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From the Bolca Lagerstätte (Italy) Has Provided New Insights Into the Fsh Biodiversity of the Western Tethys

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From the Bolca Lagerstätte (Italy) Has Provided New Insights Into the Fsh Biodiversity of the Western Tethys www.nature.com/scientificreports OPEN A bizarre Eocene dasyatoid batomorph (Elasmobranchii, Myliobatiformes) from the Bolca Received: 10 April 2019 Accepted: 13 September 2019 Lagerstätte (Italy) reveals a new, Published: xx xx xxxx extinct body plan for stingrays Giuseppe Marramà 1, Giorgio Carnevale2, Luca Giusberti3, Gavin J. P. Naylor4 & Jürgen Kriwet1 In the last few years, the detailed revision of the Eocene cartilaginous fshes (Chondrichthyes) from the Bolca Lagerstätte (Italy) has provided new insights into the fsh biodiversity of the western Tethys. The morphological analysis of three previously undescribed specimens from the Pesciara deposit of Bolca revealed the existence of a new stingray taxon, †Lessiniabatis aenigmatica gen. et sp. nov., which is unique among the myliobatiform batoids in having the following unique combination of characters: low number of vertebrae posterior to the pelvic girdle (65–68); thoracolumbar synarcual extending backward beyond the pelvic girdle; tail extremely short not protruding from the posterior edge of the pectoral disc; radials proximally fused to each other; pelvic girdle extremely small and strongly arched; dorsal and caudal fns absent; tail stings and cartilaginous tail rod absent; and teeth of dasyatoid morphology with smooth enameloid surface. The phylogenetic analysis suggests that †Lessiniabatis gen. nov. is deeply nested within the benthic stingrays (Dasyatoidea) representing the sister to all dasyatids and potamotrygonids. Its unique anatomy clearly reveals the existence of a new hitherto unknown body plan experimented by benthic stingrays, whose evolution can be possibly linked to the adaptive fsh radiation in the aftermath of the end-Cretaceous extinction. Stingrays (order Myliobatiformes) are a speciose group of batoid fshes comprising more than 360 extant species arranged in 11 families1,2. Although their interrelationships are still ambiguous with contrasting results emerg- ing from molecular and morphological studies1,3–6, stingrays can be unambiguously regarded as a monophyletic clade of batoids characterized by a series of derived features, including the presence of one or more serrated tail stings, a second (thoracolumbar) synarcual, absence of rostral cartilage, and other unique features of the gill arches and pectoral girdle3,4,7–10. Although the fossil record of stingrays is abundant and can be traced back to the Lower Cretaceous11, it is strongly biased toward isolated teeth with the exception of a few Cenozoic records rep- resented by complete articulated skeletons3,6,12–15. Myliobatiforms may have experienced a frst radiation on the latest Cretaceous with the appearance and diversifcation of pelagic/benthopelagic durophagous taxa, followed by a second wave of radiation during the early Paleogene with the appearance and radiation of the planktivo- rous stingrays5,16,17. Teir early Paleogene radiation co-occurred with many other remarkable diversifcations of bony and cartilaginous fsh lineages driven by the availability of new ecological niches associated with the establishment of modern coral reefs and the removal by extinction of many Cretaceous clades18–24. Te celebrated Eocene (Ypresian, ca. 49 Ma25,26) Konservat‐Lagerstätte of Pesciara of Bolca in northeastern Italy is known for the outstanding diversity and preservational quality of bony and cartilaginous fshes, which provide evidence of the recovery of shallow marine settings associated with reefs afer the K/Pg boundary27. Te Bolca fsh assemblage 1University of Vienna, Department of Palaeontology, Vienna, 1090, Austria. 2Università degli Studi di Torino, Dipartimento di Scienze della Terra, Torino, 10125, Italy. 3Università degli Studi di Padova, Dipartimento di Geoscienze, Padova, 35131, Italy. 4University of Florida, Florida Museum of Natural History, Gainesville, 32611, Florida, USA. Correspondence and requests for materials should be addressed to G.M. (email: giuseppe.marrama@ univie.ac.at) SCIENTIFIC REPORTS | (2019) 9:14087 | https://doi.org/10.1038/s41598-019-50544-y 1 www.nature.com/scientificreports/ www.nature.com/scientificreports also documents the emergence of peculiar body plans and evolutionary innovations, which are indicative of a considerable experimentation of new ecological strategies. Examples include stem fatfshes (Pleuronectiformes) showing gradual evolution of asymmetry28,29, curious ribbon-like morphology of †Bajaichthys, very diferent from the deep bodies of modern zeiforms30, basal members of the hyperdiverse benthic gobioids31, a variety of bizarre anglerfshes32–35 and plectognaths36, or the peculiar paralepidid aulopiform †Holosteus whose body plan mimics that of pike-like ambush predators23. In this study, another one in a series of papers highlighting the pal- aeobiodiversity of the Eocene batoids from the Bolca Lagerstätte6,13,15,24, we describe in detail the anatomy and the phylogenetic relationships of a new stingray genus whose unique body plan, unknown in other extinct or living myliobatiform taxa, supports the idea that evolutionary novelties and innovations also occurred in cartilaginous fshes in the afermath of the end-Cretaceous extinction, leading to the exploitation of new ecological strategies. Results Systematic palaeontology. Class Chondrichthyes Huxley, 1880. Superorder Batomorphii Cappetta, 1980. Order Myliobatiformes Compagno, 1973. Superfamily Dasyatoidea Compagno, 1973. Family incertae sedis. Genus †Lessiniabatis gen. nov. urn:lsid:zoobank.org:pub:72B8B7EE-0D87-4864-B31A-5695AAEE89C0. Type species. †Lessiniabatis aenigmatica sp. nov. Etymology. Afer Lessinia, the Italian geographic area where the Bolca Lagerstätte is located, and from the Ancient Greek word ‘βατίς’ (batis), meaning ray or skate; gender feminine. Diagnosis. A dasyatoid stingray unique in having a thoracolumbar synarcual extending backward beyond the pelvic girdle, a tail that is extremely short and not protruding from the posterior edge of the pectoral disc, and pectoral radials that are proximally fused with one another. Moreover, †Lessiniabatis gen. nov. is characterized by the following combination of traits: low number of vertebrae posterior to the pelvic girdle (65–68); dorsal and caudal fns absent; pelvic girdle extremely small and strongly arched; tail stings and cartilaginous tail rod absent; teeth with dasyatoid morphology; enameloid surface smooth; lingual tooth surface broad and slightly convex; labial tooth surface slightly concave; labial and lingual tooth faces not steep in lateral profle; tooth root bilobed, with a central foramen; holaulacorhizid root type with an elongated pulp cavity; sparse, star-shaped dermal den- ticles covering the whole body; about 130–135 pectoral-fn radials (of which 59–61 are propterygial, 16–18 are mesopterygial, and 54–57 are metapterygial); about 120 vertebral centra. Composition of the genus. Te genus is represented only by the type species †Lessianabatis aenigmatica sp. nov. †Lessiniabatis aenigmatica sp. nov. (Figures 1–7) Urolophus crassicaudatus (Blainville, 1818): Raux (2014), Figs 1, 7–9, 1137. “Urolophus” crassicaudatus (Blainville, 1818): Marramà et al. (2018), Fig. 9A,B, non C-D15. Etymology. Afer the Latin word ‘aenigmaticus’, -a, meaning enigmatic, puzzling, referring to its peculiar anat- omy; gender feminine. Holotype. MNHN F.Bol.566 (ex 11001 and 10997), nearly complete articulated skeleton, in part (566B) and counterpart (566 A); 466.8 mm DW (Fig. 1). Paratypes. MSNFI IGF 103555, nearly complete articulated skeleton in part and counterpart, 568.2 mm DW (Fig. 2a,b); MFSN GP.864, partially articulated skeleton on a single slab, with most of the neurocranium and pectoral girdle being disarticulated; 375.1 mm DW (Fig. 2c). Type locality and horizon. Pesciara site, Bolca Konservat-Lagerstätte, Italy; lower Eocene, upper Ypresian, SB 11 and NP 14a Zones25. Diagnosis. Same as genus (monotypic genus). Remarks. Te holotype we designate herein for †Lessiniabatis aenigmatica gen. et sp. nov., MNHN F.Bol.566 (previously labelled as 10997–11001), is the specimen indicated as the holotype of †Urolophus crassicaudatus (Blainville, 1818)38 in the collections of the Museum National d’Histoire Naturelle of Paris (https://science.mnhn. fr/taxon/species/urolophus/crassicaudatus). However, as already suggested by Eastman (1904, p. 25; 1905, p. 9)39,40, this specimen cannot be identified as the type of †Urolophus crassicaudatus. In fact, the original anatomi- cal description and measurements of the specimen given by Blainville (1818, p. 337)38 (originally described as †Trygonobatus crassicaudatus) clearly do not ft with those of MNHN F.Bol.566. Te author shortly described, without any illustration, a fossil ray having a thick and robust tail (whence crassicaudatus) with trace of a tail sting, with a body 15 inches long (about 38 cm) and 16 broad (about 41 cm)38. Conversely, MNHN F.Bol.566 shows a very short and slender tail (without any trace of tail sting) and the body is longer (about 55 cm) than SCIENTIFIC REPORTS | (2019) 9:14087 | https://doi.org/10.1038/s41598-019-50544-y 2 www.nature.com/scientificreports/ www.nature.com/scientificreports Figure 1. †Lessiniabatis aenigmatica gen. et sp. nov. from the Eocene of Bolca Lagerstätte. (a,b) the holotype MNHN F.Bol.566 in part and counterpart. Scale bars equal 100 mm. Figure 2. †Lessiniabatis aenigmatica gen. et sp. nov. from the Eocene of Bolca Lagerstätte. (a,b) the paratype MSNFI IGF 103555 in part and counterpart; (c) the paratype MFSN GP.864. Scale bars equal 100 mm. broad (about 47
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