Abstract Elasmosaurid plesiosaurians were globally prolific marine reptiles that dominated the Mesozoic seas for over 70 million years. Their iconic body-plan incorporated an exceedingly long neck and small skull equipped with prominent intermeshing ‘fangs’. How this bizarre dental apparatus was employed in feeding is uncertain, but fossilized gut contents indicate a diverse diet of small pelagic vertebrates, cephalopods and epifaunal benthos. Here we report the first plesiosaurian tooth formation rates as a mechanism for servicing the functional dentition. Multiple dentine thin sections were taken through isolated elasmosaurid teeth from the Upper Cretaceous of Sweden. These specimens revealed an average of 950 daily incremental lines of von Ebner, and infer a remarkably protracted tooth formation cycle of about 2–3 years–other polyphyodont amniotes normally take ~1–2 years to form their teeth. Such delayed odontogenesis might reflect differences in crown length and function within an originally uneven tooth array. Indeed, slower replacement periodicity has been found to distinguish larger caniniform teeth in macrophagous pliosaurid plesiosaurians. However, the archetypal sauropterygian dental replacement system likely also imposed constraints via segregation of the developing tooth germs within discrete bony crypts; these partly resorbed to allow maturation of the replacement teeth within the primary alveoli after displacement of the functional crowns. Prolonged dental formation has otherwise been linked to tooth robustness and adaption for vigorous food processing. Conversely, elasmosaurids possessed narrow crowns with an elongate profile that denotes structural fragility. Their apparent predilection for easily subdued prey could thus have minimized this potential for damage, and was perhaps coupled with selective feeding strategies that ecologically optimized elasmosaurids towards more delicate middle trophic level aquatic predation.

Citation: Kear BP, Larsson D, Lindgren J, Kundrát M (2017) Exceptionally prolonged tooth formation in elasmosaurid plesiosaurians. PLoS ONE 12(2): e0172759. https://doi.org/10.1371/journal.pone.0172759 Editor: Matt Friedman, University of Michigan, UNITED STATES Received: November 24, 2015; Accepted: February 9, 2017; Published: February 27, 2017 Copyright: © 2017 Kear et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: All data is contained within the paper. All specimens and metadata are accessioned into the publicly accessible collection at the Museum of Evolution, Uppsala University, Sweden. Funding: Funded by BK: Australian Research Council (LP100100339); Swedish Research Council (2011-3637). JL: Swedish Research Council (2011-3587). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.

Discussion Our evidence for protracted tooth formation in dental remains attributed to the Late Cretaceous elasmosaurid Scanisaurus concurs with previous reports of extended dental replacement cycles in plesiosaurians and other more basal sauropterygians [18, 26–28]. Indeed, delayed replacement periodicity might have been broadly characteristic of these clades (and been influenced by thecodont gomphosis, indeterminate growth and metabolism [49]), but has been more specifically linked to regionalized tooth shape variation and enlargement in heterodont pliosaurids [18]. The detection of prolonged tooth formation times in Scanisaurus could therefore indicate a comparable adaptation towards discretized tooth function, which in anisodont elasmosaurids presumably involved selective elongation of the premaxillary-maxillary and dentary ‘fangs’ via modified growth periods and rate of odontoblast/ameloblast differentiation during apical dentine secretion [42]. Nevertheless, not all elasmosaurids were anisodont [13, 20, 21], implying that disparate tooth arrangements could evince contrasting formation rates between elasmosaurid taxa (a phenomenon recognized elsewhere in polyphyodont amniotes [37, 50]). This has particular pertinence for Scanisaurus, which is frequently compared with homodont elasmosaurids such as Aristonectes [31, 34], but may have alternative affinities based on its delayed tooth formation pattern. Another important implication is the increased likelihood of severe tooth wear, breakage and/or related disease [30, 37]. Certainly, dental pathologies have been described in plesiosaurians before (mainly larger-skulled ‘pliosauromorphs’ [10, 51]), as has chronic tooth-associated bone deformation [52]. Notably, densely spaced dentine increments [39], apparently slow tooth replacement [53], and caries [54] have also all been documented in ichthyosaurians. In contrast, only superficial wear and missing teeth have thus far been described in elasmosaurids [6, 10], which likewise lacked robust crowns more typically associated with prolonged tooth development and macrophagous diets [10, 30, 38]. This might be explained by preferential feeding (inferred from bromalite contents [10, 14, 16]) on relatively small, easily subdued prey that was swallowed whole and processed using gastroliths in the gut [55]. Such dietary specialization potentially evolved hand-in-hand with the need to minimise excessive tooth damage, and was likely further coupled with selective foraging strategies that employed the slender interdigitating teeth to entrap, pierce or sieve prey from the water column and fine seafloor sediments (e.g. silt and mud); non-selective suspension feeding has been critiqued because of structural constraints on the reptilian pharynx [56]. Delayed tooth formation, together with ‘alveolarized’ replacement and heterogenous dental configurations could therefore have been a key factor constraining the adaptive radiation of elasmosaurids as middle trophic-level aquatic predators, and perhaps indirectly contributed to their environmental [57, 58] and geographical prevalence [19] via the capacity to utilize a wider range of available food resources.

Acknowledgments Peter Sečkár (Comenius University) produced the petrographic thin sections. Jan Ove Ebbestad (PMU) assisted with collections access. Sven Sachs (Naturkunde-Museum Bielefeld) provided original photographs for Fig 1B–1E. Matt Friedman (University of Oxford) and two anonymous reviewers contributed constructive comments.

Author Contributions Conceptualization: BPK MK. Data curation: MK DL BPK. Formal analysis: BPK MK DL. Funding acquisition: BPK. Investigation: DL MK BPK JL. Methodology: MK DL. Project administration: BPK MK. Resources: BPK MK. Software: MK BPK. Supervision: MK BPK. Validation: MK DL BPK. Visualization: DL BPK. Writing – original draft: BPK JL. Writing – review & editing: BPK JL.