Pre- versus post-mass extinction divergence of Mesozoic marine reptiles dictated by time-scale dependence of evolutionary rates.

The fossil record of a major clade often starts after a mass extinction even though evolutionary rates, molecular or morphological, suggest its pre-extinction emergence (e.g. squamates, placentals and teleosts). The discrepancy is larger for older clades, and the presence of a time-scale-dependent methodological bias has been suggested, yet it has been difficult to avoid the bias using Bayesian phylogenetic methods. This paradox raises the question of whether ecological vacancies, such as those after mass extinctions, prompt the radiations. We addressed this problem by using a unique temporal characteristic of the morphological data and a high-resolution stratigraphic record, for the oldest clade of Mesozoic marine reptiles, Ichthyosauromorpha. The evolutionary rate was fastest during the first few million years of ichthyosauromorph evolution and became progressively slower over time, eventually becoming six times slower. Using the later slower rates, estimates of divergence time become excessively older. The fast, initial rate suggests the emergence of ichthyosauromorphs after the end-Permian mass extinction, matching an independent result from high-resolution stratigraphic confidence intervals. These reptiles probably invaded the sea as a new ecosystem was formed after the end-Permian mass extinction. Lack of information on early evolution biased Bayesian clock rates.

Trophic convergence drives morphological convergence in marine tetrapods.

Marine tetrapod clades (e.g. seals, whales) independently adapted to marine life through the Mesozoic and Caenozoic, and provide iconic examples of convergent evolution. Apparent morphological convergence is often explained as the result of adaptation to similar ecological niches. However, quantitative tests of this hypothesis are uncommon. We use dietary data to classify the feeding ecology of extant marine tetrapods and identify patterns in skull and tooth morphology that discriminate trophic groups across clades. Mapping these patterns onto phylogeny reveals coordinated evolutionary shifts in diet and morphology in different marine tetrapod lineages. Similarities in morphology between species with similar diets-even across large phylogenetic distances-are consistent with previous hypotheses that shared functional constraints drive convergent evolution in marine tetrapods.

Bone-eating Osedax worms lived on Mesozoic marine reptile deadfalls.

We report fossil traces of Osedax, a genus of siboglinid annelids that consume the skeletons of sunken vertebrates on the ocean floor, from early-Late Cretaceous (approx. 100 Myr) plesiosaur and sea turtle bones. Although plesiosaurs went extinct at the end-Cretaceous mass extinction (66 Myr), chelonioids survived the event and diversified, and thus provided sustenance for Osedax in the 20 Myr gap preceding the radiation of cetaceans, their main modern food source. This finding shows that marine reptile carcasses, before whales, played a key role in the evolution and dispersal of Osedax and confirms that its generalist ability of colonizing different vertebrate substrates, like fishes and marine birds, besides whale bones, is an ancestral trait. A Cretaceous age for unequivocal Osedax trace fossils also dates back to the Mesozoic the origin of the entire siboglinid family, which includes chemosynthetic tubeworms living at hydrothermal vents and seeps, contrary to phylogenetic estimations of a Late Mesozoic-Cenozoic origin (approx. 50-100 Myr).

Total body water and water turnover rates in the estuarine diamondback terrapin (Malaclemys terrapin) during the transition from dormancy to activity.

Water and salt concentrations in an animal's body fluids can fluctuate with changing environmental conditions, posing osmoregulatory challenges that require behavioral and physiological adjustments. The purpose of this study was to investigate body water dynamics in the estuarine diamondback terrapin (Malaclemys terrapin), a species that undergoes seasonal dormancy in salt marsh habitats. We conducted a field study to determine the total body water (%TBW), water turnover rate (WTR) and daily water flux (DWF) of female terrapins in south eastern North Carolina pre- and post-emergence from winter dormancy. Terrapins were injected with [(2)H]deuterium on two occasions and washout of the isotope was monitored by taking successive blood samples during the period of transition from dormancy to activity. The WTR and DWF of dormant terrapins were significantly lower than those of active terrapins (WTR(dormant)=49.70±15.94 ml day(-1), WTR(active)=100.20±20.36 ml day(-1), DWF(dormant)=10.52±2.92%TBW day(-1), DWF(active)=21.84±7.30%TBW day(-1)). There was no significant difference in %TBW between dormant and active terrapins (75.05±6.19% and 74.54±4.36%, respectively). The results from this field study provide insight into the terrapin's ability to maintain osmotic homeostasis while experiencing shifts in behavioral and environmental conditions.

Complex dental wear analysis reveals dietary shift in Triassic placodonts (Sauropsida, Sauropterygia).

Placodonts were durophagous reptiles of the Triassic seas with robust skulls, jaws, and enlarged, flat, pebble-like teeth. During their evolution, they underwent gradual craniodental changes from the Early Anisian to the Rhaetian, such as a reduction in the number of teeth, an increase in the size of the posterior palatal teeth, an elongation of the premaxilla/rostrum, and a widening of the temporal region. These changes are presumably related to changes in dietary habits, which, we hypothesise, are due to changes in the type and quality of food they consumed. In the present study, the dental wear pattern of a total of nine European Middle to Late Triassic placodont species were investigated using 2D and 3D microwear analyses to demonstrate whether there could have been a dietary shift or grouping among the different species and, whether the possible changes could be correlated with environmental changes affecting their habitats. The 3D analysis shows overlap between species with high variance between values and there is no distinct separation. The 2D analysis has distinguished two main groups. The first is characterised by low number of wear features and high percentage of large pits. The other group have a high feature number, but low percentage of small pits. The 2D analysis showed a correlation between the wear data and the size of the enlarged posterior crushing teeth. Teeth with larger sizes showed less wear feature (with higher pit ratio) but larger individual features. In contrast, the dental wear facet of smaller crushing teeth shows more but smaller wear features (with higher scratch number). This observation may be related to the size of the food consumed, i.e., the wider the crown, the larger food it could crush, producing larger features. Comparison with marine mammals suggests that the dietary preference of Placochelys, Psephoderma and Paraplacodus was not exclusively hard, thick-shelled food. They may have had a more mixed diet, similar to that of modern sea otters. The diet of Henodus may have included plant food, similar to the modern herbivore marine mammals and lizards. Supplementary Information: The online version contains supplementary material available at 10.1186/s13358-024-00304-x.

Late Jurassic teeth of plesiosauroid origin from the Owadów-Brzezinki Lägerstatte, Central Poland.

Owadów-Brzezinki is currently one of the most promising Upper Jurassic sites in Central Poland, with a wide array of both vertebrate and invertebrate fossil fauna present. The discoveries of large-bodied marine reptiles fossils such as ichthyosaurs, turtles, and marine crocodylomorphs attracted attention to the location. A particular Mesozoic marine group, plesiosaurs, remained to be found, and in this report, we note four isolated teeth with distinguishing apicobasal ridging pattern and elongated, conical shape characteristic for plesiosaurians. The outcomes of the Principal Coordinates Analysis (PCoA) of the largest and most complete tooth specimen ZPAL R.11/OB/T4 enabled us to confirm its classification as Plesiosauroidea. This discovery affirms the importance of the site as the area of mixing between Boreal and Tethyan faunas, expanding the broad spectrum of fossil taxa found in this location. Together with previous findings of plesiosaur material in a nearby region, it provides the evidence for the presence of Plesiosauroidea in Owadów-Brzezinki Lägerstatte.

Rapid neck elongation in Sauropterygia (Reptilia: Diapsida) revealed by a new basal pachypleurosaur from the Lower Triassic of China.

Neck elongation has appeared independently in several tetrapod groups, including giraffes and sauropod dinosaurs on land, birds and pterosaurs in the air, and sauropterygians (plesiosaurs and relatives) in the oceans. Long necks arose in Early Triassic sauropterygians, but the nature and rate of that elongation has not been documented. Here, we report a new species of pachypleurosaurid sauropterygian, Chusaurus xiangensis gen. et sp. nov., based on two new specimens from the Early Triassic Nanzhang-Yuan'an Fauna in the South China Block. The new species shows key features of its Middle Triassic relatives, but has a relatively short neck, measuring 0.48 of the trunk length, compared to > 0.8 from the Middle Triassic onwards. Comparative phylogenetic analysis shows that neck elongation occurred rapidly in all Triassic eosauropterygian lineages, probably driven by feeding pressure in a time of rapid re-establishment of new kinds of marine ecosystems.

A new long-necked archosauromorph from the Guanling Formation (Anisian, Middle Triassic) of southwestern China and its implications for neck evolution in tanystropheids.

A long neck is an evolutionary innovation convergently appearing in multiple tetrapod lineages, including groups of plesiosaurs, non-archosauriform archosauromorphs, turtles, sauropodomorphs, birds, and mammals. Among all tetrapods both extant and extinct, two Triassic archosauromorphs, Tanystropheus and Dinocephalosaurus, have necks that are particularly elongated relative to the lengths of their trunks. However, the evolutionary history of such hyper-elongated necks in these two archosauromorph clades remains unknown, partially because known close relatives such as Macrocnemus and Pectodens possess only moderately elongated necks. Here, we describe a newly discovered early diverging archosauromorph, Gracilicollum latens gen. et sp. nov., based on a specimen comprising a partial neck and an incompletely preserved skull. The long neck is composed of at least 18 cervical vertebrae. The dentition suggests that this new taxon most likely represents an aquatic piscivore, similar to Dinocephalosaurus and Tanystropheus hydroides. Despite possessing a high number of cervical vertebrae, Gracilicollum gen. nov. is recovered as a tanystropheid in an evolutionary grade between Macrocnemus and Tanystropheus rather than as a close relative of Dinocephalosaurus, a result that is primarily attributable to the presence of palatal teeth and the anatomy of the cervical vertebrae in Gracilicollum gen. nov. Considering the information provided by the new specimen, we provide a detailed discussion of the cervical evolution in dinocephalosaurids and tanystropheids, which is shown to be highly complex and mosaic in nature.

Heart rate as a proxy for estimating oxygen consumption rates in loggerhead turtles (Caretta caretta).

Heart rates of air-breathing diving animals can change on a short time scale due to the diving response during submergence. Heart rate is used frequently as a proxy for indirectly estimating metabolic rates on a fine time scale. However, most studies to date have been conducted on endothermic diving animals, and the relationships between metabolic rates and heart rates in ectothermic diving animals have not been well studied. Sea turtles are unique model organisms of diving ectotherms because they spend most of their life in the ocean and perform deep and/or long dives. In this study, we examined the relationship between heart rates and metabolic rates in captive loggerhead turtles, Caretta caretta, to estimate oxygen consumption rates during each dive based on heart rates. The oxygen consumption rates (V̇O2: mlO2 min-1 kg-1) and average heart rates (fH: beats min-1) were measured simultaneously in indoor tanks at water temperatures of 15-25°C. Our results showed that oxygen consumption rate was affected by heart rate and water temperature in loggerhead turtles. Based on the collected data, we formulated the model equation as V̇O2=0.0124fH+0.0047Tw - 0.0791. The equation can be used for estimating fine-scaled field metabolic rates in free-ranging loggerhead turtles. The results of this study will contribute to future comparative studies of the physiological states of ectothermic diving animals.

Oil spill causes mass mortality of sea snakes in the Gulf of Oman.

Oil spills in the marine environment inflict significant impacts on a wide diversity of marine fauna. Despite the abundance of literature describing these impacts on numerous species, no studies describe the impacts on sea snakes. In this study we report, for the first time, details of an oil spill which caused mass mortality of sea snakes. In this study, 39 sea snake mortalities from the Gulf of Oman, in particular, the coast of Kalba, Sharjah, UAE, were examined. The investigated sea snakes belong to four different species (Hydrophis platurus, H. lapemoides, H. spiralis and H. ornatus). The majority (84.6%) of sea snakes were observed to have oil covering 75-100% of their bodies. The majority (91.4%) of sea snakes were also observed with oil covering their snouts and eyes. A large proportion (25.8, 41.4 and 34.5%) of sea snakes were observed with oil in their mouth, esophagus and stomach.

The oldest record of Saurosphargiformes (Diapsida) from South China could fill an ecological gap in the Early Triassic biotic recovery.

Diversification following the end-Permian mass extinction marks the initiation of Mesozoic reptile dominance and of modern marine ecosystems, yet major clades are best known from the Middle Triassic suggesting delayed recovery, while Early Triassic localities produce poorly preserved specimens or have restricted diversity. Here we describe Pomolispondylus biani gen. et sp. nov. from the Early Triassic Nanzhang-Yuan'an Fauna of China assigned to Saurosphargiformes tax. nov., a clade known only from the Middle Triassic or later, which includes Saurosphargidae, and likely is the sister taxon to Sauropterygia. Pomolispondylus biani is allied to Saurosphargidae by the extended transverse processes of dorsal vertebrae and a low, table-like dorsal surface on the neural spine; however, it does not have the typical extensive osteoderms. Rather an unusual tuberous texture on the dorsal neural spine and rudimentary ossifications lateral to the gastralia are observed. Discovery of Pomolispondylus biani extends the known range of Saurosphargiformes and increases the taxic and ecological diversity of the Nanzhang-Yuan'an Fauna. Its small size fills a different ecological niche with respect to previously found species, but the overall food web remains notably different in structure to Middle Triassic and later ecosystems, suggesting this fauna represents a transitional stage during recovery rather than its endpoint.

Ecophysiological steps of marine adaptation in extant and extinct non-avian tetrapods.

Marine reptiles and mammals are phylogenetically so distant from each other that their marine adaptations are rarely compared directly. We reviewed ecophysiological features in extant non-avian marine tetrapods representing 31 marine colonizations to test whether there is a common pattern across higher taxonomic groups, such as mammals and reptiles. Marine adaptations in tetrapods can be roughly divided into aquatic and haline adaptations, each of which seems to follow a sequence of three steps. In combination, these six categories exhibit five steps of marine adaptation that apply across all clades except snakes: Step M1, incipient use of marine resources; Step M2, direct feeding in the saline sea; Step M3, water balance maintenance without terrestrial fresh water; Step M4, minimized terrestrial travel and loss of terrestrial feeding; and Step M5, loss of terrestrial thermoregulation and fur/plumage. Acquisition of viviparity is not included because there is no known case where viviparity evolved after a tetrapod lineage colonized the sea. A similar sequence is found in snakes but with the haline adaptation step (Step M3) lagging behind aquatic adaptation (haline adaptation is Step S5 in snakes), most likely because their unique method of water balance maintenance requires a supply of fresh water. The same constraint may limit the maximum body size of fully marine snakes. Steps M4 and M5 in all taxa except snakes are associated with skeletal adaptations that are mechanistically linked to relevant ecophysiological features, allowing assessment of marine adaptation steps in some fossil marine tetrapods. We identified four fossil clades containing members that reached Step M5 outside of stem whales, pinnipeds, sea cows and sea turtles, namely Eosauropterygia, Ichthyosauromorpha, Mosasauroidea, and Thalattosuchia, while five other clades reached Step M4: Saurosphargidae, Placodontia, Dinocephalosaurus, Desmostylia, and Odontochelys. Clades reaching Steps M4 and M5, both extant and extinct, appear to have higher species diversity than those only reaching Steps M1 to M3, while the total number of clades is higher for the earlier steps. This suggests that marine colonizers only diversified greatly after they minimized their use of terrestrial resources, with many lineages not reaching these advanced steps. Historical patterns suggest that a clade does not advance to Steps M4 and M5 unless these steps are reached early in the evolution of the clade. Intermediate forms before a clade reached Steps M4 and M5 tend to become extinct without leaving extant descendants or fossil evidence. This makes it difficult to reconstruct the evolutionary history of marine adaptation in many clades. Clades that reached Steps M4 and M5 tend to last longer than other marine tetrapod clades, sometimes for more than 100 million years.

Identification of Gastrointestinal Microbiota in Hawaiian Green Turtles (Chelonia mydas).

Green turtles (Chelonia mydas) have a hindgut fermentation digestive tract, which uses cellulolytic microbes to break down plant matter in the cecum and proximal colon. Previous studies on bacterial communities of green turtles have not identified in situ hindgut microbiota, and never before in Hawaiian green turtles, which comprise an isolated metapopulation. Fresh samples using sterile swabs were taken from five locations along the gastrointestinal tracts of eight green turtles that had required euthanization. Bacteria were cultured, aerobically and anaerobically, on nutrient agar and four differential and selective media. Samples at three sections along the gastrointestinal tracts of two green turtles were analyzed using 16S metagenomics on an Ion Torrent Personal Genome Machine. More than half of the 4 532 104 sequences belonged to the phylum Firmicutes, followed by Bacteroidetes and Proteobacteria, which are characteristic of herbivore gut microbiota. Some microbiota variation existed between turtles and among gastrointestinal sections. The 16S sequence analysis provided a better representation of the total gastrointestinal bacterial community, much of which cannot be cultured using traditional microbial techniques. These metagenomic analyses serve as a foundation for a better understanding of the microbiome of green turtles in the Hawaiian Islands and elsewhere.

Neck mobility in the Jurassic plesiosaur Cryptoclidus eurymerus: finite element analysis as a new approach to understanding the cervical skeleton in fossil vertebrates.

The sauropterygian clade Plesiosauria arose in the Late Triassic and survived to the very end of the Cretaceous. Plesiosauria evolved the greatest species diversity of any marine reptile clade, attaining a global distribution. Plesiosauria consist of two clades, Rhomaleosauridae and Neoplesiosauria. Basal Neoplesiosauria have long necks with at least 30 cervicals, but show qualitative osteological evidence for a stiff neck. Here we quantify neck mobility in lateral, ventral, and dorsal directions based on finite element modeling of neck vertebrae from the Middle Jurassic plesiosaur Cryptoclidus eurymerus. We model the mobility in a single motion segment, consisting of two adjacent cervical vertebrae and the joints connecting them. Based on the model with a maximum intervertebral spacing of 3 mm, we find that in Cryptoclidus, the maximum angle of lateral deflection in the motion segment was 2°. The maximum angle of ventral deflection was 5° and of dorsal deflection was 5°. When these values are multiplied by the number of cervical vertebrae, it becomes apparent that neck mobility was limited in all directions. The maximum angle of total lateral deflection in the neck was 67°. The maximum angle of total ventral deflection was 148° and of total dorsal deflection was 157°. This raises the question of the function of such a long, multi-segment but immobile neck. We posit that the long neck served in hydrodynamic and visual camouflage, hiding the bulk of the body from the small but abundant prey, such as schooling fish and squid. Neck immobility may have been advantageous in withstanding strong hydrodynamic forces acting on the neck during predatory strikes.

Quantitative histological models suggest endothermy in plesiosaurs.

BACKGROUND: Plesiosaurs are marine reptiles that arose in the Late Triassic and survived to the Late Cretaceous. They have a unique and uniform bauplan and are known for their very long neck and hydrofoil-like flippers. Plesiosaurs are among the most successful vertebrate clades in Earth's history. Based on bone mass decrease and cosmopolitan distribution, both of which affect lifestyle, indications of parental care, and oxygen isotope analyses, evidence for endothermy in plesiosaurs has accumulated. Recent bone histological investigations also provide evidence of fast growth and elevated metabolic rates. However, quantitative estimations of metabolic rates and bone growth rates in plesiosaurs have not been attempted before. METHODS: Phylogenetic eigenvector maps is a method for estimating trait values from a predictor variable while taking into account phylogenetic relationships. As predictor variable, this study employs vascular density, measured in bone histological sections of fossil eosauropterygians and extant comparative taxa. We quantified vascular density as primary osteon density, thus, the proportion of vascular area (including lamellar infillings of primary osteons) to total bone area. Our response variables are bone growth rate (expressed as local bone apposition rate) and resting metabolic rate (RMR). RESULTS: Our models reveal bone growth rates and RMRs for plesiosaurs that are in the range of birds, suggesting that plesiosaurs were endotherm. Even for basal eosauropterygians we estimate values in the range of mammals or higher. DISCUSSION: Our models are influenced by the availability of comparative data, which are lacking for large marine amniotes, potentially skewing our results. However, our statistically robust inference of fast growth and fast metabolism is in accordance with other evidence for plesiosaurian endothermy. Endothermy may explain the success of plesiosaurs consisting in their survival of the end-Triassic extinction event and their global radiation and dispersal.

A new rhynchocephalian (Reptilia: Lepidosauria) from the Late Jurassic of Solnhofen (Germany) and the origin of the marine Pleurosauridae.

A new rhynchocephalian is described based on a recently discovered and well-preserved specimen from the Late Jurassic (Kimmeridgian) marine limestones of Solnhofen, Bavaria. Phylogenetic analysis recovers the new taxon as the sister group to Pleurosauridae, a small radiation of rhynchocephalians representing the oldest marine invasion of crown-clade Lepidosauria. The relatively strong evidence for this taxonomically exclusive lineage, within a generally volatile rhynchocephalian tree, places the new taxon in a position to inform the early history of the pleurosaur transition to the sea. The early steps in this transition are distributed throughout the skeleton and appear to increase hydrodynamic efficiency for both swimming and aquatic feeding. This early history may also have included a global truncation of plesiomorphic ontogenetic trajectories that left a number of skeletal features with reduced levels of ossification/fusion. The exact degree to which Vadasaurus had adopted an aquatic ecology remains unclear, but the insight it provides into the origin of the enigmatic pleurosaurs exemplifies the potential of Rhynchocephalia for generating and informing broad-based questions regarding the interplay of development, morphology, ecology and macroevolutionary patterns.

A new Lower Triassic ichthyopterygian assemblage from Fossil Hill, Nevada.

We report a new ichthyopterygian assemblage from Lower Triassic horizons of the Prida Formation at Fossil Hill in central Nevada. Although fragmentary, the specimens collected so far document a diverse fauna. One partial jaw exhibits isodont dentition with blunt tipped, mesiodistally compressed crowns and striated enamel. These features are shared with the Early Triassic genus Utatsusaurus known from coeval deposits in Japan and British Columbia. An additional specimen exhibits a different dentition characterized by relatively small, rounded posterior teeth resembling other Early Triassic ichthyopterygians, particularly Grippia. This Nevada assemblage marks a southward latitudinal extension for Early Triassic ichthyopterygians along the eastern margin of Panthalassa and indicates repeated trans-hemispheric dispersal events in Early Triassic ichthyopterygians.

Sea snakes rarely venture far from home.

The extent to which populations are connected by dispersal influences all aspects of their biology and informs the spatial scale of optimal conservation strategies. Obtaining direct estimates of dispersal is challenging, particularly in marine systems, with studies typically relying on indirect approaches to evaluate connectivity. To overcome this challenge, we combine information from an eight-year mark-recapture study with high-resolution genetic data to demonstrate extremely low dispersal and restricted gene flow at small spatial scales for a large, potentially mobile marine vertebrate, the turtleheaded sea snake (Emydocephalus annulatus). Our mark-recapture study indicated that adjacent bays in New Caledonia (<1.15 km apart) contain virtually separate sea snake populations. Sea snakes could easily swim between bays but rarely do so. Of 817 recaptures of marked snakes, only two snakes had moved between bays. We genotyped 136 snakes for 11 polymorphic microsatellite loci and found statistically significant genetic divergence between the two bays (F(ST)= 0.008, P < 0.01). Bayesian clustering analyses detected low mixed ancestry within bays and genetic relatedness coefficients were higher, on average, within than between bays. Our results indicate that turtleheaded sea snakes rarely venture far from home, which has strong implications for their ecology, evolution, and conservation.