Morphological variability of dermal elements of the mandibular arch in antiarchs

Although generally following the same bauplan, the jaw elements in antiarch fishes present a variety of morphologies (Figs. 2–4). The Yunnanolepidoidei differ from the Asterolepidoidei and the Bothriolepidoidei in the absence of the oral shelf and complete ornamentation of the external surface of the suborbitals, as well as the absence of the lateral notch. Symphyseal fusion between the suborbital antimeres is variable (Fig. 2.1, 2.2).

The characteristic feature of the Asterolepidoidei is a close (Asterolepis ornata, Upeniece, Reference Upeniece2011; Pterichthyodes milleri, Hemmings, Reference Hemmings1978; Remigolepis walkeri, Johanson, Reference Johanson1997) or even sutural contact between the suborbitals (A. scabra, Nilsson, Reference Nilsson1941; Remigolepis sp. from East Greenland, Nilsson, Reference Nilsson1941), suggesting the functional importance of this rigid connection (Figs. 2.3–2.5, 3.1–3.5). In contrast to yunnanolepidoids and in accordance with the bothriolepidoids, a significantly wide, smooth band devoid of dermal ornamentation runs along the oral margin of the suborbitals (Fig. 3.1, 3.2, 3.6–3.12) being unknown due to preservation in A. scabra, Remigolepis sp. from East Greenland (Nilsson, Reference Nilsson1941), and R. walkeri (Johanson, Reference Johanson1997). In Asterolepidoidei, the mesial notch on the oral side of the suborbitals is missing; thus, the oral margins of these bones are only slightly convex.

In the Bothriolepidoidei, the suborbitals are more or less lozenge shaped with the mesial (symphyseal) margin subparallel to the lateral one (Fig. 3.7–3.12), with the exception of Nawagiaspis (Fig. 3.6), in which the latter is directed at a right angle to the posterior (aboral) margin (Young, Reference Young1990). In this antiarch, the mesial part of the oral margin externally is occupied by a rugose area most probably for attachment of connective tissues serving to form an elastic connection of antimeres. In other bothriolepidoids, this area is ornamented superficially with regular dermal sculpturing suggesting placement of this connection on the visceral surface, if any. When connected, the oral margins of the suborbitals taken together would make a mesial notch, in contrast to the Yunnanolepidoidei and Asterolepidoidei, in which the oral margin is almost straight. In well-preserved and chemically prepared specimens, such as Bothriolepis sp. from Gogo (CPC 25205), the groove separating the oral shelf from the dermally ornamented aboral part demonstrates numerous vascular foramina of various sizes (Young, Reference Young1984, pl. 58, fig. 1, text-fig. 6), which suggests an active blood supply. In some species (B. canadensis, Stensiö, Reference Stensiö1948, text-figs. 35A, C; B. cellulose, Gross, Reference Gross1941, text-fig. 6A; Stensiö, Reference Stensiö1948, text-fig. 35D; Bothriolepis sp. from Gogo, Young, Reference Young1984, text-figs. 2, 3, 5, 6, pls. 58, figs. 1, 59, figs. 1, 2; Grossilepis tuberculate, Gross, Reference Gross1941, text-fig. 26G; Stensiö, Reference Stensiö1948, text-fig. 35F), this oral margin bears bony spikes arranged at an approximately regular distance from each other. This row of crenulations continues mesially, occupying approximately half of this margin.

Morphological variability of antiarch infragnathals can be grouped by the following features: (1) ratio between the length of the oral and distal divisions, (2) curvature of the oral division, (3) oral blade depth, (4) curvature of the labial margin of the distal division, and (5) porosity and superficial ornamentation of the oral division (Fig. 4).

The oral division of the infragnathal is morphologically marked by the posterior extremity of its oral blade. In Bothriolepis canadensis, the oral blade terminates distally, forming a deep semicircular flange (Stensiö, Reference Stensiö1948, text-fig. 36A).

The length of the oral division exceeds that of the distal in Pterichthyodes milleri (Fig. 4.1, 4.2), Grossilepis tuberculata (Fig. 4.6–4.8), and Nawagiaspis wadeae (Fig. 4.4, 4.5); in Bothriolepis canadensis (Fig. 4.9, 4.10), these parts are of approximately the same length. In other species, the oral division is shorter than the distal one. However, in Remigolepis walkeri (Fig. 4.3) and Bothriolepis sp. from Gogo (Fig. 4.11–4.13), the oral divisions are arched in such a manner that the lingual side is concave and the labial one is convex; this gives an impression of their shortness in the labial projection.

The curvature of the oral division might be roughly estimated by means of an angle between two planes, one tangential to the mesial and the second to the distal part of the vertical blade (lines in two dimensions). Geometrically, this angle is known as the central angle of an arch. In Pterichthyodes milleri and Bothriolepis sp. from Livny (PIN 3725/1119) and “Livnolepis zadonica” (PIN 3725/1118) these planes meet at an approximately right angle, in Remigolepis walkeri, Nawagiaspis wadeae, and Bothriolepis sp. from Gogo this angle is more acute, and in B. canadensis and Grossilepis tuberculata the angle is obtuse. An obtuse angle implies a smaller, and an acute angle a larger, curvature of the oral division.

Data on the vertical blade depth are available only when appropriate views have been provided in the descriptions. The largest depth exceeding that of the distal division is observed in Bothriolepis sp. from Livny (Fig. 4.14–4.16) and “Livnolepis zadonica” (Fig. 4.17–4.19), in which it is approximately twice as large as that of the distal division. In other available species, the vertical blade depth is much smaller and approximately equals or only slightly exceeds that of the distal division.

The labial margin of the distal division is curved to various degrees. In Pterichthyodes milleri, Bothriolepis canadensis, Bothriolepis sp. from Gogo, Bothriolepis sp. from Livny, and Grossilepis tuberculata it is almost straight or only slightly concave, in Remigolepis walkeri it is slightly sinusoid, while in Nawagiaspis wadeae it is very strongly convex. This character might reflect the difference in adductor muscle arrangement.

Another character is the degree of porosity of the vertical blade of the oral division and its superficial ornamentation. Unfortunately, in most specimens, data on the internal structure are unavailable, and all that is possible is visual evaluation of this feature from photos or drawings. In Bothriolepis canadensis the labial side of the vertical blade demonstrates feeble granulation or pitting, although this is not clearly seen in the drawing provided by Stensiö (Reference Stensiö1948, text-fig. 36A) and not commented on in the text, while in Grossilepis tuberculata this area is sculptured by clearly marked, rough tubercles (Gross, Reference Gross1941; Stensiö, Reference Stensiö1948) said to be indistinguishable from those of the ornamentation of the other dermal bones. The marginal tubercles of the occlusal margin are massive and blunt; unfortunately, data on their wear are missing and thus it is hard to judge whether they participated in food processing. In Bothriolepis sp. from Gogo, the lingual surface is strongly porous, except closer to the aboral margin; on the contrary, in Nawagiaspis wadeae, the occlusal part of the lingual side is almost smooth and the basal one is strongly porous (Young, Reference Young1990). Bothriolepis sp. from Livny demonstrates only slight porosity closer to the occlusal margin (Fig. 7.1, 7.2, 7.6, 7.7) while in “Livnolepis zadonica” the lingual side is slightly porous (Fig. 5.1, 5.2) while the labial one bears numerous rough, mostly vertically oriented branching canals opening to the surface of the bone predominantly in its mesial portion (Fig. 5.3–5.5).

The structure of the suborbital–infragnathal morphofunctional unit in antiarchs can be separated into four main groups based mostly on the morphology of the oral (occlusal) margins: (1) this least known group includes the Yunnanolepidoidei in which the oral margin of the suborbitals is devoid of the oral shelf, comparatively straight and incurved; (2) in the Asterolepidoidei, the deep suborbitals contact tightly in the midline or are even connected at a suture, presenting a straight or slightly convex oral margin; (3) in most of the Bothriolepidoidei, the oral margin is strongly convex and forms a mesial notch; on the contrary, the outline of the oral margin of the occlusal portion of the infragnathals is more or less straight or concave; (4) in the fourth group, based on two infragnathals from Central Russia described previously, the oral margin of this bone is strongly convex rather than concave due to its increase in depth toward the middle of the blade.

Thus, the infragnathals in antiarchs demonstrate a wide spectrum of characters related to their configuration and proportions, such as the ratio between the length of the oral and distal divisions, curvature of the oral margin, vertical blade depth, and curvature of the labial margin of the distal division. These differences may reflect the shape and size of the mouth cavity and might be closely related to the general skull outline. Deep skulls in Livnolepis, as described by Moloshnikov (Reference Moloshnikov2004, Reference Moloshnikov2008), might be correlated with the increased depth of the blade of the oral division. Superficial ornamentation as exemplified by Grossilepis tuberculata infragnathals suggests an external position and superficial coating by only a thin epidermal cover (Gross, Reference Gross1941). It is not impossible that in yunnanolepidoids there was no keratinized sheath at all as may be deduced from the absence of the oral shelf on their suborbitals. Sutured suborbitals in asterolepidoids suggest different jaw kinematics from that in bothriolepidoids, but currently there are insufficient data on these groups to perform kinematic studies.

Presence of a keratinous sheath on the gnathal elements in antiarchs

In all studied specimens, the oral surfaces of the gnathal elements are more or less porous. In those Bothriolepis species in which the external surface of the suborbital is adequately known (B. canadensis, B. cellulosa, B. maxima, and B. sp. from Gogo), in Grossilepis tuberculata, and in Nawagiaspis wadeae, the groove along the oral shelf shows variously expressed porosity reflecting an extensive lifetime blood supply. Superficially located vascular foramina and grooves opening on the oral surfaces of the infragnathals and reflecting trabecular spongy inner structure are especially well expressed in Bothriolepis sp. from Gogo (Young, Reference Young1984, pl. 58, figs. 2, 3), Nawagiaspis wadeae (Young, Reference Young1990, text-fig. 9C), Bothriolepis sp. from Livny (Fig. 7.1, 7.2; Supplementary videos 6–8), and especially in “Livnolepis zadonica” (Fig. 5.1, 5.3, 5.5; Supplementary videos 2–5). These foramina suggest the presence of an external cover during life protecting these superficially located blood vessels. This cover should be rigid to interact with food items and, at the same time, protect these vulnerable external vessels and bone surfaces. We suggest that the nature of this cover might have ranged from a comparatively thin layer of hard skin to even a keratinous cap forming the working jaw surfaces. Apart from protective function, a hard keratinoid substance might bear shearing, self-sharpening margins used for scraping.

To support this hypothesis, we considered recent animals. Intense superficial bone vascularization is characteristic of taxa (turtles and birds) in which teeth are missing and the jaw edges are furnished by keratin beaks known as rhamphothecas. For example, in the bill of a long-tailed duck Clangula hyemalis (Linnaeus, Reference Linnaeus1758) (Fig. 9.1–9.3, specimen PIN 41-7-5), the smallest blood vessels ending with capillaries on the ventral margin of the premaxilla are placed in superficial grooves separated by unaffected bony margin; in “Livnolepis zadonica” (Fig. 9.4), there is a strikingly similar structure of the labial side of the oral blade with branching superficial vascular grooves coming into canals at the base.

Figure 9. Vascularization of the oral margins in recent birds compared with antiarchs: (1–3) Clangula hyemalis (Linnaeus, Reference Linnaeus1758): (1) dorsal view of the rostral margin of the premaxilla; (2) ventral view of the rostral margin of the premaxilla; (3) an enlarged area of (2). (4) “Livnolepis zadonica” (Obrucheva, Reference Obrucheva1983); occlusal area of the vertical blade of the oral division of the infragnathal, labially. (1, 2) Scale bars = 2 mm; (3) scale bar = 1 mm; (4) scale bar = 3 mm.

Although keratinous structures are never preserved in the fossils except in Pleistocene mammals obtained from permafrost and asphalt sites (for example, Tridico et al., Reference Tridico, Rigby, Kirkbride, Haile and Bunce2014), presence of gnathic keratinization is widely accepted in the fossil dinosaurs considered the closest relatives of birds and in turtles (for example, Davit-Béal et al., Reference Davit-Béal, Tucker and Sire2009; Louchart and Viriot, Reference Louchart and Viriot2011). Among fossil lower vertebrates, presumed keratinous structures had been described in lampreys and hagfishes (Janvier, Reference Janvier2008). Moreover, genes for keratins are shared across extant vertebrates, including lampreys (e.g., Kimura and Nikaido, Reference Kimura and Nikaido2021), suggesting that these genes would also be expressed in antiarchs (stem gnathosomes; Zhu et al., Reference Zhu, Giles, Young, Hu, Bazzi, Ahlberg, Zhu and Lu2021), including in structures associated with the jaws.

Despite a widely held opinion that no keratin is present in fishes with the exception of horny “teeth” in the mouth sucker in the agnathan cyclostomes (Grassé, Reference Grassé1958), numerous members of the teleost fish family Cyprinidae, the specialized scrapers, possess a sharpened keratinous sheath for scraping off the periphyton (Lyovin, Reference Lyovin2007). This author also indicated that scraping in keratin-bearing Cyprinidae is often observed in those fishes in which skulls are shortened and mandibles are transverse or horseshoe shaped. This corresponds well to characteristics of the antiarch infragnathals described above. In the European periphytonophagous Chondrostoma nasus (Linnaeus, Reference Linnaeus1758), the lower jaw bears a keratinoid sheath (Vostradovsky, Reference Vostradovsky1973). Tripathi and Mittal (Reference Tripathi and Mittal2010) described horny sheaths covering jaws in a cypriniform scraper Puntius sophore (Hamilton, Reference Hamilton1822). Agrawal and Mittal (Reference Agrawal and Mittal1992) observed keratinized cone-like structure on the horny upper jaw sheath and on the horny lower jaw sheath associated with the lips of an herbivorous column feeder, Labeo rohita (Hamilton, Reference Hamilton1822). Pinky et al. (Reference Pinky, Mittal, Yashpal, Ojha and Mittal2004) reported the keratinization in lips and associated structures of Garra lamta (Hamilton, Reference Hamilton1822), and Qi et al. (Reference Qi, Chao, Guo, Zhao, Li, Wei and Zhao2012) in the members of the subfamily Schizothoracinae.

Beginning with Gross (Reference Gross1941), authors described bony crenulations on the occlusal margins of the antiarch suborbitals and infragnathals. Gross stressed that these “Zacken” (crenulations) are not denticles and are not composed of dentine (Gross, Reference Gross1941, p. 14). The groove on the external side of the suborbital (for example, in Young, Reference Young1984, pl. 58, fig. 1) might represent the base of this keratinous case housing its germinal cells. Young (Reference Young1984, text-fig. 6) also presented a photo of a perfectly preserved anterior edge of the semilunar bone forming the medial part of the anterior margin of the oral fenestra bearing tiny crenulations of the same size and distribution type as those on the oral margin of the suborbital. This might suggest the presence of a narrow keratinous cover protecting the posterior margin of the oral fenestra, as would be expected in a bottom-dwelling animal. In various turtles and tortoises, for example in Agrionemys horsfieldii (Gray, Reference Gray1844), very similar crenulations are found along the occlusal margin of the dentary (Fig. 10.1, 10.2). The same type of crenulation is observed on both jaw margins in the Arrau turtle Podocnemis expansa (Schweigger, Reference Schweigger1812) (Fig. 10.3). Formation of these spikes might result from concentration of bone tissue between capillaries supplying blood to subkeratinous dermis.

Figure 10. Crenulations along the jaw margins in modern tortoises. (1) Rostral part of the lower jaw of Agrionemys horsfieldii (Gray, Reference Gray1844), specimen PIN, unnumbered. (2) A scanning electron microscope photo showing an enlargement of bony spikes in (1). (3) The skull of Podocnemis expansa (Schweigger, Reference Schweigger1812), Morphosource-2021-08-18-025423. All figures in lateral view. Scratch marks on the bone surface in (2) are produced by dermestid larvae. (1) Scale bar = 2 mm; (2) scale bar = 1 mm; (3) scale bar = 3 mm.

Reconstruction of the jaw function

Uncertainty with respect to the position of the antiarch gnathal elements results from their bizarre structure and loose connection to the skull, as well as from postmortem displacement. The earliest author to describe the antiarch gnathal elements (Pander, Reference Pander1857) correctly identified these in Pterichthyodes as the mouth parts, but was uncertain which elements belonged to the upper and which to the lower jaws. Traquair (Reference Traquair1888), in his reconstruction of Asterolepis, placed the mouth opening between the rostral margin of the skull roof and jointed suborbital plates considered by him as the lower jaw. Woodward (Reference Woodward1892) was the first to suggest the connection of the suborbitals to the rostral margin of the skull roof by means of connective tissue and skin. The problem remaining is the natural orientation of the suborbitals in the positions “mouth closed” and “mouth opened.”

In fossils, the suborbitals are either found detached or occupy a position within the oral fenestra roughly in the same plane with the ventral part of the thoracic armor, ornamented surface facing ventrally, as exemplified by Phymolepis (Young and Zhang, Reference Young and Zhang1996), Parayunnanolepis (Wang and Zhu, Reference Wang and Zhu2021), Asterolepis ornata (Lyarskaya, Reference Lyarskaya1981; Upeniece, Reference Upeniece2011), Bothriolepis canadensis (Stensiö, Reference Stensiö1931, Reference Stensiö1948), and Bothriolepis sp. from Gogo (Young, Reference Young1984). In Stensiö's reconstruction of the Bothriolepis canadensis head (Stensiö, Reference Stensiö1948, text-figs. 4, 5), the plane of the oral fenestra is inclined anteroventrally with respect to the ventral surface of the trunk shield (Stensiö, Reference Stensiö1948, text-fig. 114), and thus the mouth position was subterminal. The position of the suborbital plates during life was demonstrated by Young and Zhang (Reference Young and Zhang1996) and Young (Reference Young2008); in their reconstructions, the ventral mouth opening position in Bothriolepis contrasts with that presented by Stensiö (Reference Stensiö1948). This anatomical correction is important in the revision of the hypotheses regarding the antiarch feeding mode.

In the yunnanolepidoid Phymolepis cuifenshanensis and in the asterolepidoids Pterichthyodes milleri and Remigolepis sp., the suborbital antimeres tightly contact or even fuse at the symphysis (Nilsson, Reference Nilsson1941; Hemmings, Reference Hemmings1978; Zhu, Reference Zhu1996; Figs. 2.2, 3.1, 3.4). This suggests their action as a single functional unit. In the Bothriolepidoidei, on the contrary (Fig. 2.6, 2.7), the adjoining suborbitals are separated in the midline (Young, Reference Young1984; Zhu, Reference Zhu1996) so that they could function separately, for example, to respond to the size and density of the food object differently.

Johanson (Reference Johanson1997, Reference Johanson1998) interpreted the mouth position in Bothriolepis and Remigolepis as strictly ventral; Béchard et al. (Reference Béchard, Arsenault, Cloutier and Kerr2014), using three-dimensional surface-scanning technology to reconstruct the armor of Bothriolepis canadensis, also clearly demonstrated that the oral fenestra faced strictly ventral.

In Phymolepis as well as in the Asterolepidoidei and the Bothriolepidoidei, the aboral (posterior) margin of the suborbital is always slightly arched (Bothriolepis canadensis, Stensiö, Reference Stensiö1948, text-fig. 35A and Nawagiaspis, Young, Reference Young1990, text-figs. 8A, 9A, B being exceptions). This bend fits the curvature of the rostral margin of the oral fenestra. This suggests that (1) in the natural “mouth closed” position, the suborbitals were situated in such a way that their external (labial) surface was oriented ventrally and in a plane with the ventral side of the trunk armor; and (2) the suborbitals were mobile and could rotate in the rostral direction during mouth opening. However, this rotation would have been limited by palatoquadrate articulations with the braincase, as well as by sensory canal, skin, and other soft tissues surrounding these bones forming no sutured connections to the adjoining ones.

Young (Reference Young1984) suggested that the position of the suborbitals in the Bothriolepis sp. specimen from Gogo was due to postmortem rotation. In the partly prepared state (Young, Reference Young1984, text-fig. 6), the suborbitals are somewhat displaced and depressed inside the cranium, but the infragnathals remain in proper position. This author also provided a reconstruction of the Bothriolepis head in lateral view; however, the upper and lower jaw elements are omitted there.

In a later paper (Young, Reference Young2008, text-fig. 3A), a new reconstruction modified the orientation of the mouth opening at the expense of a slight lifting of the snout and small posteroventral inclination of the suborbitals, thus giving more space for these within the oral fenestra. Considering the repeatedly observed placement of the suborbitals in the same plane with that of the ventral side of the trunk armor in the fossils, we suggest that this had been their natural “mouth closed” position.

Location of the mandibular joint was estimated as inside the prelateral plate, with the dorsal articular surface facing toward the lateral oval pit but some distance below it (Young, Reference Young1984). The palatoquadrate lies rostromesial to the articular process of the submarginal plate, the slope of its lingual surface in the quadrate region conforming fairly well to the slope of the articular process. Two points of articulation between the palatoquadrate and the braincase, the orbital and palatobasal connections, had been reconstructed in Bothriolepis sp. from Gogo (Young, Reference Young1984). Those provided an axis for a limited palatoquadrate + suborbital complex hinge rotation.

To overcome the difference in the transverse width of the longer suborbitals and shorter infragnathals, Young (Reference Young1984) had to assume the presence of a nonpreserved or at least nonossified (?calcified) cartilaginous basimandibular, an unpaired copula of the mandibular arch connecting the two Meckel's cartilage antimeres. If so, the mesial tips of the infragnathal oral divisions became widely separated. However, on the specimen (Young, Reference Young1984, text-fig. 6), the suborbitals and the infragnathals closely fit each other in the midline, with the mesial tips of the latter strongly bound inside the mouth, although this configuration might be explained by postmortem displacement. Wide separation of the mesial tips of the infragnathals is unlikely as in this case they would not fit between the suborbitals. To do so, any mesial connection should be very elastic to make possible rotation of each unit in the lingual–labial direction at the mouth closure/opening.

Creation of our jaw apparatus model was aimed at physical manipulation for defining the most parsimonious and noncontradictory interrelations of its parts and functioning of the mechanism on the whole during life (Supplementary Fig. 1). In our opinion, this “hardware modeling,” as compared with software modeling, allows us to make more definite conclusions as to what positions and movements of the jaws were possible and what were not. For example, our hardware model of acrylic plaster and plasticine has immediately allowed us to exclude any occlusal interactions between the antiarch upper and lower jaws, which were found to be incompatible with the integrity of the jaw articulation.

The jaw articulation reconstructed here might belong to a ball-and-socket type as no plausible opening and closing jaw movements could be achieved otherwise with the model created (Figs. 11, 12). The ball of the joint readily found its place on the oral side of the palatoquadrate part protruding distally (laterally) beyond the suborbital. Here, there is a gap in the mineralized lining of the palatoquadrate cartilage. There is a reciprocal glenoid fossa incompletely ossified as a gap in the mineralized perichondral lining on the distal end of the Meckel's cartilage. This gap is shaped as a wide notch seen from both the oral and aboral sides of the lower jaw (Fig. 12, gf). In our reconstruction, the mandibular joint socket occupies this notch completely. This more closely resembles the specimen's shape and is more parsimonious than Young's (Reference Young1984) original reconstruction with the jaw articulation on the oral side of the notch and articulation with hyoid on its aboral side (his “ventral articular area”). Neither epihyal (hyomandibula) nor ceratohyal is known in the specimen CPC25205 or any other antiarchs. Moreover, there are no biomechanical reasons to hypothesize the presence of a hyostylic jaw suspension. This seems to have been either absent or nonfunctional, for example, reduced to compliant ligaments that did not restrict or guide jaw motions.

Figure 11. Reconstruction of Bothriolepis (based on specimen CPC 25205 from Gogo) jaws and jaw muscles within the oral fenestra in ventral view: (1) “mouth closed” position; (2) “mouth opened” position. Gray: dermal bones (suborbital and infragnathal); hatched: reconstructed keratinous sheath. The right side adductor mandibulae muscle is not shown to expose the ball-and-socket jaw articulation. AVL = anterior ventral lateral bone of the trunk carapace; IG = infragnathal; MC = Meckel's cartilage; PQ = palatoquadrate; SL = semilunar bone of the trunk carapace; SO = suborbital; mam = m. adductor mandibulae; mcm = m. coracomandibularis; mim = m. intermandibularis; mlpre (mlpal) = m. levator palatoquadrati or m. levator prelabialis. Not to scale.

Figure 12. Schematic presentation of Bothriolepis (based on specimen CPC 25205 from Gogo) jaw apparatus and jaw muscles: (1) kinematic scheme of mouth opening, anterolateral view from the right side; (2) lingual view of the right mandible showing the adductor mandibulae muscle and the glenoid fossa. IG = infragnathal; MC = Meckel's cartilage; PQ = palatoquadrate; SO = suborbital; gf = glenoid fossa; ks = keratinous sheath; mam = m. adductor mandibulae; mcm = m. coracomandibularis; mim = m. intermandibularis; mlpre (mlpal) = m. levator palatoquadrati or m. levator prelabialis. Not to scale.

The typical archaic palatoquadrate connection to the braincase in gnathostomes includes two points, the orbital anteriorly and palatobasal posteriorly. In the antiarchs, the jaws are very short and placed on the ventral side of the head, while the nares and eyes are tightly packed on the dorsal side. As a result, the palatoquadrates are placed far ventrally from the ethmoid region of the braincase. To overcome this incongruency, Stensiö (Reference Stensiö and Piveteau1969) reconstructed a high orbital process on the palatoquadrate. Young (Reference Young1984) refuted this high orbital process and suggested, instead, the presence of short orbital and palatobasal connections, on the basis of two respective gaps in the mineralized perichondral lining on the lingual (inner) side of the palatoquadrate, one closer to its mesial end and the other to the jaw joint, level to the distal (lateral) edge of the suborbital. For it to preserve palatoquadrate connections in the absence of its high processes, Young (Reference Young1984) hypothesized a certain anteroventral extension of the braincase toward the palatoquadrates, beneath the anterior wall of the skull roof, and termed this extension the subnasal shelf. In fact, it corresponds to the rostrum (“rostral process of ethmoid region”) of Stensiö (Reference Stensiö and Piveteau1969), and the presumed articulations of the palatoquadrate to it cannot be treated as orbital or palatobasal but rather preorbital or even prenasal.

It is not impossible that the two gaps in palatoquadrate perichondral lining mark the insertion of two ligaments attaching the upper jaw directly to the visceral side of the anterior wall of the skull roof, at the rostral margin of the oral fenestra. Whatever was the connection, the kinematics of the upper jaw seem unequivocal. Available data suggest that the upper jaw antimeres might protract and retract in a manhole-cover manner. In the retracted position, the suborbital was placed in the oral fenestra plane; in the protracted position, it became depressed at a right angle to this plane. The rotation axes of the left and right antimeres of the upper jaw, determined by the double suspensions (connections) of the palatoquadrates, were oriented at an obtuse angle to each other. Therefore, each half was depressed anteriorly and slightly laterally. In those antiarch genera in which the suborbitals were fused in the symphysis, they might become protracted only together with each other along the strictly transversal common axis of rotation.

As to the lower jaw mobility, manipulations with the model have shown that mouth opening was performed by means of combined depression and inward rotation of each lower jaw antimere around its longitudinal axis (Fig. 12.1). Mouth closing was performed by combined adduction and outward rotation. Only the ball-and-socket type of jaw articulation could provide this combined mobility simultaneously involving two degrees of freedom. Furthermore, the antimeres of the lower jaw are located at an angle to each other. Although this angle is obtuse, rotation of the two halves around their longitudinal axes not aligned with each other requires a compliant symphyseal ligament. In fact, the jaws of Bothriolepis and a number of other antiarchs consisted of four mutually mobile quadrants.

Four muscles are reconstructed (Figs. 11, 12; Supplementary Fig. 1). The one responsible for the upper jaw retraction presumably originated from the visceral surface of the anterior wall of the skull roof or from the rostral part of the braincase and passed below the aboral edge of the suborbital to insert on the aboral side of the palatoquadrate between two points of its suspension. This muscle might be homologous either to the elasmobranch m. levator palatoquadrati (innervated with mandibular branch of trigeminal nerve, V₃) or to the chimaeriform m. levator prelabialis (innervated with maxillary branch of trigeminal nerve, V₂) (Figs. 11, 12.1, mlpre (mlpal)). In extant gnathostomes, the latter muscle is the last remnant of the preoral visceral striated musculature (Mallatt, Reference Mallatt1996).

The function of the second reconstructed muscle is lower jaw depression. It might have belonged to hypobranchial somatic musculature (with hypoglossal innervation) preserved in all gnathostomes. Following the shark nomenclature, this muscle should be termed the m. coracomandibularis. Presumably, the m. coracomandibularis originated from the visceral side of the ventral trunk shield and ran rostrally along the midline, in close association with the contralateral muscle, to insert on the aboral margin of the lower jaw close to the symphyseal end of the Meckelian cartilage (Figs. 11, 12.1, mcm). This position of the m. coracomandibularis implies that depression caused by it was restricted, limited by the rostral margin of the trunk carapace. The position of the m. coracomandibularis implies that it might depress the lower jaw no more than at right angles to the ventral plane of the trunk shield, the maximum possible range of mouth opening.

The third muscle is the m. adductor mandibulae (innervated with the mandibular branch of trigeminal nerve, V₃) connecting the upper and the lower jaws and closing the mouth. Gross (Reference Gross1941) reconstructed this muscle in Grossilepis tuberculata as running directly from the upper to the lower jaw. However, with such a placement, the length difference of muscle fibers between the mouth-closed and mouth-opened positions would exceed the known properties of striated musculature, or otherwise, the mouth opening would be improbably restricted by the shortening range of the muscle fibers. Therefore, we reconstruct the m. adductor mandibulae as extending over the labial margin of the Meckel's cartilage to insert across its expanded aboral surface up to the scars found in specimens PIN 3725/1118 and PIN 3725/1119 on the lingual side of the infragnathal bone at the distal end of its curved oral division (Figs. 11, 12.2, mam). It might be hypothesized that the muscle was bipennate, with a single tendon of origin from which the deeper muscle fibers ran to the Meckel's cartilage, and the superficial muscle fibers ran to the superficial aponeurosis, which terminated on the aforementioned scars on the infragnathal. To avoid traumatizing the muscle itself by the distal part of the oral margin (presumably covered with a keratin blade) of the suborbital at mouth closure, we reconstruct the m. adductor mandibulae origin on the palatoquadrate in close proximity to the mandibular joint. Thus, the origin of the m. adductor mandibulae was closer to the jaw articulation than to the insertion. As a result, the muscle extended from the upper to the lower jaw obliquely, somewhat along the lower jaw. Consequently, contraction of this muscle pulled the lower jaw not only upward and forward, but also laterally. The shape of the jaw joint in the specimen CPC25205 supports this conclusion since the notch on the distal end of Meckel's cartilage is exactly what is required to counterbalance the lateral pull of the obliquely reconstructed m. adductor mandibulae.

The fourth muscle is the m. intermandibularis (innervated with the mandibular branch of trigeminal nerve, V₃) preserved in all gnathostomes. It might have run transversely, connecting the aboral margins of the infragnathal antimeres (Figs. 11, 12.1, mim). This muscle is normally composed of two contralateral muscles meeting in the floor of the mouth and forming a tendinous interconnection along the midline. Most probably, this muscle attachment on the lower jaw was associated with the scars and notch found in specimens PIN 3725/1118 and PIN 3725/1119 on the labial side of the infragnathal bone at the distal end of its curved biting portion, as well as on the adjacent segment of the Meckel's cartilage. Thus, the m. intermandibularis attachment might have occupied an area between the insertion of the m. coracomandibularis and the belly of the m. adductor mandibulae wrapped around the distal expanded part of the Meckel's cartilage. The proposed function for the m. intermandibularis in antiarchs is the outward rotation of the mandibular antimeres during mouth closure. The muscle should have been strong enough as its presumed force of contraction should be concordant with the extensive development of the aforementioned scars especially developed in the Livnolepis specimen.

Thus, the m. adductor mandibulae is an antagonist for the other three jaw muscles. Its retracting of the upper jaw is opposed by protraction by the levator muscle, adducting the lower jaw—by depressing it by the coracomandibularis muscle, rotating the lower jaw inwards—by its outward rotation by the intermandibularis muscle. The last antagonism is visibly indicated by opposition of the respective m. adductor mandibulae and m. intermandibularis scars on the infragnathal. The m. adductor mandibulae should have been the largest muscle, followed by the m. intermandibularis and further by two subequal ones, the m. levator palatoquadrati (or m. levator prelabialis) and m. coracomandibularis.

With respect to feeding modes, the cartilaginous branchial arches themselves are not preserved; nevertheless, some consideration of the space in which these were held (and so size and potential complexity of the apparatus) can be made. In yunnanolepids, the anterior transverse crista, located on the visceral surface of the anterior ventral trunk shield, occurs along with an ornamented postbranchial lamina (e.g., Wang and Zhu, Reference Wang and Zhu2018). This ornamented lamina is located at the rostral margin of the trunk shield, marking the rear of the branchial cavity, comparable to the mesially directed and ornamented flange of the pectoral girdle in actinopterygians such as Acipenser (Jessen, Reference Jessen1972, fig. 5.2). In other antiarch groups, the postbranchial lamina has been lost, with the anterior transverse crista more posteriorly placed relative to the anterior margin of the trunk shield (e.g., Bothriolepis canadensis, Stensiö, Reference Stensiö1948, text-fig. 164A). This suggests additional space for the branchial arches, compared with the yunnanolepids. The submarginal is located at the lateral margin of the head shield and effectively forms the moveable bony plate covering the branchial region. With a larger branchial cavity (putatively longer branchial arches) and a moveable submarginal in the Asterolepidoidei and the Bothriolepidoidei, these antiarchs might have generated a significant water flow through the orobranchial chamber that made restricted suction feeding possible.

Despite Young's (Reference Young1984) opinion on the possibility of occlusion, manipulations with the reconstruction have shown that no occlusive interactions of the blades of the upper and the lower jaw were possible. The dermal bones of the jaws, capped by hard keratinous blades, might have acted like half-round wood chisels scraping the substrate as they moved toward each other but never met. In the lateral view, the protracted upper jaw is two times shallower than the depressed mandible. Therefore, if the fish attempted to scrape the horizontal aquatic beds, it should have inclined its body head first at approximately 45° (Fig. 13). The peculiar feature of jaw mobility found during manipulations with the model is a combination of the lower jaw adduction with the outward rotation of its antimeres powered by the m. intermandibularis. An opposite movement combining closure with inward rotation was recently suggested in Ferromirum oukherbouchi Frey et al., Reference Frey, Coates, Tietjen, Rücklin and Klug2020, a Late Devonian symmoriiform chondrichthyan (Frey et al., Reference Frey, Coates, Tietjen, Rücklin and Klug2020). Inward rotation of the lower jaw during a bite, like in Ferromirum, is apparently advantageous to pierce the prey. Outward rotation of the lower jaw during mouth closure, like in Bothriolepis, could help in maintaining an optimal cutting angle between the lower jaw half-round wood chisel and the substrate throughout mouth closure while scraping. This scraping action might have been enhanced by mutual outward–inward rotating motion of the curved infragnathal half-round wood chisel resulting from antagonistic interaction of the adductor mandibulae and intermandibularis muscles during mouth closure.

Figure 13. Whole-head reconstruction of Bothriolepis in feeding position in the right-side view with mouth open. IG = infragnathal; MC = Meckel's cartilage; PQ = palatoquadrate; SO = suborbital; mam = m. adductor mandibulae; mcm = m. coracomandibularis; mlpre (mlpal) = m. levator palatoquadrati or m. levator prelabialis. Not to scale.

The closest analogue for the feeding mechanism suggested here for antiarchs is found in the extant anuran tadpoles (e.g., de Jongh, Reference de Jongh1968; Bonacci et al., Reference Bonacci, Brunelli, Sperone and Tripepi2008; Venesky et al., Reference Venesky, Wassersug, Jorgensen, Riddle and Parris2011), despite their much smaller size. While scraping the substrate, they simultaneously suck in the scraped particles by uninterrupted breathing movements. Similarly, antiarchs would not cease to pump water through their mouth and pharynx by oscillatory movements of the submarginal bone. In anuran tadpoles, such a scraping mouth makes possible a wide range of derived applications as presented by Candioti (Reference Candioti2007). Similarly, antiarchs, by small morphological variations, could change the use of their jaw apparatus from picking algae to a wide range of feeding specializations, probably even carnivory as demonstrated by Occidozyga baluensis (Boulenger, Reference Boulenger1896) tadpoles (Haas et al., Reference Haas, Pohlmeyer, McLeod, Kleinteich, Hertwig, Das and Buchholz2014).

Feeding mode of antiarchs

In his Reference Stensiö1931 paper, Stensiö noted that nothing could be stated about the feeding mode of the antiarchs, although he and later authors focused on the morphofunctional interpretation of the shape of the antiarch trunk shield and pectoral fins, consistently interpreting these animals as bottom dwellers capable of fast occasional swimming, possibly escaping from predators.

Denison (Reference Denison1941, Reference Denison1961) described the alimentary tract in Bothriolepis canadensis noting its straightness and absence of a stomach but presence of a large spiral valve in the intestines. This structure had been reconstructed on the basis of its infilling; part of it is composed of fine muddy or silty rock usually present in the posterior part of the reconstructed gut. Frequent presence of carbonaceous material indicated that plant food formed an important part of the diet. Because of these data, Denison suggested that Bothriolepis was a mud-grubber, living much as does an earthworm on digestible material in the mud it swallows. As such, it was a bottom feeder, indicated independently by the ventral position of its mouth. Since this paper, this interpretation became canonical. Interpretation of Bothriolepis canadensis and other antiarchs as benthivorous, bottom-dwelling fishes was later supported by many authors (for example, Watson, Reference Watson1961; Moloshnikov, Reference Moloshnikov2008; Cloutier et al., Reference Cloutier, Proust and Tessier2011).

Johanson (Reference Johanson1998) suggested that “weak” ventral mouths of Bothriolepis and Remigolepis had been adapted for taking small food particles from the sediment surface, or even processing the sediment itself.

Upeniece (Reference Upeniece2001, Reference Upeniece2011) described distinctive concentrations of mineral matter different from the surrounding matrix within the anterior part of the trunk of juvenile Asterolepis ornata individuals seen in more than 100 specimens. A similar position of these concentrations in numerous specimens suggested that these structures might represent the lifetime position of the digestive tract. These infillings consist of coprolitic-like matter otherwise found separately outside the specimens as discrete coprolites in the same clay lens, being composed of quartz grains, carbonaceous matter, and detritic-like bone material. Upeniece (Reference Upeniece2001, Reference Upeniece2011) followed Denison's (Reference Denison1941) interpretation of this content as demonstrating a mud-grubbing mode of feeding in Asterolepis, similar to that in Bothriolepis. The main argument to support this was the observation that the presumable gut infillings in the trunk differed in lithology from that of the surrounding sediment but agreed with the content of isolated coprolites. However, if antiarchs consumed sediment as it was, the gut content would be indistinguishable in composition from the surrounding sediments. Differentiation of the sediment might be achieved only in the case that it was primarily sorted in the mouth, then smaller particles removed through the gill opening. Cloutier et al. (Reference Cloutier, Proust and Tessier2011) and Cloutier (Reference Cloutier2013) studied the gut contents of Bothriolepis canadensis and found the valves of the conchostracan Asmusia membranacea (Martens, Reference Martens, Schultze and Cloutier1996), which most likely lived in the water column and near the bottom, but these might be swallowed together with any other food mass. Strictly speaking, any substance scraped off the bottom surface is mud, containing inclusions.

A significant amount of the nutritional matter is constituted by various algae in the sea or any other plants in the continental basins. This plant matter could be scraped off the substrate and afterward mechanically processed. This transformation might be regarded as a transitional stage between mud filtering and herbivory. If we regard predation as a derived filter feeding, that is, extraction of a single rather than numerous prey objects from the environment, eating plants may be regarded as a derived type of filtration of sediment rich in organic matter. Partial herbivory is supported by an immense spiral valve in Bothriolepis canadensis (Denison, Reference Denison1941) used to house a large quantity of reducing bacteria and to slowly transport a large amount of food matter, maximizing the removal of nutrients.

Most researchers studying antiarch feeding and supporting the mud-grubbing hypothesis (Romer and Grove, Reference Romer and Grove1935; Denison, Reference Denison1941, Reference Denison1961; Upeniece, Reference Upeniece2001) focused on the “weak” structure of the infragnathals in Bothriolepis canadensis and other members of this group. Our survey of jaw apparatuses revealed a wide morphological spectrum of antiarch gnathals. Oral blades of “Livnolepis,” the strongest biter among antiarchs, and Bothriolepis sp. infragnathals from Livny are robust, arched, and deep, in contrast to those known in many other antiarchs, and capable of scratching and/or shearing tough food objects. We suggest here that an observed variety of jaw morphologies in various antiarch taxa reflects a wide spectrum of their trophic adaptations, most probably including herbivory.

In the aquatic assemblage, these food objects might be classified according to their resistance to mechanical processing by consumers into the following groups: (1) hard (shelled mollusks, hard-shelled arthropods and brachiopods, corals, and most echinoderms, such as sea urchins), (2) tough or dense (thallus algae, vascular plants, thin-shelled mollusks, arthropods, and brachiopods), and (3) soft (hydrozoan and scyphozoan coelenterates, ctenophores, and various worms). A separate nutritional group (4) includes micromeric objects dispersed in water and bottom sediments (bacteria, unicellular algae, protozoans, small arthropods, and various larvae).

Of these, hard-shelled animals might be easily excluded from the list of the potential antiarch food items. It is not impossible that some antiarchs fed on micromeric objects; however, we have neither direct morphological nor paleoecological evidence for this. Soft-bodied animals seem to be suitable food objects for antiarchs with less-arched gnathal elements. For those with deeper and arched oral blades, we may suggest nutritional specialization on tougher food objects, including thallus algae and arthropods with thin carapaces. Highly abundant genera, such as Bothriolepis and Remigolepis, were most probably herbivorous and fed on thallus algae scraped from the substrate.

The dispersal of antiarchs during the Devonian

Vertebrate assemblages presenting the oldest antiarchs are described from the Silurian of China (Zhao and Zhu, Reference Zhao and Zhu2010) from the territory of the Pan-Cathaysian galeaspid province. The oldest antiarchs (Telychian, late Llandovery) have been found in association with the agnathan galeaspids and other vertebrates (Fig. 14.1). Starting from the Lochkovian, the composition of the communities including antiarchs changed. Galeaspid agnathans still dominated numerically, but antiarchs had become the second most numerous vertebrate group. All known localities are thought to be formed in shallow-marine conditions. The percentage of antiarch taxa in assemblages indicated they became prevalent starting from the late Eifelian; from this time until the end of the Famennian, the depositional environments varied from shallow-water marine to lacustrine (Zhao and Zhu, Reference Zhao and Zhu2010). Increasing numbers of antiarchs suggests their success in the occupation of the new ecological niches and a certain degree of euryhalinity.

Figure 14. Paleogeographic dispersal of antiarchs and armored agnathans. (1) Global dispersal during the Silurian–Devonian. (2) Diversity curves for antiarch placoderms and osteostracan, cyathaspidiform, and pteraspidiform agnathans of Laurussia. Note the Eifelian–Frasnian increase of antiarchs versus the decline of agnathan groups. Diversity curves based on unpublished database in PIN RAS.

During the Emsian, the antiarchs expanded to Gondwana, and at the beginning of the Eifelian, to Euramerica (Young, Reference Young1990, Reference Young2010; Young et al., Reference Young, Burrow, Long, Turner and Choo2010) (Fig. 14.1). The extinction of the cyathaspidiform and most of the pteraspidiform agnathans by the Eifelian in Euramerica coincided with the antiarch invasion to these new territories (Fig. 14.2) rich in resources. Filter-feeding agnathans (Denison, Reference Denison1961) and mainly macrophytophagous scraping bothriolepidoid antiarchs exploited different food types. These vertebrates co-occurred within the same trophic webs and might have competed for common occupation of bottom-dwelling environments or some other yet unknown ecological parameter. During the Eifelian–Frasnian interval, antiarchs successfully shared space with the osteostracans, anaspids, and especially remaining pteraspidiform psammosteids.

We suggest here that antiarchs became the first phytophagous vertebrates that occupied the trophic level of primary consumers during the late Silurian–Early Devonian. This novel way of antiarch feeding might have influenced the water plant community and ecosystem as a whole. Previously existing simple predator–prey structure of vertebrate trophic chains between filter-feeding agnathans and predatory gnathostomes thus became remodeled.