First Skeletal Fossil Record of the Red Seabream Pagrus major (Sparidae, Perciformes) from the Late Pleistocene of Subtropical West Pacific, Southern Taiwan

© 2022 Academia Sinica, Taiwan Open Access First Skeletal Fossil Record of the Red Seabream Pagrus major (Sparidae, Perciformes) from the Late Pleistocene of Subtropical West Pacific, Southern Taiwan Chien-Hsiang Lin1,* , Hsin-Yueh Ou2, Chia-Yen Lin1, and Hong-Ming Chen3 1Biodiversity Research Center, Academia Sinica, Taipei, Taiwan. *Correspondence: E-mail: [email protected] (CH Lin). E-mail: [email protected] (Lin) 2Department of Life Science, Tunghai University, Taichung, Taiwan. E-mail: [email protected] (Ou) 3Department of Aquaculture, National Taiwan Ocean University, Keelung, Taiwan. E-mail: [email protected] (Chen) Received 7 July 2021 / Accepted 28 January 2022 / Published 5 May 2022 Communicated by Felipe Ottoni Fish fossils are only occasionally found in Taiwan, and such fossils are rarely appropriately analyzed and described. Despite their sparse records, several Plio-Pleistocene localities rich in marine organisms have yielded well-preserved specimens, potentially providing insight into the rarely identified fish fauna in the tropical-subtropical West Pacific. We describe a sandstone nodule containing fish skeletons from the Late Pleistocene Szekou Formation in southern Taiwan. The specimen includes nearly complete left jaws, fragmentary right jaws, and part of the anterior body. The distinct dentition of the specimen suggests it to be a member of Sparidae family. Further morphological analysis based on dentition and a comparison with 153 recent specimens belonging to 14 sparid species in the area enabled us to assign the fossil to the species Pagrus major. We found that the characteristic sparid tooth patterns are useful in generic determination, at least in Taiwan. The occurrence of the specimen is the first evidence of P. major in the region. Finally, the specialized tooth pattern and the estimated size indicate that the fish was a middle-totop predator that fed on small fish and invertebrates in a neritic lagoonal environment. Key words: Dentition, Morphology, Paleoecology, Szekou Formation, Taxonomy. Citation: Lin CH, Ou HY, Lin CY, Chen HM. 2022. First skeletal fossil record of the red seabream Pagrus major (Sparidae, Perciformes) from the Late Pleistocene of subtropical West Pacific, southern Taiwan. Zool Stud 61:10. doi:10.6620/ZS.2022.61-10. BACKGROUND Fish fossils from Taiwan are sparsely described in various local reports (see Lin et al. 2021 and the references therein). Only two relatively complete skeletal fossils (Tao 1993a b) and several isolated teeth and otoliths have been identified (e.g., Tao and Hu 2008; Lin et al. 2018; Lin and Chien 2022). Several marine deposits have yielded numerous marine fossils, but relevant research endeavors in academia are insufficient, and efforts are often limited to those of amateur collectors (Lin et al. 2021). Thus, the lack of extensive fossil records hinders our understanding of past fish fauna and formation of the present diversity hotspot in the tropical-subtropical West Pacific (Lin et al. 2021). One locality rich in fossils is the Hengchun Peninsula, in southern Taiwan (Hu 1991). The site encompasses fossils from the Late Pleistocene stratum and is known as Szekou Formation (described subsequently), wherein marine fossils including foraminifera, ostracods, corals, mollusks, brachiopods, and rarely, some land mammals, have been identified (Hu 1987 1991; Fong 1989; Hu and Tao 1991 2008). The general paleoenvironment of the Szekou Formation has been interpreted as a neritic lagoon (Huang 1988; Chen et al. 1991; Shih et al. 2002). Although the marine invertebrate assemblages are extremely abundant, some calcareous nodules containing crabs and fish are Zoological Studies 61:10 (2022) doi:10.6620/ZS.2022.61-10 1 © 2022 Academia Sinica, Taiwan occasionally found, with crustacean nodules being much more common (Hu and Tao 1996 2000). Herein, a rare, moderately-preserved fish fossil found in a nodule from the Hengchun Peninsula is described. A detailed morphological analysis of the fossil was conducted that bolstered the taxonomic assignment through an extensive comparative analysis with extant species. The taxonomical and paleoecological significance of the specimen is discussed. Geological Setting During the early Pliocene, the eastward subduction of the South China Sea basin under the Philippine Sea plate gradually transformed the Hengchun Peninsula from a stable continental margin structure into an accretionary prism structure (Chen 2016). Since the Pleistocene, the Hengchun Peninsula has been lifted, forming the southernmost part of Taiwan’s Central Mountain Range (Chen et al. 1985; Lundberg et al. 1992; Nakamura et al. 1998; Chi et al. 2003; Chen et al. 2005; Chen 2016). Accretionary prism development is accompanied by numerous wedge-top basins formed between the thrust fault. Therefore, the contact between the formations (i.e., the Shihmen Formation, Maanshan Formation, Kenting Melange, and Hengchun Limestone) on the Hengchun Peninsula is mostly nonconforming from the Pliocene to the Pleistocene (Chen et al. 2005; Fig. 1A, B). The Hengchun Limestone exhibits conformity or contemporaneous heterotopic facies with the Taiping Formation (Chen et al. 2005). The Hengchun Limestone can be further divided into the Syunguangzuei Limestone, Wanlitong Limestone, and Guanshan Limestone on the basis of lithological composition and the sedimentary environment (Chen et al. 2005; Fig. 1C). The Syunguangzuei Limestone is mainly of biogenetic composition (i.e., planktonic foraminifera with admixture of biological debris), and is rich in parallel bedding, low-angle cross-bedding, and hummocky cross-bedding influenced by an offshore sandbar environment. The Wanlitong Limestone is mainly composed of biological detritus and terrestrial materials, with large trough cross-bedding indicating a shoreface environment, whereas in the Guanshan Limestone, corals, Lithothamnium, and various biological debris from the coral reef environment have been deposited (Chen et al. 1985; Chen and Lee 1990; Wu and Chen 1990; Chen 2016). The Late Pleistocene Szekou Formation is mainly exposed in the small valleys on the east side of the Hengchun West Platform (Fig. 1B). The Szekou Formation is composed of terrestrial siliceous clasolite and argillaceous sandstone. The base of the formation is rich in brown, coarse-grained bioclastic rocks. Because of rapid erosion and weathering, numerous fossils and calcareous nodules are exposed, flushed from the valleys, and accumulated onto stream beds. The present fish nodule was collected from one such stream bed. The sedimentary environment of the Szekou Formation has been interpreted as being an intertidal/ low-tide zone with depths primarily within 20 m. In the Szekou Formation, sedimentary structure and bedding are almost absent due to severe biological disturbances (Hu and Tao 1991; Chen et al. 2005; Chen 2016). The Szekou Formation overlays the upper Wanlitong Limestone and exhibits an intertongue structure (Chen et al. 1985; Chen and Lee 1990; Wu and Chen 1990; Chen 2016; Fig. 1C). According to an electron spin resonance analysis of shell fossils, the estimated age of the Szekou Formation is approximately 90–140 kyr (Shih et al. 2002). The youngest Taiping Formation is composed of ferralitic soil and gravel bed, and the sedimentary environment ranges from river beds to coastal sand dunes. This layer is characterized by conformity with part of the Hengchun Limestone, and they are contemporaneous heterotopic facies (Chen et al. 2005; Chen 2016). MATERIALS AND METHODS Fossil specimen According to the appearance of the specimen and numerous other fossil nodules from the Szekou locality (Henchung County) of southern Taiwan (Fig. 1B), the nodule appears to have originated from the Szekou Formation (Fig. 1C). The fish fossil was collected several decades ago by amateur collectors. It is a onehalf sandstone nodule 211.20 mm in length, 116.50 mm in height, and 70.70 mm thick. The exact horizon for the fossil is not known, but during our visit to the locality in January 2021 we were told that the presumed coordinates are 22°00'45"N, 120°43'01"E. The nodule is largely exposed and displays a fish skeleton, and the details of the upper and lower jaws are especially preserved (Fig. 2; Supplementary file S1). Observation of the surface and margins indicated that it was not opened artificially. For systematic description, we followed the classification scheme of Nelson et al. (2016). For the systematic and descriptive procedure, the anatomical terminology used by Day (2002) was employed (see below for a list of anatomical abbreviations). page 2 of 14Zoological Studies 61:10 (2022) © 2022 Academia Sinica, Taiwan Fig. 1. Sampling site (A, B) and stratigraphic correlation (C) on the Hengchun Peninsula. (B) Szekou locality (black circle; modified from Chen 2016). page 3 of 14Zoological Studies 61:10 (2022) © 2022 Academia Sinica, Taiwan Fig. 2. Pagrus major (Temminck and Schlegel, 1843), ASIZF0100141, from the Late Pleistocene Szekou Formation, Hengchun Peninsula, southern Taiwan. A, Lateral view of the nodule. B, Dorsal view of the anterior part of the nodule, note that fragments of the right jaws are exposed. C, Drawing of the recognized skull parts. See text for anatomical abbreviations. Scale bars = 10 mm. page 4 of 14Zoological Studies 61:10 (2022) © 2022 Academia Sinica, Taiwan Recent comparative material A total of 15 species belonging to seven genera of Sparidae have been identified in Taiwan (Parenti 2019; Froese and Pauly 2021; Shao 2021). Our comparative material, both recently collected and from museum collections, included all but one species, Chrysophrys auratus (Forster, 1801), which has a questionable occurrence (see below in the discussion). Fresh specimens were collected from local markets. After identification (Shen and Wu 2011; Nakabo 2013; Koeda and Ho 2019; Chou et al. 2020; Shao 2021), the total length (TL, mm), standard length (SL, mm), and weight (g) of the fish were measured before their upper and lower jaws were dissected, cleared and prepared for subsequent morphological analysis. Preserved specimens of Argyrops (Ar. bleekeri and Ar. spinifer) were examined but not dissected. Specimens from museums and institutes were included to increase the sample size, and a total of 153 specimens belonging to 14 species and six genera were ultimately examined (Appendix 1). Images of the jaws of examined species (not including Argyrops spp.) are presented in figures 3–5. Character statements for dentition and morphological analysis Measurements were taken using a digital caliper (0.01 mm). Because the fossil specimen exhibited well-preserved jaws with immaculate teeth, our morphological analyses were based on associated characters. We followed Akazaki (1962), Day (2002), and Nakabo (2013) to select 11 dentition characters for all specimens (both fossil and recent) to create a data matrix (Table S1): 1. Premaxilla, anterior teeth, shape: sharp (0); caniniform (1); large canine (2); large canine with enlarged base (3); compressed (4). 2. Premaxilla, anterior teeth, pair numbers: two pairs (0); three pairs (1). 3. Dentary, anterior teeth, shape: sharp (0); caniniform (1); large canine (2); large canine with enlarged base (3); compressed (4). 4. Dentary, anterior teeth, pair numbers: two pairs (0); three pairs (1). 5. Premaxilla, villiform teeth, distribution relative to the molariform teeth: anterior (0); discontinuously on anterior and posterior sections (1); continuously distributed on anterior and posterior sections (2). 6. Dentary, villiform teeth, distribution relative to the molariform teeth: anterior (0); discontinuously on anterior and posterior sections (1); continuously distributed on anterior and posterior sections (2). 7. Jaws (premaxilla and dentary), labial side first series, shape: conical (0); molariform (1). 8. Molariform teeth, surface shape: flat (0); hemispheric (1); slightly pointed (2). 9. Molariform teeth: present (0); absent (1). 10. Premaxilla, lateral teeth series, number: one (0); two (1); three (2); four (3). 11. Dentary, lateral teeth series, number: one (0); two (1); three (2). All the characters are transformational, except character 9, which is neomorphic. Neomorphic characters (absence/presence) were analyzed separately from transformational ones (characters with variable and variable qualifier) (Sereno 2007). A multivariate correspondence analysis (CA) was performed on the dataset (Table S1) using Past4 software (Hammer et al. 2001) with Chi-squared distance to visualize the specimen groupings. Repositories and institutional abbreviations The fossil specimen examined in this study is deposited in the Biodiversity Research Museum, Academia Sinica, Taiwan (BRMAS) under the registration code ASIZF0100141. Details of other reference specimens can be found in appendix 1. SYSTEMATIC PALEONTOLOGY Order Spariformes Bleeker, 1876 Family Sparidae Rafinesque, 1818 Genus Pagrus Cuvier, 1816 Type species: Pagrus pagrus (Linnaeus, 1758) by absolute tautonymy. Mediterranean and Atlantic. Pagrus major (Temminck and Schlegel, 1843) (Fig. 2; Fig. S1A) Description: The nodule itself is large and robust; it contains an almost complete lower part (splanchnocranium) of a left skull, fragmentary right premaxilla (Pmx) and dentary (Den), and the anterior part of the body. Fragments of the coracoid and cleithrum are visible just behind the opercle (Op). The body part is largely covered by fragmented scales. The description is based on the skull part. The length of the skull is up to 94.60 mm, and the height is 73.50 mm. All associated bones are viewed from the inner (mesial, proximal) side. A fragmented right premaxilla and dentary are best visible page 5 of 14Zoological Studies 61:10 (2022) © 2022 Academia Sinica, Taiwan Fig. 3. Left jaws of recent Acanthopagrus spp. (Sparidae). A, Acanthopagrus pacificus Iwatsuki, Kume and Yoshino, 2010, CHLP 2000021; B, Acanthopagrus schlegelii (Bleeker, 1854), CHLP 2000072; C, Acanthopagrus chinshira Kume and Yoshino, 2008, CHLP 2000035; D, Acanthopagrus latus (Houttuyn, 1782), CHLP 2000099. 1–3, premaxilla; 4–6, dentary; 1, 4, labial views; 2, 5, dentitions; 3, 6, lingual views. Scale bar = 10 mm. page 6 of 14 Zoological Studies 61:10 (2022) © 2022 Academia Sinica, Taiwan Fig. 4. Left jaws of recent Acanthopagrus spp., Pagrus major, and Evynnis spp. (Sparidae). A, Acanthopagrus taiwanensis Iwatsuki and Carpenter, 2006, CHLP 2000026; B, Acanthopagrus sivicolus Akazaki, 1962, CHLP 2000029; C, D, Pagrus major (Temminck and Schlegel, 1843), CHLP 2000016 & CHLP 2000015; E, Rhabdosargus sarba (Forsskål, 1775), CHLP 2000022. 1–3, premaxilla; 4–6, dentary; 1, 4, labial views; 2, 5, dentitions; 3, 6, lingual views. Scale bar = 10 mm. page 7 of 14Zoological Studies 61:10 (2022) © 2022 Academia Sinica, Taiwan Fig. 5. Left jaws of recent Dentex spp. and Evynnis spp. (Sparidae). A, Dextex hypselosomus Bleeker, 1854, CHLP 2000018; B, Evynnis cardinalis (Lacepède, 1802), CHLP 2000031; C, Evynnis tumifrons (Temminck and Schlegel, 1843), CHLP 2000025; D, Dentex abei Iwatsuki, Akazaki and Taniguchi, 2007, CHLP 2000033. 1–3, premaxilla; 4–6, dentary; 1, 4, labial views; 2, 5, dentitions; 3, 6, lingual views. Scale bar = 10 mm. page 8 of 14Zoological Studies 61:10 (2022) © 2022 Academia Sinica, Taiwan from the dorsal view (Fig. 2B). The neurocranium is nearly missing, and gill skeletons are not preserved. Infraorbital bones and otoliths are absent. The mouth is obtuse but not protruding anteriorly. The oral jaws are up to 29.40 mm in length. The ascending process of the left premaxilla (as.p.pm) is covered (obviously fused) by the right one, which is broken, and at least two pulp cavities of the caniniform teeth are exposed. Two caniniform teeth (2.04 and 6.08 mm, respectively) are attached to the nearby matrix. The tooth field of the alveolar process is elongate, accommodating two series of anterior conical (2–3 teeth, tilted) and posterior molariform (6 teeth, 1.57– 2.14 mm) teeth (Fig. S1A). The proximal series of the teeth is in situ, whereas in the labial (distal) one, teeth are dislodged and tilted in the surrounding matrix. The conical teeth are very slightly smaller than the molariform ones, and the latter are not progressively larger or become stout posteriorly. At least two indistinct rows of tiny villiform teeth (0.55–0.60 mm each) are present along the proximal edge of the premaxilla; they appear to be more densely spaced anteriorly and can be extended sparsely to the rear molariform teeth (Fig. S1A). In the maxilla (Mx), the maxillary dorsal crest (mdc) is broad and well-developed. The maxilla anteriorly articulates with the articular process of the premaxilla (ar.p.pm), and its ventral rim adjoins the dorsal roof of the premaxillary alveolar process (al. p.pm). In the lower jaws, the left dentary, articular (Art) and angular (An), and part of the right dentary are recognized. The right dentary is better observed from the dorsal view; two caniniform teeth (2.43 and 4.72 mm, respectively) in the anterior tip and two pulp cavities of the conical teeth are preserved (Fig. 2B). In the left dentary, the coronoid process (cp) is welldeveloped and broadly extending upwards. Caniniform teeth are not seen from the surface. Two series of conical (6 teeth, 1.72–1.80 mm) and molariform (7 teeth, 1.67–2.30 mm) teeth are exquisitely preserved in the tooth field (Table S1). The pattern of these teeth on the dentary is very similar to that of the upper jaw. Similarly, as in the premaxilla, numerous villiform teeth are present on the proximal rim of the dentary, though many of them are shed, leaving only the pulp cavities. The articular articulates with the dentary and quadrate (Q), and its descending process (d.p.art) seems to be extending below the dentary ventral margin (character no. 39 in Day 2002), but it is not clear if it extends further beyond the symphyseal process because the latter is not observable. The jaw joint between the articular and quadrate is in the level of anterior margin of the orbit. The angular is rudimentary but still evident in the quadrate-articular facet. In the suspensorium bones, the palatine arch, the endopterygoid (Enp), metapterygoid (Mpt), and quadrate, and possibly the palatine (Pl), are evident, but these are only fragmentary and less preserved. The hyomandibular is not preserved. Bones of the opercular region are visible but not well-preserved and indistinct; of these, the preopercle (Pop) is best distinguished and apparently has a very long ascending process with a smooth posterior margin. Other hyoid-associated skeletons are less preserved and not recognized here. A single branchiostegal ray (Brr) is preserved. RESULTS Comparison of sparid teeth and jaws In the family Sparidae, the premaxilla overlaps the maxilla externally in the distal end of the premaxillary alveolar process (Regan 1913; Smith 1938; Day 2002). However, this condition could not be observed in ASIZF0100141 because only the mesial side is exposed in the jaws. On the other hand, the maxilla largely articulating with the articular process of the premaxilla (Day 2002), along with its distinct dentition (Smith 1938; Akazaki 1962), suggest that our fossil belongs to the family Sparidae. Because numerous genera and species present similar dentition, we further compared their morphological characters. A single neomorphic character, the absence or presence of the molariform teeth, allowed a clear separation of Dentex species (absence of molariform) from all other remaining genera and the fossil. This separation suggests that the fossil does not belong to the genus Dentex. The 10 transformational tooth-related morphological characters facilitate further differentiation of the remaining genera (Fig. 6). The species of Acanthopagrus are grouped with Rhabdosargus sarba, whereas the fossil ASIZF0100141 is tightly grouped with P. major (Fig. 6). Pagrus major is more related to Evynnis species; these taxa are characterized by the presence of villiform teeth along the proximal rim of the jaws. On the other hand, P. major has larger anterior caniniform teeth than those of Evynnis spp. (Figs. 4, 5). Aside from dentition, the alveolar process of the premaxilla (al.p.pm) is much longer than its ascending process (as.p.pm) in Dextex spp. (Fig. 5), whereas these processes are similar in length in P. major and Evynnis spp. (Uyeno 1979; Figs. 4, 5). With a more prominent dorsal crest, the maxilla is most robust in species of Dextex than the other two taxa. In the anterior part of maxilla, the articular condyle of maxilla is separated from the dorsal crest in Evynnisi spp., but in Dentex spp., this condyle is tightly attaching with the dorsal page 9 of 14Zoological Studies 61:10 (2022)