Introduction
A conodont natural assemblage is a fossil of its skeletal elements juxtaposed on a bedding plane from which it is possible to discuss the homology of the elements within the conodont apparatus. Knowledge of homology allows deduction of relationships among taxa, and thus improved knowledge of the phylogeny of conodonts. Logical and statistical methods can be applied to taxa for which evidence of natural assemblages or clusters is not available for multielement apparatus reconstructions (e.g., Walliser, Reference Walliser1964; Webers, Reference Webers1966; Jeppsson, Reference Jeppsson1971; Dzik, Reference Dzik1991). The apparatus structure of the genus Hindeodus, the subject of this study, is currently poorly understood. This genus has a long stratigraphic range, from the lower Carboniferous (Mississippian) to the lowermost Triassic. When Rexroad and Furnish (Reference Rexroad and Furnish1964) first described the morphogenus Hindeodus, they designated Hindeodus imperfectus (=Trichonodella imperfecta Rexroad, Reference Rexroad1957) as the type species. This morphospecies, a symmetrical crown-shaped element, was incorporated into the multielement apparatus of Hindeodus cristulus (=Spathognathodus cristulus Youngquist and Miller, Reference Youngquist and Miller1949) as the Sa element by Sweet (Reference Sweet1977). According to Sweet’s definition, Hindeodus has a skeletal apparatus comprising six kinds of elements: Pa, Pb, M, Sa, Sb, and Sc.
The morphological variety of Hindeodus Pa elements causes them to be generally useful for biostratigraphy, whereas the associated ramiform elements appear to be somewhat difficult to distinguish as separate species. Sweet (Reference Sweet1977), who defined multielement Hindeodus, described four species, including H. cristulus and H. typicalis (Sweet, Reference Sweet1970a), and reconstructed four ramiform complexes, consisting of Pb, M, Sa, Sb, and Sc elements, for those species. He described the morphological characters of these ramiform elements and mentioned that it was difficult, at least in part, to assign dissociated specimens to each species. The ramiform complex has often confused the classification of both species and genera. This problem emerged as part of the “Hindeodus-Diplognathodus Problems” (von Bitter and Merrill, Reference von Bitter and Merrill1985, p. 81). In any case, for discrimination of the element set forming a Hindeodus apparatus, it is necessary to examine closely the stratigraphic co-occurrence and similarities of morphological characters between ramiform and Pa elements.
In general, the morphological variation of the Pa element and of the ramiform complex of Hindeodus species was relatively monotonous from the late Carboniferous to the middle Permian (Sweet, Reference Sweet1988; Nicoll et al., Reference Nicoll, Metcalfe and Wang2002). In contrast, during the late Permian to earliest Triassic, Hindeodus evolved rapidly into more than 10 species, the Pa elements of which have been reported in many papers discussing the biostratigraphy of the Permian-Triassic Boundary (PTB) (e.g., Kozur, Reference Kozur1995; Lai et al., Reference Lai, Yang., Hallam and Wignall1996; Nicoll et al., Reference Nicoll, Metcalfe and Wang2002). Apparatus reconstruction and description of ramiform complexes have been undertaken mainly for the early Carboniferous species H. cristulus and H. scitulus (Hinde, Reference Hinde1900), and PTB species including H. typicalis, H. julfensis (Sweet in Teichert et al., Reference Teichert, Kummel and Sweet1973), H. latidentatus (Kozur, Mostler, and Rahimi-Yazd, Reference Kozur, Mostler and Rahimi-Yazd1975), H. parvus (Kozur and Pjatakova, Reference Kozur and Pjatakova1976), H. changxingensis Wang, Reference Wang1995, H. postparvus Kozur, Reference Kozur1989, and H. sosioensis Kozur, Reference Kozur1996 (e.g., Sweet, Reference Sweet1977, Reference Sweet1988; von Bitter and Plint-Geberl, Reference von Bitter and Plint-Geberl1982; von Bitter and Plint, Reference von Bitter and Plint1987; Kozur, Reference Kozur1996).
From the cladistic analysis of Donoghue et al. (Reference Donoghue, Purnell, Aldridge and Zhang2008), the genus Hindeodus currently belongs to the superfamily Polygnathacea, suborder Ozarkodinina, order Ozarkodinida. That analysis used the premise that the multielement reconstruction of this genus proposed by Sweet (Reference Sweet1977) and others is strongly reliable. In this study, the apparatus of the earliest Triassic conodont H. parvus is reconstructed using synchrotron radiation micro-tomography (SR–μCT). Our conclusion supports Donoghue and his colleagues’ premise and provides a taxonomic framework for the genus.
Materials and methods
Agematsu et al. (Reference Agematsu, Sano and Sashida2015) described natural assemblages of H. parvus and H. typicalis from siliceous claystones of the Hashikadani Formation, which forms part of the Mino Terrane, a Jurassic accretionary complex in central Japan. Their study section (3.8 m thick) consists of uppermost Permian chert and lowermost Triassic black claystone; the latter contains conodonts (Fig. 1). Because all specimens are preserved as impressions and some additional elements may be hidden under the visible molds, the composition of the assemblages cannot be completely observed under binocular or scanning electron microscopes. According to Agematsu et al. (Reference Agematsu, Sano and Sashida2015), the assemblages of both species comprise at most 13 elements, including pairs of P1, P2, and M elements, as well as a single S0 element with two digyrate and four bipennate elements making up the S array. A pair of S1 elements was not recognized. In this study, the multielement apparatus of H. parvus is reconstructed using SR–μCT.
Figure 1 Locality and horizon of the conodont natural assemblage: (1) locality map of the study section; (2) lithologic column of the study section indicating the sample horizon.
SR–μCT measurements were performed at experimental hutch 1 of BL20B2 in the synchrotron radiation facility, SPring-8, Hyogo, Japan (Goto et al., Reference Goto, Takeshita, Suzuki, Ohashi, Asano, Kimura, Matsushita, Yagi, Isshiki, Yamazaki, Yoneda, Umetani and Ishikawa2001). Claystone samples containing natural conodont assemblages were cut into small pieces ~10–20 mm high, 5–10 mm wide, and 2–5 mm thick. The measurement conditions of the mirco-tomography were as follows: X-ray energy was 15–35 keV; number of projections was 1800 for 180 degrees; exposure time for one projection was 200 msec; total scan time of one CT measurement was ~8 minutes; effective pixel size was 2.76 μm; distance from the sample to detector was set to 70 mm.
The CT reconstruction was done with convolution back projection method (Uesugi et al., Reference Uesugi, Hoshino, Takeuchi, Suzuki, Yagi and Nakano2010) after phase retrieval (Paganin et al., Reference Paganin, Mayo, Gureyev, Miller and Wilkins2002). Three-dimensional images were built from the stacked 2D images with volume rendering using the open-source visualization software Drishti (Limaye, Reference Limaye2012).
Nineteen samples were analyzed, of which two yielded well-preserved fossil images. Figure 2 illustrates specimens of the ventral and dorsal parts of the assemblage, which originally constituted one natural assemblage. The images include the claystone-air interface and distinctly show the outline of each element. This fossil was recovered from a horizon 40 cm above the base of the claystone strata, which is correlated with the lower Induan (Sano et al., Reference Sano, Kuwahara, Yao and Agematsu2010).
Figure 2 Three-dimensional images of the natural assemblage of Hindeodus parvus (Kozur and Pjatakova, Reference Kozur and Pjatakova1976) from the horizon 11C of the NF1212R section, the upper part of the Hashikadani Formation: (1.1–1.3) ventral view of the ventral specimen (EESUT-ag0005); (2.1–2.3) dorsal view of the dorsal specimen (EESUT-ag0006). Scale bar indicates 500 μm.
Repository and institutional abbreviation
Two specimens described herein are deposited at the Doctoral Program in Earth Evolution Sciences, University of Tsukuba, Japan, with the prefix EESUT.
Systematic paleontology
Order Ozarkodinida Dzik, Reference Dzik1976
Suborder Ozarkodinina, Dzik, Reference Dzik1976
Superfamily Polygnathacea Bassler, Reference Bassler1925
Genus Hindeodus Rexroad and Furnish, Reference Rexroad and Furnish1964
Type species
Spathognathodus cristulus Youngquist and Miller, Reference Youngquist and Miller1949, from the Mississippian of south-central Iowa, USA, by original designation.
Hindeodus parvus (Kozur and Pjatakova, Reference Kozur and Pjatakova1976)
Figure 3 Colored pictures of H. parvus: (1.1–1.5) ventral view of the ventral specimen (EESUT-ag0005); (2.1–2.5) dorsal view of the dorsal specimen (EESUT-ag0006). Scale bar indicates 500 μm.
Multielement
1975 Anchignathodus parvus; Reference KozurKozur, p. 7, pl. 1, figs. 17, 22 (P1), 21(S3-4).
1976 Anchignathodus parvus Kozur and Reference Kozur and PjatakovaPjatakova, p. 123, pl. 1, figs. a, b, e (P1), h (S3-4).
1995 Hindeodus parvus; Reference KozurKozur, p. 69, pl. 2, figs. 4, 6, 9, 13 (P1), pl. 3, figs. 1–4 (P1), 5 (M), 6 (S1-2), 7 (P2), 8 (S3-4).
1995 Hindeodus parvus; Reference Kozur, Ramovš, Wang and ZakharovKozur et al., p. 206, pl. 1, figs. a, b, g (P1), e (S1-2).
1996 Hindeodus parvus; Reference KozurKozur, p. 94, pl. II, figs. 5, 6, 7, 8 (P1), pl. III, figs. 1–3, 9, 11 (P1), 4 (S0), 5 (M), 6, 10 (S1-2), 7 (P2), 8 (S3-4), pl. IV, figs. 5, 6, 7 (P1).
2015 Hindeodus parvus; Reference Agematsu, Sano and SashidaAgematsu et al., p. 1285, figs. 2–4.
Holotype
Carminiscaphate form from the lowermost Triassic of Achura, Azerbaijan (Kozur and Pjatakova, Reference Kozur and Pjatakova1976, pl. 1, fig. b).
Description
Natural assemblage consists of ventral and dorsal specimens. The former contains 14 elements: sinistral–dextral pairs of P1, P2, S2, S3, and S4; single S0; dextral S1; and parts of paired M elements. The latter mainly comprises a ramiform cluster, including sinistral–dextral pair of M, sinistral S1, and parts of S2, S3, and S4 elements.
Carminiscaphate P1 bears the largest distal denticle on an ‘anterior’ process. That denticle is twice as high as the other five, accompanied by accessory node on ‘posterior’ end of unit. Basal cavity expands ‘laterally,’ occupying ‘posterior’ two-thirds of element. P2 angulate, with long robust cusp and short ‘anterior’ process bearing large denticle. Relatively long ‘posterior’ process carrying at least a number of short denticles twists distally; its ‘inner’ surface faces medial side. Small basal cavity opens under cusp. Makellate M with long slender cusp, very short ‘inner lateral’ process, and denticulate ‘outer lateral’ process with relatively long denticle adjoining cusp. Unit bends sharply ‘posteriorly’ just ‘outside’ cusp.
S0 symmetrical alate lacking ‘posterior’ process; both ‘lateral’ processes high and short. Digyrate elements in S1–2 positions possess long robust cusp and denticulate ‘inner’ and ‘outer lateral’ processes, although distal parts of ‘outer lateral’ processes of both S1 elements not preserved in this material. ‘Inner lateral’ process higher and shorter than ‘outer lateral’ one; the latter twists at joint and its ‘posterior’ surface turns ‘upward’. Bipennate elements in S3–4 positions characterized by long slender cusp, denticulate long ‘posterior’ process, and short ‘anterior’ process bearing relatively long ‘antero-terminal’ denticle.
Materials
Two clusters constituting one natural assemblage: EESUT-ag0005, 0006.
Remarks
On the basis of the morphology of the P1 and S1–2 elements, the specimens are identified as H. parvus. According to Kozur (Reference Kozur1996), the S1–2 element of this species is distinguished from those of H. typicalis and H. latidentatus (Kozur, Mostler, and Rahimi-Yazd, Reference Kozur, Mostler and Rahimi-Yazd1975) by the bending position of the unit: the S1–2 elements of the latter two species bend ‘posteriorly’ just ‘outside’ a cusp; in contrast, those of H. parvus bend ‘posteriorly’ just ‘inside’ a cusp. Because both the sinistral and dextral S1 elements in the present specimens are broken just ‘inside’ the cusp, these cracks indicate the bending position. This feature of the S1–2 elements is consistent with H. parvus.
Results and discussion
Natural assemblage of Hindeodus parvus
The SR–μCT images clearly show that an apparatus of H. parvus is composed of 15 elements settled in sinistral–dextral pairs in the P1, P2, M, S1, S2, S3, and S4 positions and a single S0 position probably on the median plane (Figs. 3, 4; Supplemental Data 1). The element structure is in agreement with the definition of Hindeodus by Sweet (Reference Sweet1977). The SR–μCT images also clarify the three-dimensional microarchitecture of the natural assemblage in terms of the general location and direction of elements in the apparatus.
Figure 4 Drawings of the reconstructed assemblage based on the ventral and dorsal specimens. The upper one represents the dorsal view of the assemblage and the lower represents the ventral view. The rostral and caudal sides mean that these are nearer head and tail ends of a conodont body, respectively.
A crown-shaped alate element without a ‘posterior’ process, the S0 element, lies on the rostralmost side of the specimens. The element has the ‘upper’ side turned rostrally and the ‘anterior’ surface ventrally. It is probable that the element is on the median plane and its ‘anterior’ surface was oriented in the ventral or rostral direction in the living conodont body. The central parts of the specimens are made up of ramiform clusters, consisting of juxtaposed elements in the S1–S4 and M positions. The so-called S array, which is the main part of the ramiform cluster, comprises two pairs of digyrate S1–2 elements on the inside and two pairs of bipennate S3–4 on the outside. Although a sinistral S1 element is out of place, the ‘inner lateral’ and ‘outer lateral’ processes of the other digyrate elements point to the rostral and caudal directions of the apparatus, respectively. Their ‘posterior’ surfaces face ventrally. The bipennate elements have their cusp and a terminal denticle on an ‘anterior’ process pointing in the rostro-inner direction, and with a ‘posterior’ process extending caudally. The ‘inner’ surfaces of these elements are turned to the ventral side of the specimen. Two makellate elements, located in the M positions, lie on the dorso-sinistral and -dextral sides of the S array with cusps pointing to the rostro-inner side and the ‘outer lateral’ process at the caudal side. The ‘posterior’ side faces ventrally. It is quite likely that the ‘outer lateral’ processes of the S1–2 and M elements and the ‘posterior’ ones of the S3–4 elements were arranged approximately parallel to the rostro-caudal axis in the living conodont body. In addition, all elements in the ramiform clusters seem to have their concave surfaces directed ventrally or inwardly as a whole.
A pair of angulate elements in the P2 position is placed between the caudal half of the sinistral and dextral S arrays. The ‘inner’ sides face ventrally. The ‘upper’ or ‘inner lateral’ surfaces appear to be opposite each other across the median plane. In the caudalmost part, there are P1 positions in which two carminiscaphate elements are disposed. Although the posture of the P1 elements in the living conodont body is unclear, the ‘upper’ surfaces at least appear to face each other.
This arrangement and direction of elements is also supported by the natural-assemblage specimens analyzed by Agematsu et al. (Reference Agematsu, Sano and Sashida2015). This reconstruction is nearly identical to a well-known apparatus model of ozarkodinids including 4P-2M-9S elements (Purnell and Donoghue, Reference Purnell and Donoghue1997; Purnell et al., Reference Purnell, Donoghue and Aldridge2000).
Terms for orientation of S 1–2 elements
Elements disposed in the S1–2 and S3–4 positions have been labeled Sb and Sc, respectively, in previous studies. Sweet (Reference Sweet1988) stated that the Sb element was the most diagnostic feature of the Hindeodus apparatus. According to Kozur (Reference Kozur1996), the morphological differences of some Hindeodus Sb elements are sufficient to help with identification of species. However, the terms for orientation of the digyrate elements have been confused, and thus need to be summarized here.
Most papers reporting Hindeodus S1–2 elements and their equivalents have described the two processes of the element as the ‘anterior’ and ‘posterior’ ones, whereas Sweet (Reference Sweet1977) defined the Sb element as a digyrate form with two ‘lateral’ processes. The present study follows the usage of Sweet and describes these processes as ‘lateral.’ An additional problem is that many previous studies have stated that the S1–2 elements of Hindeodus are characterized by an ‘upwardly’ bent process (e.g., Sweet, Reference Sweet1988). This character is sometimes difficult to discriminate. The LE element of Ellisonia teicherti Sweet, Reference Sweet1970a, which is included in some Hindeodus species as part of the ramiform complexes, is equivalent to the S1–2 elements. Sweet (Reference Sweet1970b) described that an ‘anterior’ process of the LE element “projected laterally and upward” (Sweet, Reference Sweet1970b, p. 233). This element is homologous with the Pl element of Ellisonia teicherti?, which was described by von Bitter (Reference von Bitter1972), and the A2 element of Ozarkodina minuta (Ellison, Reference Ellison1941) (=Hindeodus minutus) of Baesemann (Reference Baesemann1973). The Pl element is characterized by “an anterior bar that is directed sharply upward” (von Bitter, Reference von Bitter1972, p. 71), whereas the A2 element possesses a ‘posterior’ process with “upswept posterior end” (Baesemann, Reference Baesemann1973, p. 706). Matsuda (Reference Matsuda1981), however, gives the clearest explanation for the morphology of the Sb element. According to him, the ‘anterior’ process of the element bends ‘inward’ around a cusp and the ‘inner’ surface of the ‘anterior’ process faces slightly ‘upward’ as a result of twisting at the bend. It seems that all previously illustrated S1–2 elements of Hindeodus possess a process with a similar bend and twist. The present study describes the bent and twisted process of a digyrate element as an ‘outer lateral’ process. That is, the S1–2 element bears two ‘lateral’ processes and bends around the cusp; the ‘outer lateral’ process twists at the bend and turns its ‘posterior’ surface ‘upward.’ The ‘outer lateral’ process, which can be compared with the ‘anterior’ processes or bars of Sweet (Reference Sweet1970b), von Bitter (Reference von Bitter1972), Matsuda (Reference Matsuda1981), and Kozur (Reference Kozur1996), and the ‘posterior’ process of Baesemann (Reference Baesemann1973), extends caudally in the conodont apparatus.
Conclusions
Although previous multielement reconstructions have strongly suggested a similarity between the apparatuses of Hindeodus and other ozarkodinids, the natural assemblages described by Agematsu et al. (Reference Agematsu, Sano and Sashida2015) were insufficient to determine whether the S1 element was present. In this study, SR–μCT images of H. parvus specimens show that the element composition is consistent with the multielement definition of this genus given by Sweet (Reference Sweet1977) and that the 15-element plan is quite similar to a well-known ozarkodinid model. These data will be useful for future studies of the classification and phylogeny of Hindeodus.
Acknowledgments
We express sincere thanks to M.J. Orchard for his useful suggestions and comments. The synchrotron radiation experiments were performed at the BL20B2 of SPring-8 with the approval of the Japan Synchrotron Radiation Research Institute (JASRI) (Proposal No. 2014B1442).
Accessibility of supplemental data
Data available from the Dryad Digital Repository: http://dx.doi.org/10.5061/dryad.488rt
