New ophthalmosaurid ichthyosaurs from the European lower cretaceous demonstrate extensive ichthyosaur survival across the Jurassic–Cretaceous boundary

Background Ichthyosauria is a diverse clade of marine amniotes that spanned most of the Mesozoic. Until recently, most authors interpreted the fossil record as showing that three major extinction events affected this group during its history: one during the latest Triassic, one at the Jurassic–Cretaceous boundary (JCB), and one (resulting in total extinction) at the Cenomanian-Turonian boundary. The JCB was believed to eradicate most of the peculiar morphotypes found in the Late Jurassic, in favor of apparently less specialized forms in the Cretaceous. However, the record of ichthyosaurs from the Berriasian–Barremian interval is extremely limited, and the effects of the end-Jurassic extinction event on ichthyosaurs remains poorly understood. Methodology/Principal Findings Based on new material from the Hauterivian of England and Germany and on abundant material from the Cambridge Greensand Formation, we name a new ophthalmosaurid, Acamptonectes densus gen. et sp. nov. This taxon shares numerous features with Ophthalmosaurus, a genus now restricted to the Callovian–Berriasian interval. Our phylogenetic analysis indicates that Ophthalmosauridae diverged early in its history into two markedly distinct clades, Ophthalmosaurinae and Platypterygiinae, both of which cross the JCB and persist to the late Albian at least. To evaluate the effect of the JCB extinction event on ichthyosaurs, we calculated cladogenesis, extinction, and survival rates for each stage of the Oxfordian–Barremian interval, under different scenarios. The extinction rate during the JCB never surpasses the background extinction rate for the Oxfordian–Barremian interval and the JCB records one of the highest survival rates of the interval. Conclusions/Significance There is currently no evidence that ichthyosaurs were affected by the JCB extinction event, in contrast to many other marine groups. Ophthalmosaurid ichthyosaurs remained diverse from their rapid radiation in the Middle Jurassic to their total extinction at the beginning of the Late Cretaceous

Pas d’extinction à la limite Jurassique–Crétacé pour les ichthyosaures

Les ichthyosaures sont un groupe diversifié de reptiles marins mésozoïques. Pour de nombreux auteurs, trois extinctions majeures ont perturbé leur longue histoire évolutive : une à la fin du Trias, une à la limite Jurassique–Crétacé (JCB) et une (résultant en l’extinction totale) à la limite Cénomanien–Turonien. On croyait que l’extinction de la JCB avait éradiqué la plupart des morphotypes particuliers trouvés dans le Jurassique supérieur, à la faveur de quelques formes crétacées considérées moins spécialisées. Ici, nous réévaluons cette hypothèse en utilisant des analyses phylogénétiques et des taux de cladogenèse/survie/extinction. Notre analyse phylogénétique indique que les ophthalmosauridés (clade unissant tous les ichtyosaures post-bajociens) ont divergé très tôt dans leur histoire en deux clades distincts ; tous deux traversent la JCB et persistent au moins jusqu’ à l'Albien terminal. Pour évaluer l'effet de l'extinction de la JCB sur les ichthyosaures, nous avons calculé des taux de cladogenèse, d'extinction, et de survie pour chaque étage de l'intervalle Oxfordien-Barrémien, selon différents scénarii. Le taux d'extinction de la JCB ne surpasse pas le taux « background » pour l'intervalle Oxfordien-Barrémien et la JCB enregistre un des taux de survie le plus élevé de l'intervalle. Par conséquent, il n'existe actuellement aucune preuve que les ichthyosaures aient été touchés par une extinction à la JCB, contrairement à de nombreux autres groupes d’animaux marins. Les ophthalmosauridés restent diversifiés de leur rayonnement rapide au Jurassique moyen jusqu’à leur extinction totale au début du Crétacé supérieur

Regionalization of the vertebral column in <i>Acamptonectes densus</i>.

<p>Both specimens have incomplete vertebral series and the centra were therefore superposed manually in each region, using the centrum shape and relative position of the apophyses. Each obvious gap in the vertebral column is represented by a single void in the series of SNHM1284-R. The x-axis refers to the centrum count, not its actual position within the vertebral column. The regionalization of the vertebral column is quite weak, in between that of <i>Sveltonectes insolitus </i><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0029234#pone.0029234-Fischer2" target="_blank">[34]</a> and <i>Ophthalmosaurus icenicus </i><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0029234#pone.0029234-Massare1" target="_blank">[69]</a>.</p

Diagnostic features of the axial skeleton of <i>Acamptonectes densus</i>.

<p>A: anterior dorsal centrum and associated neural spine of SNHM1284-R, showing the large size of the neural spine with respect to the centrum height. B: series of posterior postflexural centra of SNHM1284-R showing their square shape (H/L≈1). C: series of posterior dorsal centra of GLAHM 132588 (holotype), showing the markedly curved profile of the posterolateral lamella. D: cross-section of a rib of NHMUK R11185 showing their robust morphology and the minute groove occurring on one side only.</p

Basicranium, quadrate, and dentition of <i>Acamptonectes densus</i> (GLAHM 132588, holotype).

<p>A–C: basisphenoid, in dorsal view (A), in lateral view (B), and in posterior view (C). The thick and claw-like shape of the basipterygoid process in lateral view in shown in B. Note the dorsal crest and the paired facialis (VII) nerve foramen. D,E: left exoccipital, in medial view (D) and ventral view (E). The arrow indicates a notch that matches a small bump on the dorsal surface of the basioccipital, suggesting a close fit of these bones (and therefore a thin cartilage layer) that we interpret as indicator of a mature age. F,G: left stapes, in anteromedial view (F) and posterolateral view (G). Note the slenderness of the shaft compared to the occipital head. H,I: left quadrate, in lateral view (H) and posterior view (I). J,K: fragmentary tooth crowns magnified four times with respect to the other bones. Note the subtle striations and the constriction at the base of the crown in K. Abbreviations: bbf: facet for basioccipital and basisphenoid; bpp: basipterygoid process; hgf: hypoglossal foramina; sof: supraoccipital facet; VII: foramen for the facialis nerve (VII).</p

Variable morphological features in <i>Acamptonectes densus</i>.

<p>The features listed here are those not previously assigned to ontogeny: typical ontogenetic features (such as sandpaper-like texture on the humerus, the shape of the capitulum of the humerus, and the overall ‘fit’ of the basicranium and forefin bones) are discussed in the text. Potentially, the variations listed here could be interpreted as representing ontogenetic, phyletic, or intraspecific variation, given the differences in ontogenetic stage (subadult VS adult) and stratigraphic age (late Hauterivian VS basal Hauterivian) of the two specimens. Because we interpret both individuals as representatives of the same species, we propose that the morphological features listed here are within normal intraspecific variation and hence possibly of limited phylogenetic interest.</p

Survival, extinction, and cladogenesis rates of ophthalmosaurids for each boundary of the Oxfordian–Barremian interval.

<p>A: survival (positive) and extinction (negative) rates in the conservative scenario, in which post-Jurassic occurrences of both <i>Ophthalmosaurus</i> and <i>Brachypterygius</i> are ignored. B: survival (positive) and extinction (negative) rates in the total evidence scenario. C: cladogenesis rate. Light color represents phylogenetic lineages and dark color represents genera. Rates for the JCB are colored in orange. The JCB records high survival rates and low to null extinction rates, suggesting that no extinction took place amongst ichthyosaurs at the end of the Jurassic. Abbreviations: Apt: Aptian; Bar: Barremian; Ber, Berriasian; Hau: Hauterivian; Kim: Kimmeridgian; Oxf: Oxfordian; Tit: Tithonian.</p

Left prootic of <i>Acamptonectes densus</i> compared to that of other ophthalmosaurids.

<p>A–C: <i>A. densus</i> (GLAHM 132588, holotype), in posterior view (A,B) and anterior view (C). D,E: <i>A. densus</i> (SNHM1284-R), in posterior view. F: <i>Platypterygius australis</i> (QMF14339), in posterior view redrawn from Kear <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0029234#pone.0029234-Kear1" target="_blank">[58]</a>. G: <i>Sveltonectes insolitus</i> (IRSNB R269, holotype), in posterior view, from Fischer et al. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0029234#pone.0029234-Fischer2" target="_blank">[34]</a>. H: <i>Ophthalmosaurus icenicus</i> (NHMUK R4522, mirrored), in posterior view, redrawn from Kirton <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0029234#pone.0029234-Kirton1" target="_blank">[43]</a>. I: <i>Ophthalmosaurus icenicus</i> (NHMUK R2161), in posterior view, redrawn from Andrews <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0029234#pone.0029234-Andrews2" target="_blank">[51]</a>. Abbreviations: amp: ampulla; avsc: impression of the anterior vertical semicircular canal; hsc: impression of the horizontal semicircular canal; M.a.m.e. facet: facet for attachment of musculus adductor mandibulae externus; sac: sacculus; ut: utriculus.</p

Skull roof of <i>Acamptonectes densus</i> (GLAHM 132588, holotype).

<p>A: articulated nasals in dorsal view. B: left nasal in lateral view. C: right supratemporal in dorsal view. D–F: supraoccipital magnified two times with respect to the other bones, in posterior view (D) and in left anterolateral (otic) view (E,F). Note the lateral wing of the nasal forming an overhang on the naris, the narial process of the nasal, the long and straight squamosal facet of the supratemporal, and the weakly arched shape of the supraoccipital. Abbreviations: avsc: impression of the anterior vertical semicircular canal; pvsc: impression of the posterior vertical semicircular canal; ut: utriculus.</p