Why ichthyosaurs — marine Mesozoic reptiles — disappeared before the dinosaur extinction has remained a mystery. New research suggests they may have gone extinct stepwise, during one of the most extreme greenhouse periods in the history of complex life-forms.

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1 McGowan C. The Dragon Seekers: How an Extraordinary Circle of Fossilists Discovered the Dinosaurs and Paved the Way for Darwin. 2 McGowan C.

Motani R. 3 Carroll R.L. Evolutionary constraints in aquatic diapsid reptiles. 4 Motani R.

Rothschild B.M.

Wahl W. Large eyeballs in diving ichthyosaurs. 5 Fernandez M.S. Dorsal or ventral? Homologies of the forefin of Caypullisaurus (Ichthyosauria: Ophthalmosauria). 6 Kolb C.

Sander P.M. Redescription of the ichthyosaur Platypterygius hercynicus (KUHN 1946) from the Lower Cretaceous of Salzgitter (Lower Saxony, Germany). 7 Kelley N.P.

Pyenson N.D. Evolutionary innovation and ecology in marine tetrapods from the Triassic to the Anthropocene. 8 Fischer V.

Bardet N.

Benson R.B.J.

Arkhangelsky M.S.

Friedman M. Extinction of fish-shaped marine reptiles associated with reduced evolutionary rates and global environmental volatility. Figure 1 Temnodontosaurus platyodon, the first ichthyosaur to be collected by Mary Anning and her brother. Show full caption 19 Home E. Some accounts of the fossil remains of an animal more nearly allied to fishes than any of the other classes of animals. A skeletal reconstruction based on two fossil skeletons, and the original illustration of the first skull given by Home (1814). Temnodontosaurus was the apex marine predator of its time, about 195 million years ago. The silhouette surrounding the skeleton is approximate. In 1811, Mary Anning and her brother found the fossil skull of a giant reptile on a beach in Lyme Regis in Dorset, England. This find triggered an era of paleontological discoveries that eventually led Richard Owen to christen a new class of extinct reptiles, the Dinosauria, in 1842 []. But ironically, the first skull was not of a dinosaur — it belonged to Temnodontosaurus platyodon, an ichthyosaur ( Figure 1 ). Ichthyosaurs are an iconic group of marine reptiles that are best known for the evolution of a fish-shaped body, which is reflected in their name that means ‘fish lizard’ []. They are often portrayed as the reptiles that were best-adapted to marine life []. Ranging from half a meter to over 20 meters in body length, most ichthyosaurs were pelagic predators of fish, squid-like cephalopods and sometimes other marine reptiles. They are noted for the records for the largest eyeball among vertebrate animals [], and the highest number of digits, with at least eight []. Ichthyosaurs were indeed very successful and remained a major component of marine predator guilds for more than 150 million years []. One of the greatest mysteries surrounding this celebrated group is their extinction. Ichthyosaurs became extinct long before the dinosaur extinction, when some other, seemingly less well-adapted marine reptiles survived. The cause of this ‘unreasonable’ extinction has never been clearly explained. Finally, a new study by Valentin Fischer and colleagues casts new light on this issue [].

9 Baird D. No ichthyosaurs in the Upper Cretaceous of New Jersey… or Saskatchewan. 10 Bardet N. Stratigraphic evidence for the extinction of the ichthyosaurs. 11 Bambach R.K. Phanerozoic biodiversity mass extinctions. 12 Schlanger S.O.

Jenkyns H.C. Cretaceous oceanic anoxic events: causes and consequences. 10 Bardet N. Stratigraphic evidence for the extinction of the ichthyosaurs. 13 McGowan C. Dinosaurs, Spitfires, and Sea Dragons. 14 Fischer V.

Bardet N.

Guiomar M.

Godefroit P. High diversity in Cretaceous ichthyosaurs from Europe prior to their extinction. 8 Fischer V.

Bardet N.

Benson R.B.J.

Arkhangelsky M.S.

Friedman M. Extinction of fish-shaped marine reptiles associated with reduced evolutionary rates and global environmental volatility. It had been known for a few decades that the ichthyosaurian fossil record ends in a time period called the Cenomanian (∼100.5 to ∼93.9 million years ago) [], the first geologic age of the Late Cretaceous epoch. The Cenomanian was an unusual time period. The extinction rate of marine life was elevated in the late Cenomanian [], which ended with a notorious event during which a large percentage of the seafloor became anoxic []. Natalie Bardet pointed out in 1992 that the disappearance of the ichthyosaurs may have been related to this marine extinction event [], based on a pivotal investigation of the time ranges of ichthyosaurian species in the Cretaceous. One of the questions has been whether the evolutionary diversity and disparity of ichthyosaurs were already declining in the Early Cretaceous [], ahead of the anoxic event, making them susceptible to extinction. However, a recent careful examination of the ichthyosaurian fossil record concluded that their diversity remained high until the Cenomanian []. The new study by Fischer et al. [] builds on these early works by improving the temporal resolution to the subage level (i.e., an average data resolution of about three million years, as opposed to about 7.3 previously) and refining statistical treatments in a trial to clarify what may have happened during the last chapters of ichthyosaurian existence.

8 Fischer V.

Bardet N.

Benson R.B.J.

Arkhangelsky M.S.

Friedman M. Extinction of fish-shaped marine reptiles associated with reduced evolutionary rates and global environmental volatility. The new study [] reaches three novel conclusions: first, the extinction of ichthyosaurs occurred in two steps within the Cenomanian, where early and final extinction peaks are recognized. Second, the Early Cenomanian extinction reduced ichthyosaurian diversity and variation in feeding strategy, without the subsequent origination of new phenotypes to fill the ecological vacancy until the final extinction in the Late Cenomanian. Fish and squid feeders were eliminated, leaving only a group of apex predators. And third, the extinction rate increased with rising environmental volatility, including changes in sea levels and carbon dioxide levels in the atmosphere, which, according to the rising consensus, disturbed the marine ecosystem globally by reducing the diversity of many organisms, from microplankton to ammonites, while enabling rapid radiations of others. It now seems that the extinction of ichthyosaurs proceeded stepwise over the about four million years of the Cenomanian. The new findings represent a significant advance of our understanding of the ichthyosaurian extinction, but some scrutiny may be due, as discussed below.

Some important questions still remain to be answered. Most of all, if the extinction of ichthyosaurs was driven by global environmental changes, why did some other marine reptiles survive the same time interval? Apart from ichthyosaurs, four more lineages of marine reptiles lived in the Cenomanian, namely plesiosaurs, a group of long-necked marine reptiles that was supposedly used as a model for the imaginary Loch Ness Monster, mosasauroids, a group of seagoing lizards, sea turtles, and marine snakes such as Pachyrhachis. Three of them survived the late Cenomanian extinction, although one of them, mosasauroids, experienced a significant change in their anatomy that seems to have improved their aquatic adaptation. It would be important to examine if plesiosaurs, the largest clade that survived, also experienced a similar reduction in diversity and disparity during the Early Cretaceous, in a trial to tease out the factors specific to ichthyosaurs that may have contributed to their extinction.

8 Fischer V.

Bardet N.

Benson R.B.J.

Arkhangelsky M.S.

Friedman M. Extinction of fish-shaped marine reptiles associated with reduced evolutionary rates and global environmental volatility. 12 Schlanger S.O.

Jenkyns H.C. Cretaceous oceanic anoxic events: causes and consequences. The fossil record is inherently incomplete. This raises the question of whether the dataset has a sufficiently high resolution and completeness for the relevant segment of ichthyosaurian evolution. This problem was recognized by the new study by Fischer et al. [], which tried its best to account for the incompleteness of the data using statistical tests. However, at least some of these tests may not be as conclusive as they may appear. For example, the paper claimed that ichthyosaurs were extinct by the earliest Turonian, the geologic age after the Cenomanian, at the latest based on a statistical confidence interval calculated from the fossil record density. However, this method, which was originally designed to examine local stratigraphic ranges of small taxonomic units, such as species [], may be misleading when used outside of the original context. Most importantly, it inherently narrows the confidence interval as increasingly inclusive taxonomic units are analyzed. That is, if the interval was calculated for the genus Platypterygius alone instead of the entire ichthyosaurs, then the interval would be wider, i.e., the genus potentially outlived the group that contained it. The precise timing of ichthyosaur extinction will still need to be scrutinized in the future.

15 Fu W.

Jiang D.

Montañez I.P.

Meyers S.R.

Motani R. Timing of Olenekian carbon cycle events and the recovery of oceanic ecosystem following the end-Permian extinction. Another problem with the dataset is the coarse resolution of the temporal axis. The main dataset has an average resolution of around three million years, i.e., the average span of geologic subages in the Early Cretaceous. Therefore, even if a species is known from a single fossil specimen, it appears as if it was consistently present during a time interval of three million years. The paper argues that the confidence interval of the extinction timing is 0.99 million years but this value is smaller than the data resolution, and may need to be rounded up to a unit time, i.e., three million years. This would place the latest possibility of ichthyosaurian extinction to the Late Turonian subage, affecting the rest of the argument. It is possible to place much finer temporal resolution of about ∼0.1 million years using geochemical records of planetary movement cycles, as, for example, being done to study the emergence of ichthyosaurs []. It seems necessary to improve the temporal resolution of the data in the future to strengthen the argument of the timing of ichthyosaurian extinction.

8 Fischer V.

Bardet N.

Benson R.B.J.

Arkhangelsky M.S.

Friedman M. Extinction of fish-shaped marine reptiles associated with reduced evolutionary rates and global environmental volatility. 16 Marshall C.R. Using confidence intervals to quantify the uncertainty in the end-Points of stratigraphic ranges. For a similar set of reasons, the raised extinction rate of ichthyosaurs in the Early Cenomanian may need to be reexamined carefully before it is widely accepted. Although it appears as if several species became extinct during a short time span within the Early Cenomanian [], this may at least partly be an artefact of the low temporal resolution, as well as the incompleteness of the record. It is more likely that some of these species lasted longer than they appear and the others shorter, and this possibility needs to be examined by calculating the confidence interval of the stratigraphic range for each species []. However, we may not have sufficient data to allow such a rigorous test at this point.