Helicoprion

Diagram of the teeth within the spiral

Almost all Helicoprion specimens are known solely from "tooth whorls", which consist of dozens of enameloid covered teeth embedded within a common logarithmic spiral-shaped root. The youngest and first tooth at the center of the spiral, referred to as the "juvenile tooth arch", is hooked, but all other teeth are generally triangular in shape, laterally compressed and often serrated.[7] Tooth size increases away from the center of the spiral (abaxial), with the largest teeth possibly exceeding 10 centimetres (3.9 in) in length. The lower part of the teeth form projections that are shingled below the crown of the previous tooth. The lowest portion of the root below the enameloid tooth projections is referred to as the "shaft", and lies on cartilage that encapsulates the previous revolutions of the whorl. In a complete tooth whorl, the outermost part of the spiral terminates with an extended root that lacks the middle and upper portions of the tooth crown.[2]

Restoration of the skull of Helicoprion, based on IMNH 37899

Helicoprion specimens preserving more than tooth whorls are very rare. The best-preserved specimen of Helicoprion is IMNH 37899 (also known as "Idaho 4"), referred to Helicoprion davisii. It was found in Idaho in 1950 and was originally described in 1966 by Svend Erik Bendix-Almgreen.[8] A 2013 redescription by Tapanila and colleagues was accompanied by CT scanning, in order to reveal the cartilaginous remains in more detail. CT scanning revealed a nearly complete jaw apparatus, articulated in a closed position with three-dimensional preservation. Alongside the tooth whorl, the specimen preserves a palatoquadrate (forming the upper jaw), Meckel's cartilage (forming the lower jaw), and a robust labial cartilage bracing the tooth whorl. All of these structures are composed of prismatic calcified cartilage, as with modern chondrichthyans. The specimen did not preserve a chondrocranium, the cartilaginous structure which would have housed the brain and sensory organs. The jaws are extensively laterally compressed (narrow) compared to living chondrichthyans, though this may at least partially be an artifact of post-mortem compression.[3][9]

Helicoprion had an autodiastylic jaw suspension, meaning that the inner edge of the palatoquadrate was firmly attached (but not fused) to the chondrocranium at two separate points. These two attachment points are the dome-shaped ethmoid process at the front of the palatoquadrate, and the flange-like basal process at its upper rear corner.[3] Autodiastylic jaws are common in early euchondrocephalans, though in modern animals they can only be found in embryonic chimaeriforms.[10] Another well-preserved specimen, USNM 22577+494391 (the "Sweetwood specimen"), has demonstrated that the inner surface of the palatoquadrate was covered with numerous small (~2 mm wide) teeth.[7] The palatoquadrate teeth were low and rounded, forming a "pavement" which scraped against the tooth whorl.[9] When seen from behind, the palatoquadrate forms a paired jaw joint with the Meckel's cartilage. There is no evidence for an articulation between the palatoquadrate and the hyomandibula.[3]

Meckel's cartilage has an additional projection right before the joint with the palatoquadrate. This extra process, unique to Helicoprion, likely served to limit jaw closure to prevent the whorl from puncturing the chondrocranium. Another unique characteristic of Helicoprion is that the preserved labial cartilage forms a synchondrosis (fused joint) with the upper surface of the Meckel's cartilage. This joint is facilitated via a long facet on the upper edge of Meckel's cartilage. The labial cartilage provides lateral support for the tooth whorl, widening near the root of each volution. By wedging into the palatoquadrate while the mouth is closed, the upper edge of the labial cartilage helps to spread out the forces used to limit the extent of the jaw closure. The rear portion of the labial cartilage has a cup-like form, protecting the developing root of the last and youngest volution.[3][9][7]

Tooth-like chondricthyan scales, specifically known as odontodes, have been found associated with H. bessonowi remains in Kazakhstan. They are broadly similar to scales of other eugeneodonts such as Sarcoprion and Ornithoprion. The scales have a cap-shaped base with a concave lower surface. The crowns are conical and covered with serrated longitudinal ridges. The scales may be monodontode (with one crown per base) or polyodontode (with a bundle of multiple crowns resulting from the fusion of several odontodes into a larger structure). Compared to other eugeneodonts, the scales of Helicoprion are more strongly pointed.[6]

The first specimen of Helicoprion to be described was WAMAG 9080,[2] a 15-tooth fragment of a tooth whorl found along a tributary of the Gascoyne River in Western Australia. Henry Woodward described the fossil in 1886 and named it as the species Edestus davisii, commemorating the man who discovered it.[12] Upon naming H. bessonowi in 1899, Alexander Karpinsky reassigned E. davisii to Helicoprion.[13] In 1902, Charles R. Eastman referred H. davisii to his new genus Campyloprion, but this proposal was never widely accepted.[14] Karpinsky's identification of Edestus davisii as a species of Helicoprion would eventually be upheld by Curt Teichert, who described several more complete tooth whorls from the Wandagee Formation of Western Australia in the late 1930s.[15]

IMNH 37899 ("Idaho 4"), a Helicoprion davisii (=H. ferrieri) tooth-whorl from the Phosphoria Formation, and the only specimen in the genus with preserved soft tissue

In 1907 and 1909, Oliver Perry Hay described a new genus and species of eugeneodont, Lissoprion ferrieri, from numerous fossils found in phosphate-rich Phosphoria Formation on the border between Idaho and Wyoming. He also synonymized H. davisii with his new genus and species.[16] However, Karpinsky separated the two species once more and transferred them to Helicoprion in 1911.[17] H. ferrieri was initially differentiated using the metrics of tooth angle and height, but Tapanila and Pruitt (2013) considered these characteristics to be intraspecifically variable. As a result, they reassigned H. ferrieri as a junior synonym of H. davisii. Outside the Phosphoria Formation, H. davisii specimens have also been found in Mexico, Texas, and Canada (Nunavut and Alberta). H. davisii is characterized by its tall and widely spaced tooth whorl, with these becoming more pronounced with age. The teeth also noticeably curve forwards.[2]

FMNH PF 74455, a H. davisii (=H. ferrieri) tooth-whorl found in the Glass Mountains of Texas

In a 1939 publication, Harry E. Wheeler described two new species of Helicoprion from California and Nevada. One of these, Helicoprion sierrensis, was described from a specimen (UNMMPC 1002) found in glacial moraine deposits in Eastern California, likely originating from the Goodhue Formation.[18] Tapanila and Pruitt determined that the distinguishing shaft range of H. sierrensis was well within the variation found in H. davisii.[2]

H. jingmenense was described in 2007 from a nearly complete tooth whorl (YIGM V 25147) with more than four volutions across a part and counterpart slab. It was discovered during the construction of a road passing through the Lower Permian Qixia Formation of Hubei Province, China. The specimen is very similar to H. ferrieri and H. bessonowi, though it differs from the former by having teeth with a wider cutting blade, and a shorter compound root, and differs from the latter by having fewer than 39 teeth per volution.[19] Tapanila and Pruitt argued that the specimen was partially obscured by the surrounding matrix, resulting in an underestimation of tooth height. Taking into account intraspecific variation, they synonymized it with H. davisii.[2]

Cast of specimen TsNIGR 1/1865, a well-preserved Helicoprion bessonowi tooth-whorl from the Ural Mountains of Russia

Helicoprion bessonowi was first described in an 1899 monograph by Alexander Karpinsky. Although it was not the first Helicoprion species to be described, it was the first known from complete tooth whorls, demonstrating that Helicoprion was distinct from Edestus.[13] As a result, H. bessonowi serves as the type species for Helicoprion.[20] H. bessonowi is primarily based on a number of specimens from Artinskian-age limestone of the Divya Formation, in the Ural Mountains of Russia. H. bessonowi specimens are also known from the Tanukihara Formation of Japan[21] and Artinskian-age strata in Kazakhstan.[6] It can be differentiated from other Helicoprion species by a short and narrowly spaced tooth whorl, backward-directed tooth tips, obtusely-angled tooth bases, and a consistently narrow whorl shaft.[2]

One of two Helicoprion species described by Wheeler in 1939, H. nevadensis, is based on a single partial fossil found in a Nevadan mine by Elbert A. Stuart in 1929.[18] This fossil, UNMMPC 1001, has been lost. It was reported as having originated from the Rochester Trachyte deposits, which Wheeler considered to be of Artinskian age. However, the Rochester Trachyte is in fact Triassic, and H. nevadensis likely did not originate in the Rochester Trachyte, thus rendering its true age unknown. Wheeler differentiated H. nevadensis from H. bessonowi by its pattern of whorl expansion and tooth height, but Leif Tapanila and Jesse Pruitt showed in 2013 that these were consistent with H. bessonowi at the developmental stage that the specimen represents.[2]

Based on isolated teeth and partial whorls found on the island of Spitsbergen, Norway, H. svalis was described by Stanisław Siedlecki in 1970. The type specimen, a very large whorl with specimen number PMO A-33961, was noted for its narrow teeth that apparently are not in contact with each other. However, this seems to be a consequence of only the central part of the teeth being preserved, according to Tapanila and Pruitt. Since the whorl shaft is partially obscured, H. svalis cannot be definitely assigned to H. bessonowi, but it closely approaches the latter species in many aspects of its proportions. With a maximum volution height of 72 mm (2.8 in), H. svalis is similar in size to the largest H. bessonowi, which has a maximum volution height of 76 mm (3.0 in).[2]

In 1999, the holotype of H. bessonowi was stolen, but afterwards was shortly recovered with the aid of an anonymous fossil dealer.[22]

IMNH 30900, a Helicoprion ergassaminon tooth-whorl from Gay Mine in Bingham County, Idaho.

Like H. davisii, Helicoprion ergassaminon is known from the Phosphoria Formation of Idaho. However, it is comparatively much rarer. H. ergassimon was named and described in detail within a 1966 monograph by Svend Erik Bendix-Almgreen.[8] The holotype specimen ("Idaho 5"), now lost, bore breakage and wear marks indicative of its usage in feeding. H. ergassimon is also represented by several other specimens from the Phosphoria Formation, though none of these show wear marks. This species is roughly intermediate between the two contrasting forms represented by H. bessonowi and H. davisii, having tall but narrowly-spaced teeth. Its teeth are also gently curved, with obtusely-angled tooth bases.[2]

Several large whorls are difficult to assign to any particular species group, H. svalis among them. IMNH 14095, a specimen from Idaho, appears to be similar to H. bessonowi, but it has unique flange-like edges on the apices of its teeth. IMNH 49382, also from Idaho, has the largest known whorl diameter at 56 cm (22 in) for the outermost volution (the only one preserved), but it is incompletely preserved and still partially buried.[2] H. mexicanus, named by F.K.G. Müllerreid in 1945, was supposedly distinguished by its tooth ornamentation. Its holotype is currently missing, though its morphology was similar to that of IMNH 49382. In the absence of other material, it is currently a nomen dubium. Vladimir Obruchev described H. karpinskii from two teeth in 1953. He provided no distinguishing traits for this species, thus it must be regarded as a nomen nudum.[2] Various other indeterminate Helicoprion specimens have been described from Canada, Japan, Laos,[23] Idaho, Utah, Wyoming, and Nevada.[20][2]

In 1922, Karpinsky named a new species of Helicoprion, H. ivanovi, from Gzhelian (latest Carboniferous) strata near Moscow. However, this species has subsequently been removed from Helicoprion and placed as a second species of the related eugeneodont Campyloprion.[24]

Alexander Karpinsky's 1899 hypothesis of the placement of the tooth whorl on H. bessonowi.

Hypotheses for the placement and identity of Helicoprion's tooth whorls were controversial from the moment it was discovered. Woodward (1886), who referred the first known Helicoprion fossils to Edestus, discussed the various hypotheses concerning the nature of Edestus fossils.

Joseph Leidy, who originally described Edestus vorax, argued that they represented the jaws of "plagiostomous" (chondrichthyan) fish. William Davies agreed, specifically comparing it to the jaws of Janassa bituminosa, a Permian petalodont. On the other hand, J.S. Newberry suggested that the jaw-like fossils were defensive spines of a stringray-like fish. Woodward eventually settled on E.D. Cope's argument that they represented pectoral fin spines from fish similar to "Pelecopterus" (now known as Protosphyraena).[12]

Karpinsky's 1899 monograph on Helicoprion noted that the bizarre nature of the tooth whorl made it difficult to reach precise conclusions on its function. He tentatively suggested that it curled up from the upper jaw for defensive or offensive purposes. This was justified by comparison to the upper tooth blades of Edestus, which by 1899 had been re-evaluated as structures belonging to the jaw.[13]

Debates over the identity of Helicoprion's tooth whorl were abundant in the years following Karpinsky's monograph. In 1900, the publication was reviewed by Charles Eastman, who appreciated the paper as a whole but derided the sketch of the supposed life position of the whorl. Though Eastman admitted that the teeth of the whorl were very similar to those of other chondrichthyans, he still supported the idea that the whorl may have been a defensive structure embedded into the body of the animal, rather than the mouth.[25] Shortly after his original monograph, Karpinsky published the argument that the whorl represented a curled, scute-covered tail akin to that of Hippocampus (seahorses).[26] This proposal was immediately criticized by various researchers. E. Van den Broeck noted the fragility of the structure and argued that it was most well-protected as a paired feeding apparatus in the cheek of the animal.[27] A.S. Woodward (unrelated to Henry Woodward) followed this suggestion with the hypothesis that each whorl represented a tooth battery from a gigantic shark.[28] G. Simoens illustrated Karpinsky's various proposals and used histological data to adamantly argue that the whorls were toothed structures placed within the mouth.[29] In 1911, Karpinsky illustrated the whorls as components of the dorsal fins.[17] Reconstructions similar to those of Karpinsky (1899) were common in Russian publications as late as 2001.[6]

An outdated illustration of H. bessonowi, with the skull based on a figure published by Janvier (1996).

By the mid-20th century, the tooth whorl was generally accepted as positioned in the lower jaw of the animal. Though this general position was suspected almost immediately in the aftermath of Karpinsky's monograph, it was not illustrated as such until the mid-1900s. Around that time, an artist known only as "F. John" depicted Helicoprion within a set of "Tiere der Urwelt" trading cards. Their reconstruction presented the tooth whorl as an external structure curling down from the lower jaw of the animal. Similar downward-curling reconstructions have also been created by modern paleontologists and artists such as John A. Long, Todd Marshall and Karen Carr. The utility of the tooth whorl in this type of reconstruction was inferred based on sawfish, which incapacitate prey via lateral blows of their denticle-covered snouts.[6][3]

Information on the position of eugeneodont tooth whorls was bolstered by two major publications in 1966. The first was Rainer Zangerl's description of a new Carboniferous eugeneodont, Ornithoprion. This taxon had a highly specialized skull with a small tooth whorl in a symphysial position, i.e. at the midline of the base of the lower jaw. Although skull material had also been reported for Sarcoprion and Fadenia at the time, Ornithoprion was the first eugeneodont to have its skull described in detail.[30]

The other publication was Bendix-Almgreen's monograph on Helicoprion. His investigations reinterpreted the tooth-whorl as a symphyseal structure wedged between the meckelian cartilages, which were separated by a gap at the front. A pair of cartilage loops, the symphyseal crista, seems to develop as a paired extension of the jaw symphysis where the meckelian cartilages meet at the back of the jaw. Each loop arches up before curling back inwards, tracing over the root of the tooth whorl. The largest and youngest teeth form at the symphysis near the back of the jaw. Over time they are carried along the symphyseal crista, spiraling forwards, then downwards and inwards. The series of teeth accumulate into a spiraling structure, which is housed within the cavity defined by the symphyseal crista. The lateral and lower edges of the tooth whorl would have been obscured by skin during life. According to Bendix-Almgreen, the most likely use of the tooth whorl was as a tool for tearing and cutting prey against the upper jaw.[8]

In the 1994 book Planet Ocean: A Story of Life, the Sea, and Dancing to the Fossil Record, author Brad Matsen and artist Ray Troll describe and depict a reconstruction based on the information gleaned by Bendix-Almgreen (1966). They proposed that no teeth were present in the animal's upper jaw, besides crushing teeth for the whorl to cut against. The two envisioned the living animal to have a long and very narrow skull, creating a long nose akin to the modern-day goblin shark.[31] A 1996 textbook by Philippe Janvier presented a similar reconstruction, albeit with sharp teeth at the front of the upper jaw and rows of low crushing teeth in the back of the jaw.[32]

In 2008, Mary Parrish created a new reconstruction for the renovated Ocean Hall at the Smithsonian Museum of Natural History. Designed under the direction of Robert Purdy, Victor Springer, and Matt Carrano, Parrish's reconstruction places the whorl deeper within the throat. This hypothesis was justified by the argument that the teeth supposedly had no wear marks, and the assumption that the whorl would have created a drag-inducing bulge on the chin of the animal if located in a symphysial position. They envisioned the tooth whorl as a structure derived from throat denticles and designed to assist swallowing. This would hypothetically negate the disadvantages the tooth whorl would produce if positioned further forward in the jaw.[33] This reconstruction was criticized for the overly intricate and potentially ineffective design of such a structure, if solely used to assist swallowing.[34]

Lebedev (2009) found more support for a reconstruction similar to those of Bendix-Almgreen (1966) and Troll (1994).[6] A tooth whorl found in Kazakhstan preserved radial scratch marks; the whorl was also found near several wide tuberculated teeth similar to those of the putative caseodontoid Campodus. Lebedev's reconstruction presented a cartilage-protected tooth whorl in a symphysial position at the front of the long lower jaw. When the mouth was closed, the tooth whorl would fit into a deep longitudinal pocket on the upper jaw. Both the pocket in the upper jaw and the edges of the lower jaw would have been lined with dense rows of Campodus-like teeth. This was similar to the situation reported in related helicoprionids such as Sarcoprion and Agassizodus. As for Helicoprion's ecology, it was compared to modern cetaceans such as Physeter (the sperm whale), Kogia (dwarf and pygmy sperm whales), Grampus (Risso's dolphin), and Ziphius (Cuvier's beaked whale). These fish- and squid-eating mammals have reduced dentition, often restricted to the tip of the lower jaw.[6] Lebedev's reconstruction approximates modern views on Helicoprion's anatomy, though the hypothetical long jaw and Campodus-like lateral dentition has been superseded by CT data.[3]