from carapace posterior. Faint ophthalmic ridge located posterior to lateral eyes, extending to carapace posterior in line with fulcrum of thoracetron pleural region. Narrow (0.2 mm) marginal rim extends to distal portion of genal spines. Genal spines extending 4.4 mm beyond prosomal carapace posterior, narrowing distally from width of 3.4 mm proximally. Thoracetron 5.9 mm long, 7.7 mm wide anteriorly narrowing to 5.3 mm wide posteriorly, semicircular in outline. Thoracetron composed of eight tergites. First two thoracetron tergites freely articulating, both tergites 0.7 mm long. Flattened pleural region, potentially corresponding to the ventral doublure, extends around the thoracetron margin posterior to the freely articulating segments and is 0.5 mm wide. Axial region of thoracetron exhibiting faintly visible vestigial differentiation of six fused tergites, sixth axial segment in line with thoracetron pleural region. Postabdomen composed of at least three freely articulating segments. Axial nodes poorly preserved but appear to be present on fused thoracetron segments.
ROM IP 64618 comprises the prosomal carapace, thoracetron and postabdomen in dorsal view preserved in positive relief. Maximum preserved length 13.5 mm, missing the telson. Prosomal carapace 6.2 mm long, 13.7 mm wide, lunate in outline. Cardiac lobe 2.8 mm wide at base. Cardiac node, 0.4 mm long by 0.4 mm wide, located centrally on cardiac lobe. Reniform lateral eyes, 1.8 mm long by 0.6 mm wide, located 4.0 mm from carapace lateral margin and 2.1 mm from carapace posterior. Narrow (0.3 mm) marginal rim extends to distal portion of genal spines. Genal spines extending 5.2 mm beyond prosomal carapace posterior, narrowing distally from width of 2.6 mm proximally. Thoracetron 6.2 mm long, 8.6 mm wide anteriorly narrowing to 6.3 mm wide posteriorly, semicircular in outline. Thoracetron composed of eight tergites. First two thoracetron tergites freely articulating, both tergites 0.7 mm long. Flattened pleural region, potentially corresponding to the ventral doublure, extends around the thoracetron margin posterior to the freely articulating segments and is 0.5 mm wide. Axial region of thoracetron with axis margins in line with cardiac lobe. Vestigial differentiation of six fused thoracetron tergites visible within axis, sixth axial segment in line with thoracetron pleural region. Postabdomen composed of three freely articulating segments and pretelson. First postabdominal segment 0.5 mm long, second 0.5 mm long, third 0.4 mm long, lateral margins indistinct. Pretelson elongated, 2.4 mm long. Axial nodes, 0.3 mm long and 0.3 mm wide, present on thoracetron segments.
4. Discussion
Lunataspis borealis sp. nov. exhibits a number of traits considered diagnostic of the genus Lunataspis, including the large, lunate prosomal carapace with a low cardiac lobe and a shallow U-shaped posterior embayment (Rudkin et al. Reference Rudkin, Young and Nowlan2008). The original diagnosis for Lunataspis indicates that the thoracetron is completely fused and composed of six or seven sclerites while the postabdomen consists of three tergites with a medially constricted telson. Lunataspis borealis, however, possesses two freely articulating tergites anterior to a thoracetron comprising six sclerites with a postabdomen of four tergites, the last of which is an elongated pretelson. These differences would be enough to place the new species in a new genus; however, large specimens of Lunataspis aurora show that two freely articulating segments exist anterior to the thoracetron (Young et al. Reference Young, Rudkin, Dobrzanski, Robson, Cuggy, Demski and Thompson2012) while other specimens demonstrate that the ‘constriction’ of the telson of Lunataspis aurora in the original description is actually the articulation between a narrow telson and an elongated pretelson (Rudkin & Young, Reference Rudkin, Young, Tanacredi, Botton and Smith2009), as in Lunataspis borealis. The new species described here, while congeneric with Lunataspis aurora, can be clearly differentiated based on its position of a large node located at the base of the shallow cardiac lobe and the position of the lateral eyes along the median third of the carapace length compared to the posterior third in Lunataspis aurora. The discovery of Lunataspis borealis demonstrates that multiple roughly coeval species of Lunataspis occupied the shallow seas of Laurentia during the Late Ordovician and extends the range of the genus from Manitoba into eastern Ontario.
The three available specimens of Lunataspis borealis comprise at least two distinct instars, with the larger holotype (ROM IP 64616; Fig. 1a) representing an adult or subadult, while the paratypes (Fig. 1b, c) are smaller juvenile individuals. Although the ontogenetic data for the new species is limited to two instars, a number of changes are apparent. The overall proportions of the animal change, with the prosoma increasing from being equal in size to the thoracetron in juveniles to half again the thoracetron size in adults. Within the prosoma, the lateral eyes exhibit negative allometry, being proportionally smaller in the adult specimen compared to the juveniles, and shift to being more centrally positioned along the carapace length compared to their more posterior position in the juveniles. The genal spines also proportionally reduce in length, accounting for around a third of the total prosomal carapace length in the adult compared to just under half the prosomal carapace length in the juvenile specimens. The thoracetron also undergoes a shift from a semicircular outline in the juveniles to a markedly rectangular shape in the adult specimen.
The ontogeny of Lunataspis borealis reveals conflicting adherence to the generalized ontogenetic trajectories identified across Xiphosura (Lamsdell, Reference Lamsdell2021 a), with different tagma (Lamsdell, Reference Lamsdell2013) exhibiting different trends, suggesting some degree of developmental modularity. The changes observed within the thoracetron, specifically the transition from a semicircular to a more angular outline and the apparent reduction of visible tergite margins and axial nodes, fit the previously identified trends. Conversely, the migration of the lateral eyes anteriorly as the organism matures, the decrease in the proportional length of the genal spines, and the negative allometry of the lateral eyes result in the structures of the prosoma exhibiting a general opposite trend to that inferred for other xiphosurans. Interestingly, a decrease in both the length of genal carapace extensions and lateral eye size is observed in eurypterid ontogeny (Lamsdell & Selden, Reference Lamsdell and Selden2013). As the generalized developmental trajectory for Xiphosura is recognized in both Belinurina and Limulina (Lamsdell, Reference Lamsdell2021 a; Bicknell et al. Reference Bicknell, Kimmig, Budd, Legg, Bader, Haug, Kaiser, Laibl, Tashman and Campione2022) it is possible that Lunataspis, which resolves as the basal-most xiphosuran outside of the Belinurina and Limulina clades, is exhibiting a mixture of ancestral and derived ontogenetic trajectories and that the highly conserved developmental trajectory of Xiphosura developed somewhere within its stem lineage.
Acknowledgements
We thank Henk Doornekamp for graciously providing site access and Maryam Akrami (ROM) for facilitating loan of the specimens. Two anonymous reviewers provided useful comments on the manuscript. J.C.L. is supported by National Science Foundation CAREER award EAR-1943082 ‘Explaining Environmental Drivers of Morphological Change through Phylogenetic Paleoecology’.
Conflict of interest
None.
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