Computational Fluid Dynamics Analysis of the Fossil Crinoid Encrinus liliiformis (Echinodermata: Crinoidea)

RESEARCH ARTICLE Computational Fluid Dynamics Analysis of the Fossil Crinoid Encrinus liliiformis (Echinodermata: Crinoidea) Janina F. Dynowski1,2, James H. Nebelsick2*, Adrian Klein3, Anita Roth-Nebelsick1 1 Staatliches Museum für Naturkunde Stuttgart, Stuttgart, Germany, 2 Fachbereich Geowissenschaften, Eberhard Karls Universität Tübingen, Tübingen, Germany, 3 Institut für Zoologie, Rheinische FriedrichWilhelms-Universität Bonn, Bonn, Germany * a11111 Abstract OPEN ACCESS Citation: Dynowski JF, Nebelsick JH, Klein A, RothNebelsick A (2016) Computational Fluid Dynamics Analysis of the Fossil Crinoid Encrinus liliiformis (Echinodermata: Crinoidea). PLoS ONE 11(5): e0156408. doi:10.1371/journal.pone.0156408 Editor: Stuart Humphries, University of Lincoln, UNITED KINGDOM Received: August 24, 2015 Accepted: May 14, 2016 Published: May 31, 2016 Copyright: © 2016 Dynowski 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 Statement: All relevant data are within the paper and its Supporting Information files. Crinoids, members of the phylum Echinodermata, are passive suspension feeders and catch plankton without producing an active feeding current. Today, the stalked forms are known only from deep water habitats, where flow conditions are rather constant and feeding velocities relatively low. For feeding, they form a characteristic parabolic filtration fan with their arms recurved backwards into the current. The fossil record, in contrast, provides a large number of stalked crinoids that lived in shallow water settings, with more rapidly changing flow velocities and directions compared to the deep sea habitat of extant crinoids. In addition, some of the fossil representatives were possibly not as flexible as today’s crinoids and for those forms alternative feeding positions were assumed. One of these fossil crinoids is Encrinus liliiformis, which lived during the middle Triassic Muschelkalk in Central Europe. The presented project investigates different feeding postures using Computational Fluid Dynamics to analyze flow patterns forming around the crown of E. liliiformis, including experimental validation by Particle Image Velocimetry. The study comprises the analysis of different flow directions, velocities, as well as crown orientations. Results show that inflow from lateral and oral leads to direct transport of plankton particles into the crown and onto the oral surface. With current coming from the “rear” (aboral) side of the crinoid, the conical opening of the crown produces a backward oriented flow in its wake that transports particles into the crown. The results suggest that a conical feeding position may have been less dependent on stable flow conditions compared to the parabolic filtration fan. It is thus assumed that the conical feeding posture of E. liliiformis was suitable for feeding under dynamically changing flow conditions typical for the shallow marine setting of the Upper Muschelkalk. Funding: This work was supported by Deutsche Forschungsgemeinschaft, grant number NE 537/24-1 (to JHN) and grant number RO 3250/20-1 (to ARN) (http://www.dfg.de/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Introduction Competing Interests: The authors have declared that no competing interests exist. Crinoids today live in all oceans, from littoral settings to about 9000 m water depth [1]. In general, two main groups are recognized: the stalked sea lilies, which today are restricted to deep PLOS ONE | DOI:10.1371/journal.pone.0156408 May 31, 2016 1 / 27 CFD Analysis of Encrinus liliiformis sea environments, and the unstalked feather stars, which occur in various environments, from the deep sea to shallow water habitats [2]. Stalked crinoids have existed since the early Palaeozoic and the fossil representatives, in contrast to living ones, were highly abundant and diverse in shallow water settings. Members of the class Crinoidea share a similar basic shape with the major organs located in the small cup or calyx, and a skeleton that is constructed of ossicles of high Mg calcite, which is covered by a thin integument [3] (Fig 1, S1 Fig). The arms, making up the filter apparatus, possess numerous pinnules, which in turn bear hundreds of small ambulacral tube feet, to which nutritive particles adhere [4–7]. Crinoids are passive suspension feeding animals thus depending on the movement of the surrounding water mass to supply them with food [8, 9]. Their main diet consists of miscellaneous planktonic organisms, with diameters typically less than 200 μm [10, 11]. Living stalked crinoids, which have only limited ability for locomotion [12], show a typical feeding position, with the arms bent into the incoming water flow, thus creating a simple but effective three dimensional filter, the so called parabolic filtration fan [13] (S1 Fig). In this posture, the concave side of the filter apparatus faces the current directly, while the particle catching tube feet are located on the leeward side. This leeward feeding with a dish-shaped filter is known from various suspension feeders and is interpreted as to increase fluid flux through the filter and particle capture efficiency in comparison to a planar arrangement [8, 14]. On the leeward side of such a filter, the velocity is reduced and turbulence occurs that leads to a recirculation of particles onto the filtering surface [8]. In crinoids, this feeding position is confined to special flow conditions, including unidirectional flow with velocities of up to 0.25 m/s [13,15]. Below a special threshold (approximately 0.01 m/s), insufficient numbers of particles would reach the animal to compensate the energy needed for capture, mainly due to the influence of the boundary layer around the feeding structures preventing plankton to penetrate through it and touch the sticky surface [16–18]. In slack currents, crinoids typically adopt an upright position with the oral surface facing upwards, resembling a wilted flower [13, 19, 20]. In high flow velocities, the drag on the crown and thus the strain on the stalk increases to such an extent that the crinoid Fig 1. Encrinus liliiformis. (A) Fossil crown from Crailsheim, Germany, showing typical preservation with arms opened to a slight extent (deposited in the collection of the State Museum of Natural History Stuttgart, specimen number SMNS21859). (B) Schematic illustration of morphological features. doi:10.1371/journal.pone.0156408.g001 PLOS ONE | DOI:10.1371/journal.pone.0156408 May 31, 2016 2 / 27 CFD Analysis of Encrinus liliiformis is in danger of becoming detached from the ocean floor once the force reaches a critical value. In strong currents, stalked crinoids close their arms forming a d (...truncated)