Revision of Eocene electric rays (Torpediniformes, Batomorphii) from the Bolca Konservat-Lagerstätte, Italy, reveals the first fossil embryo in situ in marine batoids and provides new insights into the origin of trophic novelties in coral reef fishes

Abstract

The Eocene electric ray †Titanonarke Carvalho, 2010 from the Bolca Konservat-Lagerstätte, north-eastern Italy, is redescribed in detail based upon new material from recent excavations. This taxon exhibits a combination of features (large voids between the pectoral and the axial skeleton filled in life by electric organs, anteriorly directed fan-shaped antorbital cartilages, lack of dermal denticles, long prepelvic processes, and rounded basibranchial copula with a small caudal tab) that clearly supports its assignment to the order Torpediniformes. The analysis of new material also demonstrates that the previous apparent absence of typical narcinoid characters used to diagnose †Titanonarke was the result of taphonomic biases. †Titanonarke shares at least three synapomorphies (presence of a rostral fontanelle, low number of ribs, and rostral cartilage connected to the antorbital cartilage through lateral appendices) with the extant genera Benthobatis, Diplobatis, Discopyge and Narcine, with which it forms a clade (family Narcinidae) recognized herein as unquestionably monophyletic. Moreover, based upon a single specimen of †Titanonarke that exhibits a unique combination of morphometric and meristic features, a new species of Eocene numbfish †T. megapterygia sp. nov., is recognized. The presence of several specimens representing different ontogenetic stages of at least two species of numbfishes suggests a close association of this taxon with shallow-water habitats corresponding to coral reefs as hypothesized for the Monte Postale palaeoenvironment. The occurrence of a fossilized marine batoid embryo is reported here for the first time. Moreover, the analysis of the gut contents suggests that the dietary adaptations of †Titanonarke can be related, at least in part, to an opportunistic strategy in the context of abundant larger foraminifera in the Monte Postale palaeobiotope, suggesting that this kind of feeding mode, known to occur in present-day reefs, already was realized 50 million years ago.

Keywords: Chondrichthyes; Elasmobranchii; embryo; gut content; morphology; phylogeny.

Figure 1

A, location and geological map of the Bolca area. B, stratigraphical section of the uppermost part of the Monte Postale sequence. Modified from Marramà et al. (2016c).

Figure 2

†Titanonarke molini (Jaekel, 1894) from the Eocene Monte Postale site. A, B, MGP-PD 26275/6, holotype in part and counterpart. Scale bars = 100 mm.

Figure 3

†Titanonarke molini (Jaekel, 1894) from the Eocene Monte Postale site. A, MCSNV IG.VR.67290; B, MCSNV IG.91128/9. Scale bars = 100 mm.

Figure 4

Juvenile individuals of †Titanonarke molini (Jaekel, 1894) from the Eocene Monte Postale site. A, MCSNV IG.VR.91359; B, MCSNV IG.135581. Scale bars = 10 mm.

Figure 5

†Titanonarke molini (Jaekel, 1894) from the Eocene Monte Postale site. A, MCSNV IG.VR.67290, close-up of the head and hyoid apparatus; B, reconstruction. Abbreviations: ao, antorbital cartilage; bb, basibranchials; bbc, basibranchial copula; cb, ceratobranchials; cc, chondrocranium; eb, epibranchials; hb, hypobranchials; hym, hyomandibula; la, labial cartilages; me, Meckel’s cartilage; nc, nasal capsule; pq, palatoquadrate; ps, pseudohyoid; ra, rostral appendix; rf, rostral fontanelle; ro, rostral cartilage; sca, scapulocoracoid; ss, suprascapula; syn, synarcual. Scale bars = 50 mm.

Figure 6

†Titanonarke molini (Jaekel, 1894) from the Eocene Monte Postale site. A, the juvenile individual MCSNV IG.VR.91359; B, reconstruction. Abbreviations: ao, antorbital cartilage; cb, ceratobranchials; hym, hyomandibula; la, labial cartilages; me, Meckel’s cartilage; mes, mesopterygium; met, metapterygium; nc, nasal capsule; pel, prepelvic process; pub, puboischiadic bar; pq, palatoquadrate; pro, propterygium; ps, pseudohyoid; rad, pectoral radials; ro, rostral cartilage; sca, scapulocoracoid; ss, suprascapula; syn, synarcual. Scale bars = 50 mm.

Figure 7

†Titanonarke molini (Jaekel, 1894) from the Eocene Monte Postale site. A, B, UV images of the holotype MGP-PD 26275/6 showing that it was covered with a pigment reflecting an orange light (see also Supplementary material). The arrows in A indicate a leaf also covered with the pigment, a drop, and some rays that were not distally covered (they are blue/grey, as expected); the arrowhead in A indicates part of the third branch of the antorbital cartilage not covered by pigment; the arrowhead in B indicates the rostral appendix; C, Narcine brasiliensis (TNHC 18512); the arrows indicate the rostral appendices. Scale bars: A, B = 50 mm; C = 10 mm.

Figure 8

Visual image of the principal component analysis (PCA) performed on the entire set of log-transformed standardized morphometric and meristic features, showing the separation of the specimens referred to †Titanonarke molini (right side of morphospace) from those referred to †Titanonarke megapterygia sp. nov. (left side). The illustrations lying along the extreme values of PC1 represent the hypothetical reconstruction of the two species based on body proportions.

Figure 9

A, synarcual and pectoral girdle of Narcine brasiliensis (AMNH 95343) in dorsal view; B, synarcual and pectoral girdle of †Titanonarke molini (MCSNV IG.VR.91359) in ventral view. The arrowheads indicate the posteriorly directed lateral stays of the synarcual. The arrows indicate the posteriorly directed scapular process of the scapulocoracoid. Abbreviations: cb, ceratocranchials; sca, scapulocoracoid; ss, suprascapula; syn, synarcual. Scale bar = 5 mm.

Figure 10

Pectoral fin of †Titanonarke molini (Jaekel, 1894) from the Eocene Monte Postale site. A, MCSNV IG.VR.67290; B, reconstruction; different colours are used to distinguish the propterygial (green), mesopterygial (yellow) and metapterygial (red) radials (colours in the online version). Abbreviations: mes, mesopterygium; met, metapterygium; pro, propterygium; sca, scapulocoracoid. Scale bars = 50 mm.

Figure 11

Pelvic fins of †Titanonarke molini (Jaekel, 1894) from the Eocene Monte Postale site. A, MCSNV IG.VR.67290; B, reconstruction. Abbreviations: bas, basipterygia; ilp, iliac process; pel, pelvic processes; pub, puboischiadic bar; rad, pelvic radials. The arrowhead indicates the iliac process. Scale bars = 50 mm.

Figure 12

†Titanonarke molini (Jaekel, 1894) from the Eocene Monte Postale site. Close-up of the distal end of pelvic fins of MCSNV IG.91128, which is supposed to be the unique male individual based on the presence of claspers. Abbreviations: cla, clasper; dfr, first dorsal-fin radials, pelvic radials. Scale bar = 50 mm.

Figure 13

†Titanonarke molini (Jaekel, 1894) from the Eocene Monte Postale site. Details of the precaudal tail of A, MCSNV IG. VR.67290 and B, MGP-PD 26276. The arrows mark the position of the two dorsal fins in MCSNV IG.VR.67290 and the second dorsal fin in MGP-PD 26276 already detected and figured by Jaekel (1894). C, Detail of the caudal fin of MCSNV IG.91129. Scale bars: A, B = 50 mm; C = 10 mm.

Figure 14

†Titanonarke molini (Jaekel, 1894) from the Eocene of Monte Postale site. A, upper and lower tooth bands in MCSNV IG.VR.67290, with a close-up of some teeth in the area indicated. B, reconstruction. Abbreviations: la, labial cartilage; me, Meckel’s cartilage; pq, palatoquadrate. Scale bars 5 mm.

Figure 15

A, B, †Titanonarke molini (Jaekel, 1894) from the Eocene Monte Postale site; A, detail of the abdominal region in MGP-PD 26275 showing the stomach content; B, reconstruction; note also the embryo lying next to the stomach. C, D, close-up of some of the larger foraminifera of the genus †Alveolina in the stomach of MGP-PD 26275. E, dissected specimen of Torpedo nobiliana in ventral view (ESB tn200707_159) showing the position of the stomach, used to identify the accumulation in MGP-PD 26275 as gut contents. Abbreviations: int, intestine; liv, liver; met, metapterygium; pub, puboischiadic bar; sca, scapulocoracoid; st, stomach, syn synarcual. Scale bars: A, B = 50 mm; C, D = 2 mm.

Figure 16

A, B, D, †Titanonarke molini (Jaekel, 1894) from the Eocene Monte Postale site; A, close-up of the abdominal region of MGP-PD 26275 showing the embryo; the anterior region of the body lies on the lower portion of the photo; B, reconstruction; D, detail of the vertebral column of the embryo indicated in B with a dotted rectangle. C, dissected specimen of Potamotrygon tigrina (IUWP 7361) showing the position of the left uterus, just next to the stomach. Abbreviations: int, intestine; liv, liver; lu, left uterus; na, neural arches; ru, right uterus; st, stomach; vc, vertebral centra. Scale bars: A, B = 10 mm; D = 1 mm.

Figure 17

†Titanonarke megapterygia sp. nov. from the Eocene Monte Postale site. A, MCSNV IG.135576; B, detail of the head and hyoid apparatus. Abbreviations: ao, antorbital cartilage; cb, ceratobranchials; hym, hyomandibula; me, Meckel’s cartilage; nc, nasal capsule; pq, palatoquadrate; sca, scapulocoracoid; syn, synarcual; rf, rostral fontanelle; ro, rostral cartilage. Scale bars = 50 mm.

Figure 18

The single tree retrieved in TNT 1.5 based on 72 morphological characters and 16 taxa, showing the hypothetic relationships of †Titanonarke and †Eotorpedo within the Torpediniformes. Black squares indicate consistency index (CI) = 1.00; white squares CI < 1.00.

Figure 19

Palaeobiogeographical distribution of the Torpediniformes during the Cenozoic: 1, Texas; 2, Belgium; 3, Morocco; 4, Jordan; 5, Saudi Arabia; 6, Enclave of Cabinda; 7, Nigeria; 8, Niger; 9, Cameroun; 10, Senegal; 11, Tunisia; 12, South Carolina; 13, France; 14, Guinea-Bissau; 15, Togo; 16, Egypt; 17, Italy; 18, Portugal; 19, Switzerland; 20, Germany; 21, Netherlands. Data from Hasse (1879), Jaekel (1904), White (1934), Dartvelle & Casier (1943), Arambourg (1952), Cappetta et al. (1967, 2000), Cappetta (1972, 1987, 1988, 2012), Herman (1974), Banks (1978), Cappetta & Traverse (1988), Cappetta & Nolf (1991), Bolliger et al. (1995), Madden et al. (1995), Noubhani & Cappetta (1997), Antunes et al. (1999), Smith (1999), Bracher (2005), Reinecke et al. (2005), Adnet (2006), Knight et al. (2007), Adnet et al. (2010), Carvalho (2010), Mollen (2010), Underwood et al. (2011), Case et al. (2015), Reinecke (2015) and Siguendibo Sambou et al. (2017). Maps are modified from Scotese (2002).