Arachnids are the second most successful terrestrial animal group after Insects and were one of the first Arthropod clades to successfully invade land. Fossil evidence for this transition is limited, with the majority of Arachnid clades first appearing in the terrestrial fossil record. Furthermore, molecular clock dating has suggested a Cambrian-Ordovician terrestrialization event for Arachnids, some 60million years before their first fossils in the Silurian, although these estimates assume that Arachnids evolved from a fully aquatic ancestor. Eurypterids or 'Sea Scorpions', the sister clade to terrestrial Arachnids, are known to have undergone major macroecological shifts in transitioning from marine to freshwater environments during the Devonian. Discoveries of apparently subaerial eurypterid trackways have led to the suggestion that Eurypterids were even able to venture on land and possibly breathe air. However, modern Horseshoe Crabs undertake amphibious excursions onto land to reproduce, rendering trace fossil evidence alone inconclusive.
In a paper published in the journal Current Biology on 10 September 2020, James Lamsdell of the Department of Geology and Geography at West Virginia University, Victoria McCoy of the Department of Geosciences at the University of Wisconsin-Milwaukee, Opal Perron-Feller of the Department of Geology at Oberlin College, and Melanie Hopkins of the Division of Paleontology (Invertebrates) at the American Museum of Natural History, present details of the respiratory organs of a new species of Eurypterid 'Sea Scorpion' from the Carboniferous of Montagne Noire, France.
The new species is placed in the genux Adelophthalmus, and given the specific name pyrrhae, after Pyrrha of Thessaly, daughter of Epimetheus and Pandora in Greek mythology, who along with her husband Deucalion cast stones that turned into babies to repopulate the earth after a great flood, which is a reference to the nodular mode of preservation of the holotype. It is described from a single specimen in the collection of the Hunterian Museum, University of Glasgow, (GLAHM) A23113, an almost complete specimen lacking the telson.
The specimen is from the Lower Carboniferous (Middle to Late Tournaisian) Lydiennes Formation(?) of the St. Nazaire Group in the Montagne Noire region of France. Specific details about the source locality for the specimen are lacking; however, the Lydiennes Formation is the only geological unit in the region to produce fossil-bearing phosphatic nodules. The Lydiennes Formation is made up of black siliceous rocks, primarily described as radiolarian cherts, as well as black shales, and is characterized by abundant phosphate nodules, typically about 5 to 6 cm long, bearing exceptionally preserved, permineralized fossils. The localities of the Lydiennes Formation range from classic localities, interpreted as an offshore basin with well-formed nodules, to more recently described nearshore localities typically with poorly formed nodules. The fossils in the Lydiennes phosphatic nodules include Cephalopods, Arthropods, and abundant plants, which are in situ in the lower Lydiennes Formation.
The fossil is preserved within a phosphate nodule approximately 71 mm long and 55 mm wide and is visible where the nodule has been split medially, exposing the eurypterid along its dorsal plane. Almost the entire Eurypterid is preserved, with the exception of the telson. Externally, a portion of the book gills is visible on the sixth body segment, where the split has crossed through the operculum into the branchial chamber, revealing six overlapping lamellae that appear semicircular in shape attaching obliquely to the midline of the body. A more complete view of the eurypterid’s morphology is afforded through micro computed tomography scanning, permitting digital reconstruction of the entire specimen preserved within the nodule. This reveals details of the external ventral morphology, including prosomal appendages, the metastoma, genital appendage, and opercula, as well as the structure of the respiratory organs and gut. The specimen is interpreted as a carcass based on the retracted position of the prosomal appendages and the lack of opisthosomal curvature or telescoping.
All six pairs of prosomal appendages are preserved, including the chelicera, which are short and robust, and the distally expanded paddle of appendage VI. Appendages II–V all bear a pair of spines ventrodistally on each podomere; this, combined with the presence of postabdominal epimera and the lack of any lateral reduction in the anterior opisthosomal segment, indicates that Adelophthalmus pyrrhae has a close affinity to the American species Adelophthalmus mazonensis and Adelophthalmus mansfieldi. As in other Eurypterids, the mesosomal opisthosomal appendages of somites VIII–XIII are highly modified into broad, medially fused opercular plates that cover the entirety of the ventral sternites. The first two opercula are further fused into a single functional unit called the genital operculum, which bears the genital appendage. Posterior to the genital operculum are four more opercula, although the penultimate operculum, corresponding to the fifth dorsal tergite, is absent from the specimen and appears to have been lost due to taphonomic processes, potentially having broken off separately when the nodule was opened and subsequently been lost.
The opercula enclose the book gills within a branchial chamber that is defined dorsally by the abdominal sternites. The opercula enclose the book gills within a branchial chamber that is defined dorsally by the abdominal sternites, indicating a total of five pairs of book gills in life, as in Xiphosura. The genital operculum bears only a single pair of book gills, located on the posteriormost of the two fused opercula, representing the appendages of somite IX. The book gills are horizontally oriented and fragmentary, with only the book gills of the sixth operculum preserved in their entirety; these are oval, attach close to the midline of the body, and consist of six lamellae. The number of lamellae in the anterior gills is unclear; however, the amount of fragmentary material within the branchial chamber indicates a higher lamella count and that these lamellae also bore trabeculae. Further evidence that the anterior book gills had more lamellae comes from a specimen of the Ordovician Eurypterid Onychopterella augusti that exhibits four sets of book gills (interpreted here as belonging to segments 2–5), each with 45 lamellae. The gills in Onychopterella were interpreted as being vertically stacked rather than horizontally oriented, as indicated by Adelophthalmus pyrrhae. This apparent difference, however, is taphonomic; the lamellae of Adelophthalmus pyrrhae are deflected into a more vertical orientation laterallyby the curvature of the opercula, and specimens of the Cretaceous Xiphosurid Tachypleus syriacus show that the lateral margins of the book gills can be preserved so as to appear vertically stacked. Although the gill macrostructure is Xiphosuran in appearance, the microstructure is markedly Arachnid in nature. The dorsal surface of each lamella is covered with regularly spaced 0.15-mm-tall, 0.05-mm-wide pillar-like trabeculae projecting up into the media space between lamellae, with a clear hemolymph space within each lamella. Trabeculae are commonly found in pulmonate arachnids and are a terrestrial adaptation for air breathing, serving to keep the lung lamellae from collapsing together and eliminating the media space, which would suffocate the organism. Trabeculae are absent in Horseshoe Crabs, the gills of which collapse out of water and are not efficient at air oxygen transfer, rendering them incapable of subaerial breathing, nor have trabeculae been described in any of the fossil Xiphosurans or stem Euchelicerates preserving gills. The presence of trabeculae in Adelophthalmus pyrrhae is therefore direct evidence that Eurypterids were able to breathe in subaerial environments through their main respiratory organs. The trabeculae exhibit regular spacing and possess a morphology comparable to the trabeculae found in arachnids, which comprise a conical base extending into a narrow pillar. The majority of the trabeculae within the specimen are represented by the broad conical base, with very few retaining the pillar structure; however, this preservation is identical to that of the trabeculae in an exceptionally preserved Devonian Trigonotarbid, which also preferentially preserves the base of the trabeculae but preserves the pillars in irregular shapes and widths. When sufficiently preserved, the trabeculae of Adelophthalmus pyrrhae exhibit a differentiation into anterior proximal trabeculae attached to both lamellar surfaces and posterior distal trabeculae attached only to the dorsal surface of the ventral lamella, a distribution also observed in modern Arachnids.
Eurypterids are known to utilize a dual respiratory system, with gills on the opercula supplemented by vascular structures located on the ventral surface of the body wall termed Kiemenplatten. These Kiemenplatten have been tentatively suggested to act as ancillary respiratory structures for putative amphibious excursions. The occurrence of trabeculae on the book gills indicates that these too were active respiratory organs in air and confirms that Eurypterids were fully capable of persisting in terrestrial environments for extended periods. The low number of respiratory lamellae in the posterior book gills of Adelophthalmus pyrrhae is puzzling but may be a desiccation resistance strategy to reduce overall surface area while promoting subaerial gas exchange as seen in amphibious and terrestrial Crustaceans. Interestingly, amphibious Crustaceans also maintain some gills with a higher surface area for aquatic respiration. Despite these adaptations for subaerial breathing, Eurypterids had a predominantly aquatic life habit, as indicated by the diversity of species (including Adelophthalmus pyrrhae) with their posterior pair of prosomal appendages modified into a broad swimming paddle and their abundant aquatic fossil record. It has also been suggested that the Eurypterid’s method of masticating food via appendicular gnathobases would have been unable to function on land, thereby limiting the amount of time that Eurypterids could have spent out of their usual aquatic environment. Instead, the semi-terrestriality may have allowed Eurypterids to move between ephemeral pools to reproduce in sheltered creche environments, as indicated by the spatial segregation between adults and juveniles observed in the fossil record. Further support for this interpretation comes from the discovery that eurypterids, like Arachnids, possessed spermatophores. Spermatophore-mediated reproduction may have permitted female eurypterids to store sperm for up to several months as in modern Arachnids, permitting time for migration to creche environments to reproduce after mating. The presence of spermatophores also opens up the possibility that Eurypterids were capable of transferring sperm in terrestrial environments.
Molecular divergence estimates indicate that Arachnids occupied terrestrial environments during the early Ordovician or late Cambrian. Until now, such a time frame for terrestrialisation would have required an almost saltationist transition from an aquatic to terrestrial life habit. Some Silurian Scorpions have been proposed to be aquatic and exhibit a stepwise acquisition of terrestrial characteristics; however, this would necessitate two terrestrialisation events within Arachnida, and the aquatic nature of these Scorpions has been debated. Similar disconnects between molecular estimates and the fossil record of myriapods were recently resolved by the recognition that the aquatic Cambrian-Triassic Euthycarcinoids are stem Myriapods. Similarly, the solution to the discrepancies in the projected and observed timing of Arachnid terrestrialisation may lie within their stem lineage. The discovery of air-breathing adaptations in the Eurypterids, the Arachnid sister group, indicates that terrestrial adaptations accrued in a stepwise pattern along the Arachnid stem lineage, culminating in the modifications for preoral digestion, including a preoral cavity formed from the basal articles of the pedipalp and anteroventrally directed mouth that characterise Arachnids (which Adelophthalmus pyrrhae lacks). Critically, the occurrence of subaerial breathing can be inferred across all Eurypterids based on trackway evidence of terrestrial excursions in Stylonurina; the occurrence of Kiemenplatten across Eurypterida, including records from the early Silurian; and the morphological evidence from Adelophthalmus pyrrhae, indicating that terrestrial adaptations were likely inherited from the common ancestor of Eurypterids and Arachnids. The Cambrian-early Ordovician ancestor of Arachnids and Eurypterids would therefore have been semi-terrestrial, corresponding to the molecular clock estimates for terrestrialisation within the group, with the radiation and diversification of Arachnids occurring fully within a terrestrial setting.
Recent molecular phylogenetic work has suggested that Xiphosurans are in-group Arachnids and are secondarily aquatic, but has been rebutted based on further molecular analyses and assessment of whole-genome duplication events. Eurypterids have not been considered in these studies and were assumed to have a life habit similar to Horseshoe Crabs. As such, our revised understanding of Eurypterid respiration has important ramifications for the suggestion that Horseshoe Crabs (and Eurypterids) are secondarily aquatic. The semi-aquatic nature of Eurypterids could be indicative of a lineage in the process of either leaving or returning to the water; however, other aspects of their morphology, including the lack of terrestrial feeding capabilities and the absence of paired apoteles, are more indicative of an organism with greater affinity to the aquatic rather than terrestrial realm. Crucially, the ancillary respiratory Kiemenplatten, which would not have functioned in subaqueous media, are distinct to any respiratory structure in Arachnida. This strongly indicates that Eurypterids were experimenting with modes of terrestrial respiration and were in the process of terrestrialising rather than returning to aquatic environments. This in turn suggests that Horseshoe Crabs evolved from fully aquatic ancestors. Assuming a single terrestrialisation event for Arachnida therefore necessitates that non-pulmonate Arachnids lost their book lungs, with tracheae evolving multiple times among non-pulmonates, as indicated by their occurrence on different body segments in different groups. Alternatively, Arachnids may have invaded land multiple times; however, this scenario still necessitates that non-pulmonates lost their respiratory lamellae and independently developed tracheae. Nevertheless, the discovery of trabeculae in the book gills of Eurypterids demonstrates that terrestrialization in at least pulmonate Arachnids occurred as the final step of a protracted series of character acquisitions within the Arachnid stem lineage and that eurypterids represent a truly unique example of semiterrestriality as part of a broader evolutionary trajectory toward the invasion of land.
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