Information

14.21: Phylum Echinodermata - Biology

14.21: Phylum Echinodermata - Biology


We are searching data for your request:

Forums and discussions:
Manuals and reference books:
Data from registers:
Wait the end of the search in all databases.
Upon completion, a link will appear to access the found materials.

Learning Objectives

  • Describe the distinguishing characteristics of echinoderms
  • Identify the different classes in phylum Echinodermata

Characteristics of Echinoderms

Echinodermata are so named owing to their spiny skin (from the Greek “echinos” meaning “spiny” and “dermos” meaning “skin”), and this phylum is a collection of about 7,000 described living species. Echinodermata are exclusively marine organisms. Sea stars (Figure 1), sea cucumbers, sea urchins, sand dollars, and brittle stars are all examples of echinoderms. To date, no freshwater or terrestrial echinoderms are known.

Morphology and Anatomy

Adult echinoderms exhibit pentaradial symmetry and have a calcareous endoskeleton made of ossicles, although the early larval stages of all echinoderms have bilateral symmetry. The endoskeleton is developed by epidermal cells and may possess pigment cells, giving vivid colors to these animals, as well as cells laden with toxins. Gonads are present in each arm. In echinoderms like sea stars, every arm bears two rows of tube feet on the oral side. These tube feet help in attachment to the substratum. These animals possess a true coelom that is modified into a unique circulatory system called a water vascular system. An interesting feature of these animals is their power to regenerate, even when over 75 percent of their body mass is lost.

Water Vascular System

Echinoderms possess a unique ambulacral or water vascular system, consisting of a central ring canal and radial canals that extend along each arm. Water circulates through these structures and facilitates gaseous exchange as well as nutrition, predation, and locomotion. The water vascular system also projects from holes in the skeleton in the form of tube feet. These tube feet can expand or contract based on the volume of water present in the system of that arm. By using hydrostatic pressure, the animal can either protrude or retract the tube feet. Water enters the madreporite on the aboral side of the echinoderm. From there, it passes into the stone canal, which moves water into the ring canal. The ring canal connects the radial canals (there are five in a pentaradial animal), and the radial canals move water into the ampullae, which have tube feet through which the water moves. By moving water through the unique water vascular system, the echinoderm can move and force open mollusk shells during feeding.

Nervous System

The nervous system in these animals is a relatively simple structure with a nerve ring at the center and five radial nerves extending outward along the arms. Structures analogous to a brain or derived from fusion of ganglia are not present in these animals.

Excretory System

Podocytes, cells specialized for ultrafiltration of bodily fluids, are present near the center of echinoderms. These podocytes are connected by an internal system of canals to an opening called the madreporite.

Reproduction

Echinoderms are sexually dimorphic and release their eggs and sperm cells into water; fertilization is external. In some species, the larvae divide asexually and multiply before they reach sexual maturity. Echinoderms may also reproduce asexually, as well as regenerate body parts lost in trauma.

Classes of Echinoderms

This phylum is divided into five extant classes: Asteroidea (sea stars), Ophiuroidea (brittle stars), Echinoidea (sea urchins and sand dollars), Crinoidea (sea lilies or feather stars), and Holothuroidea (sea cucumbers) (Figure 2).

The most well-known echinoderms are members of class Asteroidea, or sea stars. They come in a large variety of shapes, colors, and sizes, with more than 1,800 species known so far. The key characteristic of sea stars that distinguishes them from other echinoderm classes includes thick arms (ambulacra) that extend from a central disk where organs penetrate into the arms. Sea stars use their tube feet not only for gripping surfaces but also for grasping prey. Sea stars have two stomachs, one of which can protrude through their mouths and secrete digestive juices into or onto prey, even before ingestion. This process can essentially liquefy the prey and make digestion easier.

Explore the sea star’s body plan up close, watch one move across the sea floor, and see it devour a mussel.

Brittle stars belong to the class Ophiuroidea. Unlike sea stars, which have plump arms, brittle stars have long, thin arms that are sharply demarcated from the central disk. Brittle stars move by lashing out their arms or wrapping them around objects and pulling themselves forward. Sea urchins and sand dollars are examples of Echinoidea. These echinoderms do not have arms, but are hemispherical or flattened with five rows of tube feet that help them in slow movement; tube feet are extruded through pores of a continuous internal shell called a test. Sea lilies and feather stars are examples of Crinoidea. Both of these species are suspension feeders. Sea cucumbers of class Holothuroidea are extended in the oral-aboral axis and have five rows of tube feet. These are the only echinoderms that demonstrate “functional” bilateral symmetry as adults, because the uniquely extended oral-aboral axis compels the animal to lie horizontally rather than stand vertically.


SCBI 208 Invertebrate Zoology

World Cafe Polychaete Model Making

การสอบปลายภาควิชา วทชว 208 สัตว์ไม่มีกระดูกสันหลัง ในภาคเรียนที่ 2 ปีการศึกษา 2561 เมื่อวันศุกร์ที่ 17 พฤษภาคม 2562 ที่ผ่านมา มีข้อหนึ่งที่ให้นักศึกษาร่วมกันทำโมเดลโพลีคีตในห้องสอบ และเนื่องจากเป็นการสอบแบบจำกัดเวลา หรือที่เรียกว่าแล็บกริ๊ง นักศึกษาแต่ละคน ที่วนมาถึงคำถามข้อนี้ จะมีเวลาเพียง 1 นาทีในการปั้นส่วนใดส่วนหนึ่งของโมเดล เมื่อหมดเวลาในแต่ละรอบการสอบ ซึ่งใช้เวลาประมาณ 21 นาที ทำให้ได้โมเดลที่สร้างจาก play dough ขึ้นมา 3 ตัว จาก 3 รอบการสอบ ดังภาพด้านบน

นักศึกษามีเวลา 1 นาทีในการทำบางส่วนของโมเดลโพลีคีต ต่อจากเพื่อน ๆ แบบจำลองสัตว์ไม่มีกระดูกสันหลังบางส่วนจากนักศึกษาชั้นปีที่ 3 ภาควิชาชีววิทยา ปีการศึกษา 2561-2562

การแสดงตัวอย่างแบบจำลองสัตว์ไม่มีกระดูกสันหลังในการจัดกิจกรรม One in a Hundred Science Fair เนื่องในงาน 100 ปี ชาตกาล ศาตราจารย์ ดร.สตางค์ มงคลสุข ณ ห้องประชุมอาคารสตางค์ มงคลสุข อาคารสตางค์ มงคลสุข คณะวิทยาศาสตร์ มหาวิทยาลัยมหิดล เมื่อวันพุธที่ 10 กรกฎาคม 2562 เวลา 1330-1630

Inverterbate Models


Contents

A widely accepted hypothesis, based on molecular data (mostly 18S rRNA sequences), divides Bilateria into four superphyla: Deuterostomia, Ecdysozoa, Lophotrochozoa, and Platyzoa (sometimes included in Lophotrochozoa). The last three groups are also collectively known as Protostomia. [ citation needed ]

However, some skeptics [ who? ] emphasize inconsistencies in the new data. The zoologist Claus Nielsen argues in his 2001 book Animal Evolution: Interrelationships of the Living Phyla for the traditional divisions of Protostomia and Deuterostomia. [ citation needed ]

It has been suggested that one type of molecular clock and one approach to interpretation of the fossil record both place the evolutionary origins of eumetazoa in the Ediacaran. [13] However, the earliest eumetazoans may not have left a clear impact on the fossil record and other interpretations of molecular clocks suggest the possibility of an earlier origin. [14] The discoverers of Vernanimalcula describe it as the fossil of a bilateral triploblastic animal that appeared at the end of the Marinoan glaciation prior to the Ediacaran Period, implying an even earlier origin for eumetazoans. [15]


14.3 Seed Plants: Gymnosperms

The first plants to colonize land were most likely closely related to modern-day mosses (bryophytes) and are thought to have appeared about 500 million years ago. They were followed by liverworts (also bryophytes) and primitive vascular plants, the pterophytes, from which modern ferns are derived. The life cycle of bryophytes and pterophytes is characterized by the alternation of generations. The completion of the life cycle requires water, as the male gametes must swim to the female gametes. The male gametophyte releases sperm, which must swim—propelled by their flagella—to reach and fertilize the female gamete or egg. After fertilization, the zygote matures and grows into a sporophyte, which in turn will form sporangia, or "spore vessels,” in which mother cells undergo meiosis and produce haploid spores. The release of spores in a suitable environment will lead to germination and a new generation of gametophytes.

The Evolution of Seed Plants

In seed plants, the evolutionary trend led to a dominant sporophyte generation, in which the larger and more ecologically significant generation for a species is the diploid plant. At the same time, the trend led to a reduction in the size of the gametophyte, from a conspicuous structure to a microscopic cluster of cells enclosed in the tissues of the sporophyte. Lower vascular plants, such as club mosses and ferns, are mostly homosporous (produce only one type of spore). In contrast, all seed plants, or spermatophytes, are heterosporous, forming two types of spores: megaspores (female) and microspores (male). Megaspores develop into female gametophytes that produce eggs, and microspores mature into male gametophytes that generate sperm. Because the gametophytes mature within the spores, they are not free-living, as are the gametophytes of other seedless vascular plants. Heterosporous seedless plants are seen as the evolutionary forerunners of seed plants.

Seeds and pollen—two adaptations to drought—distinguish seed plants from other (seedless) vascular plants. Both adaptations were critical to the colonization of land. Fossils place the earliest distinct seed plants at about 350 million years ago. The earliest reliable record of gymnosperms dates their appearance to the Carboniferous period (359–299 million years ago). Gymnosperms were preceded by the progymnosperms (“first naked seed plants”). This was a transitional group of plants that superficially resembled conifers (“cone bearers”) because they produced wood from the secondary growth of the vascular tissues however, they still reproduced like ferns, releasing spores to the environment. In the Mesozoic era (251–65.5 million years ago), gymnosperms dominated the landscape. Angiosperms took over by the middle of the Cretaceous period (145.5–65.5 million years ago) in the late Mesozoic era, and have since become the most abundant plant group in most terrestrial biomes.

The two innovative structures of pollen and seed allowed seed plants to break their dependence on water for reproduction and development of the embryo, and to conquer dry land. The pollen grains carry the male gametes of the plant. The small haploid (1n) cells are encased in a protective coat that prevents desiccation (drying out) and mechanical damage. Pollen can travel far from the sporophyte that bore it, spreading the plant’s genes and avoiding competition with other plants. The seed offers the embryo protection, nourishment and a mechanism to maintain dormancy for tens or even thousands of years, allowing it to survive in a harsh environment and ensuring germination when growth conditions are optimal. Seeds allow plants to disperse the next generation through both space and time. With such evolutionary advantages, seed plants have become the most successful and familiar group of plants.

Gymnosperms

Gymnosperms (“naked seed”) are a diverse group of seed plants and are paraphyletic. Paraphyletic groups do not include descendants of a single common ancestor. Gymnosperm characteristics include naked seeds, separate female and male gametes, pollination by wind, and tracheids, which transport water and solutes in the vascular system.

Life Cycle of a Conifer

Pine trees are conifers and carry both male and female sporophylls on the same plant. Like all gymnosperms, pines are heterosporous and produce male microspores and female megaspores. In the male cones, or staminate cones, the microsporocytes give rise to microspores by meiosis. The microspores then develop into pollen grains. Each pollen grain contains two cells: one generative cell that will divide into two sperm, and a second cell that will become the pollen tube cell. In the spring, pine trees release large amounts of yellow pollen, which is carried by the wind. Some gametophytes will land on a female cone. The pollen tube grows from the pollen grain slowly, and the generative cell in the pollen grain divides into two sperm cells by mitosis. One of the sperm cells will finally unite its haploid nucleus with the haploid nucleus of an egg cell in the process of fertilization.

Female cones , or ovulate cones, contain two ovules per scale. One megasporocyte undergoes meiosis in each ovule. Only a single surviving haploid cell will develop into a female multicellular gametophyte that encloses an egg. On fertilization, the zygote will give rise to the embryo, which is enclosed in a seed coat of tissue from the parent plant. Fertilization and seed development is a long process in pine trees—it may take up to two years after pollination. The seed that is formed contains three generations of tissues: the seed coat that originates from the parent plant tissue, the female gametophyte that will provide nutrients, and the embryo itself. Figure 14.19 illustrates the life cycle of a conifer.


Xenoturbellida: The fourth deuterostome phylum and the diet of worms

Since the discovery of the marine worm Xenoturbella bocki in 1915 by Sixten Bock and its first published description by Einar Westblad (Westblad, 1949 , Arkiv Zoologi 1:3–29), Xenoturbella was generally allied to the turbellarian flatworms, perhaps most closely to acoelomorphs. In 1997, however, analyses of ribosomal DNA (Norén and Jondelius, 1997, Nature 390:31–32) and developing oocytes (Israelsson, 1997, Nature 390:32) [and, subsequently, embryos (Israelsson, 1999, Proc R Soc Lond B 266:835–841)] recovered from Xenoturbella specimens led to the surprising conclusion that it was in fact a highly degenerate bivalve mollusc. Bourlat et al. showed in 2003 that this result was due to contamination from bivalves in its diet (Bourlat et al., 2003 , Nature 424:925–928). Our analyses showed Xenoturbella is a deuterostome, related to the Ambulacraria (echinoderms and hemichordates). Subsequent work has shown that Xenoturbellida is a separate lineage from the Ambulacraria and therefore constitutes the fourth deuterostome phylum (Bourlat et al., 2006 , Nature 444:85–88). I consider this phylogenetic position in the light of what is known of its genetics, morphology, and ontogeny. I examine what this phylogenetic position for Xenoturbella can tell us about its own evolution and what light this might shine on the common ancestor of the deuterostomes and hence on the origins of the chordates. genesis 46:580–586, 2008. © 2008 Wiley-Liss, Inc.


Cambrian cinctan echinoderms shed light on feeding in the ancestral deuterostome

Reconstructing the feeding mode of the latest common ancestor of deuterostomes is key to elucidating the early evolution of feeding in chordates and allied phyla however, it is debated whether the ancestral deuterostome was a tentaculate feeder or a pharyngeal filter feeder. To address this, we evaluated the hydrodynamics of feeding in a group of fossil stem-group echinoderms (cinctans) using computational fluid dynamics. We simulated water flow past three-dimensional digital models of a Cambrian fossil cinctan in a range of possible life positions, adopting both passive tentacular feeding and active pharyngeal filter feeding. The results demonstrate that an orientation with the mouth facing downstream of the current was optimal for drag and lift reduction. Moreover, they show that there was almost no flow to the mouth and associated marginal groove under simulations of passive feeding, whereas considerable flow towards the animal was observed for active feeding, which would have enhanced the transport of suspended particles to the mouth. This strongly suggests that cinctans were active pharyngeal filter feeders, like modern enteropneust hemichordates and urochordates, indicating that the ancestral deuterostome employed a similar feeding strategy.

1. Introduction

Deuterostomes are one of the three major clades of bilaterian animals. Molecular phylogenetics has helped resolve the relationships of the main deuterostome phyla (chordates, echinoderms and hemichordates) [1–3], but despite extensive study of their anatomy, development and phylogeny for over a century, important aspects of the early evolutionary history of deuterostomes remain unclear [4]. Feeding is one such outstanding issue it was long speculated that the ancestral deuterostome had tentacles for collecting food from the water column, like modern crinoids and pterobranch hemichordates [5–7], but more recently it has been proposed that it had a pharynx with gill slits for actively generating feeding currents, similar to enteropneust hemichordates, urochordates, cephalochordates and larval lampreys [8–10]. Distinguishing between these competing hypotheses is problematic because it is disputed whether the latest common ancestor of deuterostomes had a pterobranch-like body plan (with tentacular feeding), or an enteropneust-like body plan (with pharyngeal filter feeding) [4].

The fossil record provides an alternative means of differentiating these two hypotheses through the inference of feeding modes in the earliest fossil forms, and could thus inform on the ancestral feeding strategy of deuterostomes. Although the early record of most deuterostome phyla is patchy and incomplete [4], echinoderms possess a rich record dating back to the Cambrian [11,12] because a mineralized skeleton was among their first derived traits [13]. Several groups of pre-radiate fossil stem-group echinoderms (Ctenoimbricata, ctenocystoids and cinctans) are especially important, as they document the earliest steps in the assembly of the echinoderm body plan and retain plesiomorphic characters of the ancestral deuterostome [14–16]. Cinctans are the best understood of these groups in terms of their anatomy and functional morphology, and so have the greatest potential for elucidating deuterostome evolution however, their mode of feeding is controversial. It is widely accepted that cinctans were sessile epibenthic suspension feeders with an anterolateral mouth and one or a pair of marginal grooves [7,14,17–20], but it is debated whether they were passive suspension feeders with a system of tentacles, analogous to crinoids [19,20], or active pharyngeal filter feeders, similar to urochordates [14,21].

In order to evaluate competing hypotheses of cinctan feeding mode, we quantitatively analysed the functional performance of a Cambrian fossil cinctan. Using three-dimensional computational fluid dynamics (CFD), we simulated flow past a digital reconstruction of the fossil in a range of different positions relative to the current direction and the sediment–water interface, approximating both hypothesized feeding scenarios. The results provide new insights into the hydrodynamics of feeding in cinctans, with implications for the plesiomorphic mode of feeding in deuterostomes.

2. Material and methods

(a) Fossil specimen

The holotype of the cinctan Protocinctus mansillaensis (MPZ 2004/170 Museo Paleontológico de la Universidad de Zaragoza, Spain) was selected for use in CFD simulations owing to its exceptional three-dimensional preservation as recrystallized calcite. This species comes from the Mansilla Formation of Purujosa, northeast Spain, which is early middle Cambrian (Cambrian Series 3, Stage 5) in age (approx. 510 Ma) and is characterized by purple to reddish nodular limestones and shales, indicative of a shoreface to offshore depositional setting. Like all cinctans, Protocinctus has a flattened, asymmetrical body (theca) and a rigid posterior appendage. A circular mouth is located on the anterior right side of the theca a larger exhalant aperture (the porta) is situated at the anterior midline of the theca, covered by a movable plate (the operculum). Protocinctus is also characterized by an elongate, oval-shaped theca, a single left marginal groove and a weakly developed ventral swelling at the anterior (figure 1a).

Figure 1. Protocinctus mansillaensis. (a) Original fossil specimen (ventral view). (b) Digital restoration with the operculum closed (anterolateral view). (c) Digital restoration with the operculum open (anterolateral view). (d) Digital restoration with the operculum closed (lateral view). (Online version in colour.)

(b) X-ray micro-tomography

The fossil was scanned with a Phoenix v|tome|x s system and digitally reconstructed using the SPIERS software suite [22]. See Rahman & Zamora [23] for details. A ZIP archive containing the digital reconstruction in VAXML format can be downloaded from Dryad (doi:10.5061/dryad.g4n5m).

(c) Digital restoration

In order to restore the poorly preserved upper surface of the studied specimen, the dorsal integument and the operculum were virtually extrapolated in SPIERS with a closed spline (using other specimens in which the upper surface is better preserved as a reference). The operculum was restored in two hypothetical life positions: (i) ‘closed’, with the porta entirely covered by the operculum (figure 1b) and (ii) ‘open’, with the operculum raised above the porta (figure 1c). These reconstructions were then optimized with a low smoothing value to remove noise, and converted into NURBS surfaces using G eomagic S tudio (www.geomagic.com) (models can be downloaded from Dryad: doi:10.5061/dryad.g4n5m).

(d) Computational fluid dynamics simulations

CFD simulations of water flow around Protocinctus were performed using COMSOL M ultiphysics (www.uk.comsol.com). The computational domain consisted of a three-dimensional volume above a flat solid boundary (85 mm in length and 17.5 mm in diameter), on which the Protocinctus reconstruction (23 mm in length and 10 mm in width) was centrally fixed (electronic supplementary material, figure S1a). Flow was simulated through this domain with an initially uniform inflow velocity at the upstream end and an outflow boundary condition (zero pressure gradient across the boundary) at the downstream end. Slip conditions (zero stress across the boundary) were used for the domain sides and top, with no-slip conditions (zero velocity relative to the boundary) for the solid surfaces of the reconstruction and the underlying base. The flow domain was a semi-cylinder and was sufficiently large that the boundary conditions did not influence the flow. The domain was meshed using free tetrahedral elements (electronic supplementary material, figure S1b), with mesh resolution fully tested to ensure grid scale independence for the simulation results (electronic supplementary material, sensitivity analyses).

A total of 100 simulations were undertaken, using a range of input parameters (electronic supplementary material, table S1). In all cases, three-dimensional, incompressible (constant density) flow of water was simulated, with the Protocinctus reconstruction held stationary. Ambient flow velocities of 0.05, 0.1 and 0.2 m s −1 (Reynolds numbers of 525–925, 1050–1850 and 2100–3700, respectively width of the specimen in the flow taken as the characteristic dimension) were simulated to approximate typical near-bottom currents in modern shoreface to offshore environments [24]. A stationary solver was used to compute the steady-state flow patterns and a laminar flow model was used to solve the Navier–Stokes equations for conservation of momentum and the continuity equation for conservation of mass. The effects of varying the solver type and flow model were examined for the higher Reynolds number flows (electronic supplementary material, sensitivity analyses). In addition, experimental studies of flow around a three-dimensional printed model of Protocinctus were carried out in a flume tank for comparison with the computer simulations (electronic supplementary material, flume tank experiments and figure S2).

Three different feeding scenarios were simulated: (i) passive tentacular feeding using the closed Protocinctus reconstruction with the mouth cross-section allowing flow to pass through (outflow boundary) (ii) the inhalant current of active pharyngeal filter feeding using the closed Protocinctus reconstruction with flow velocity through the mouth cross-section given a normal outflow velocity of 0.015 m s −1 and (iii) the exhalant current of active pharyngeal filter feeding using the open Protocinctus reconstruction with flow velocity through the operculum cross-section given a normal inflow velocity of 0.04 m s −1 . The inhalant and exhalant velocities of pharyngeal filter feeding were based on analogy with the extant urochordate Styela clava [25].

To explore the hydrodynamic consequences of different life positions, all of the above simulations were performed with the Protocinctus reconstruction oriented at 0°, 45°, 90°, 135° and 180° to the current, and with the ventral swelling positioned either below (equivalent to burial within the sediment) or on top of (equivalent to resting on the sediment) the lower boundary of the computational domain. The results were visualized as two-dimensional cross sections of flow velocity magnitude with flow vectors (arrows) and streamlines. Drag and lift forces and their coefficients (projected frontal area taken as the reference area) were calculated to quantify flow around the digital reconstructions.

3. Results

The results of the CFD simulations show that the overall characteristics of the flow around the Protocinctus reconstruction conformed to expectations for boundary layer and wake development. In all cases, the velocity decreased rapidly immediately upstream of the Protocinctus reconstruction (figure 2 electronic supplementary material, figures S3–S8) and a distinctive wake (elongate, low-velocity flow region, typically with an asymmetrical vortex) was formed immediately downstream. The size and shape of the wake varied depending on the orientation of the reconstruction to the current, but were not significantly affected by the simulated feeding scenario, or the placement of the reconstruction in relation to the lower boundary of the domain (figure 2 electronic supplementary material, figures S3–S8). A characteristic boundary layer, shown by a rapid drop in velocity as the flow approached the bottom of the domain, was well developed in all the simulations. The thickness of the boundary layer was roughly equal to the height of the Protocinctus reconstruction in both positions relative to the underlying base (figure 2).

Figure 2. Results of the CFD simulations with Protocinctus oriented at 180° to the current, visualized as two-dimensional plots (horizontal and vertical cross sections) of flow velocity magnitude (false-colour scale different for each ambient flow velocity) with flow vectors (arrows length of arrows proportional to the natural logarithm of the flow velocity magnitude) and streamlines. (a–f) Simulations of passive tentacular feeding. (g–l) Simulations of the inhalant current of pharyngeal filter feeding. (m–r) Simulations of the exhalant current of pharyngeal filter feeding. The mouth is indicated by an asterisk (*) symbol and the porta is indicated by a plus (+) symbol. The ambient flow is from left to right. (Online version in colour.)

Distinctly different flow patterns were associated with different feeding scenarios. Flow vectors and streamlines indicate that the velocity of the flow into the mouth was greatest in the simulations of the inhalant current generated by pharyngeal filter feeding (figure 2g–l electronic supplementary material, figures S5 and S6). This was most pronounced when the Protocinctus reconstruction was oriented at 180° to the current. Conversely, in the simulations where there was no inhalant current, flow into the mouth was generally much weaker (figure 2af, mr electronic supplementary material, figures S3, S4, S7 and S8). Flow to the marginal groove was very low for all the simulated feeding modes (electronic supplementary material, figure S9).

In the simulations of the exhalant current produced by pharyngeal filter feeding, a jet of high-velocity flow passed out of the porta, intruding into the ambient flow or the wake, depending on the orientation of the reconstruction (figure 2mr electronic supplementary material, figures S7 and S8). When the Protocinctus reconstruction was oriented at 0° to the current, this jet directly opposed the ambient flow direction (electronic supplementary material, figures S7a–c and S8a–c), whereas with the reconstruction oriented at 180° to the current, it flowed in the same direction as the ambient flow, contributing to the wake (figure 2m–r).

Consistent with theoretical expectations, the drag force exerted by the reconstruction on the fluid flow increased as the ambient velocity increased, whereas the drag coefficient decreased. The lift force also increased with increasing ambient velocity. The orientation of the reconstruction strongly influenced both the drag and lift forces and the lift coefficient, which were greatest when the reconstructions were oriented at 45°, 90° or 135° to the current. The reconstruction position relative to the domain bottom was likewise important, with the drag and lift forces and the drag coefficient higher when the ventral swelling was positioned on top of the lower boundary of the domain (figure 3 electronic supplementary material, figures S10, S11 and tables S2, S3).

Figure 3. Drag and lift forces for the CFD simulations. (a–c) Simulations of passive tentacular feeding. (d–f) Simulations of the inhalant current of pharyngeal filter feeding. (g–i) Simulations of the exhalant current of pharyngeal filter feeding. Red symbols indicate drag force, blue symbols indicate lift force. Triangles indicate results of simulations of the ventral swelling resting on top of the sediment surface, circles indicate results of simulations of the ventral swelling buried in the sediment. (Online version in colour.)

The results of the simulations were not greatly influenced by varying the mesh size, solver or flow type, with all these analyses producing very similar flow structures, drag and lift (electronic supplementary material, figures S12–S14 and table S4). Moreover, comparisons between the experimental studies and the computer simulations showed that both approaches obtained similar downstream current velocities (electronic supplementary material, figure S15).

4. Discussion

The CFD simulations indicate that orientation had a marked effect on the amount of drag generated by Protocinctus, with the largest wake size and highest drag force occurring when the reconstruction was oriented at 45°, 90° or 135° to the current (figure 3 electronic supplementary material, figures S3–S8 and table S2). The lift force and coefficient were also greatest when the reconstruction was non-parallel to the current (figure 3 electronic supplementary material figure S11 and table S3). Drag and lift can be detrimental to epibenthic organisms, making it harder to maintain posture and even dislodging or injuring animals [26,27]. While some suspension feeders seek to increase drag to aid feeding [26], this was almost certainly not the case for Protocinctus, which exhibits a streamlined profile (figure 1) that is clearly adapted to reduce drag parallel to the flow direction. Therefore, it seems most probable (on functional grounds) that Protocinctus was preferentially oriented parallel to the current in life, minimizing both drag and lift. Simulations with the reconstruction facing upstream and downstream produced similar amounts of drag (figure 3 electronic supplementary material figure S10 and table S2). However, the lift was substantially greater when the reconstruction faced upstream (figure 3 electronic supplementary material figure S11 and table S3). Moreover, the simulations of the exhalant current clearly show that the jet of exhalant flow out of the porta would have been transported to the mouth by the ambient flow if the reconstruction faced into the current (electronic supplementary material, figures S7a–c and S8a–c). Because the porta is interpreted as an exhalant opening under both passive [19,20] and active [14,21] feeding scenarios, an upstream orientation would have led to fouling of the mouth and associated marginal groove in either mode of feeding. Consequently, it can be inferred that cinctans were oriented downstream in life, and this agrees with previous interpretations of cinctan functional morphology [7,19,21] and a qualitative flume study [18], which suggested that an orientation with the mouth facing away from the prevailing current would have enhanced feeding and/or stability.

The flow structure did not vary appreciably according to the position of Protocinctus relative to the sediment–water interface, but the drag and lift forces were higher in the simulations of the ventral swelling resting on top of the sediment surface (figure 3 electronic supplementary material, tables S2 and S3). This suggests that a position with the ventral swelling buried was optimal for reducing drag and lift, and might also have been beneficial for anchoring the animal to the seafloor [17,28]. Regardless of the placement of the ventral swelling, however, Protocinctus would always have been situated in the low-velocity boundary layer, with the mouth and marginal groove close to the sediment surface (figure 2). This position has implications for the interpretation of the animal's mode of feeding. The simulations of passive feeding with Protocinctus in a downstream orientation demonstrate that there was almost no flow to the mouth and adjacent marginal groove (figure 2a–f electronic supplementary material, figure S9), indicating that the transport of suspended particles to the animal would have been extremely limited. Nutrient flux is known to be very low within the boundary layer [29], and modern passive suspension feeders typically possess specialized food-capturing structures, such as fans, nets or tentacles, which are elevated above this zone, where there are higher rates of flow and nutrient flux, to facilitate feeding [26,30]. There is no evidence of such morphological adaptations in cinctans, which are characterized by a flattened body with recumbent feeding structures (mouth and marginal groove). Thus, if cinctans faced downstream (as argued above) and relied on external flows alone, they would have had access to a very limited supply of nutrients, which was probably insufficient for passive tentaculate feeding.

The CFD simulations provide better support for an active pharyngeal filter feeding mode of life. The inhalant current generated by Protocinctus channelled considerable flow towards the animal (figure 2g–l), which would have enhanced the transport of suspended particles into the mouth. Furthermore, simulations of active feeding with Protocinctus facing downstream show that the exhalant jet ejected from the porta travelled above any recirculating flow in the wake close to the mouth and marginal groove, avoiding potential contamination of feeding currents (figure 2m–r). The same pattern is documented in extant pharyngeal filter feeders, such as urochordates, which are capable of generating powerful exhalant flows that carry wastewater beyond the mouth [25,26]. Consequently, simulations of both inhalant (figure 2g–l) and exhalant (figure 2m–r) currents are compatible with pharyngeal filter feeding, and this agrees with studies of cinctans that suggested such a feeding mode based on the functional morphology of the porta–operculum complex and detailed comparisons with urochordates [14,18,21].

Our findings are broadly in agreement with previous interpretations of the earliest fossil stem-group echinoderms (Ctenoimbricata, ctenocystoids and cinctans) as pharyngeal filter feeders [14–16], and argue against their interpretation as passive tentaculate feeders [19,20]. Among modern deuterostomes, active suspension feeding with pharyngeal gill slits is documented in enteropneust hemichordates, urochordates, cephalochordates and larval lampreys, while suspension feeding with tentacles characterizes crinoids and pterobranch hemichordates. Owing to their position close to the base of echinoderm phylogeny, the inference of pharyngeal filter feeding in cinctans allows us to extend this feeding mode back to the latest common ancestor of all deuterostomes (figure 4). This provides strong support for the hypothesis that the ancestral deuterostome fed through pharyngeal filtering [8–10], indicating that a pharynx with gill slits is in all likelihood a deuterostome symplesiomorphy and that the tentacular feeding systems of echinoderms and pterobranchs are probably not homologous.

Figure 4. Phylogeny showing feeding modes of extant and extinct deuterostomes (cinctans marked with a †). Blue boxes indicate tentaculate suspension feeding, red boxes indicate pharyngeal filter feeding and green boxes indicate multiple feeding modes. (Online version in colour.)


Evolution of echinoderms may not have required modification of the ancestral deuterostome HOX gene cluster: first report of PG4 and PG5 Hox orthologues in echinoderms

Is the extreme derivation of the echinoderm body plan reflected in a derived echinoderm Hox genotype? Building on previous work, we exploited the sequence conservation of the homeobox to isolate putative orthologues of several Hox genes from two asteroid echinoderms. The 5-peptide motif (LPNTK) diagnostic of PG4 Hox genes was identified immediately downstream of one of the partial homeodomains from Patiriella exigua. This constitutes the first unequivocal report of a PG4 Hox gene orthologue from an echinoderm. Subsequent screenings identified genes of both PG4 and PG4/5 in Asterias rubens. Although in echinoids only a single gene (PG4/5) occupies these two contiguous cluster positions, we conclude that the ancestral echinoderm must have had the complete deuterostome suite of medial Hox genes, including orthologues of both PG4 and PG4/5 (= PG5). The reported absence of PG4 in the HOX cluster of echinoids is therefore a derived state, and the ancestral echinoderm probably had a HOX cluster not dissimilar to that of other deuterostomes. Modification of the ancestral deuterostome Hox genotype may not have been required for evolution of the highly derived echinoderm body plan.

This is a preview of subscription content, access via your institution.


Cell cultures from marine invertebrates: obstacles, new approaches and recent improvements

The establishment of cell lines from marine invertebrates has been encountered with obstacles. Contrary to insects and arachnids where the development of a variety of cell lines has become routine+ there is no single established cell line from marine invertebrates. This review examines the activity in the field of marine invertebrate cell cultures within the last decade (1988–1998). During this period, attempts (90 peer reviewed studies in addition to many other abstracts, chapters in books, symposia presentations and reports) were limited to a few species within only six phyla (Porifera, Cnidaria, Crustacea, Mollusca, Echinodermata, Urochordata: in addition to freshwater/terrestrial annelids and platyhelminths). These studies which are summarized here+ on one hand indicated ubiquitous problems and on the other, unique characterizations to each phylum studied. Only one-third of the studies revealed cultures of 1 month or longer but most of these were long-term cultures found or suspiciously considered to be contaminated by other unicellular eukaryotic organisms, mainly by thraustochytrids. Three unique approaches/obstacles for marine invertebrate cell cultures (source of cell, cryopreservation and eukaryotic contaminants) are further discussed. The overall impact of recent improvements and developed protocols raises the suggestion for testing different, novel routes in the establishment of cell cultures from marine invertebrates.


We also thank Mervyn Greaves (Cambridge) for assistance with the trace element analyses.

Addadi, L., Joester, D., Nudelman, F., and Weiner, S. (2006). Mollusc shell formation: a source of new concepts for understanding biomineralization processes. Chem. Eur. J. 12, 980�. doi: 10.1002/chem.200500980

Addadi, L., Raz, S., and Weiner, S. (2003). Taking advantage of disorder: amorphous calcium carbonate and its roles in biomineralization. Adv. Mater. 15, 959�. doi: 10.1002/adma.200300381

Allen, K. A., Hönisch, B., Eggins, S. M., Haynes, L. L., Rosenthal, Y., and Yu, J. (2016). Trace element proxies for surface ocean conditions: a synthesis of culture calibrations with planktic foraminifera. Geochim. Cosmochim. Acta 193, 197�. doi: 10.1016/j.gca.2016.08.015

Allison, N., Finch, A. A., Sutton, S. R., and Newville, M. (2001). Strontium heterogeneity and speciation in coral aragonite: implications for the strontium paleothermometer. Geochim. Cosmochim. Acta 65, 2669�. doi: 10.1016/S0016-7037(01)00628-7

Anderson, D., and Burnham, K. (2004). Model Selection and Multi-Model Inference, 2nd Edn, Vol. 63. New York, NY: Springer-Verlag, 10.

Barker, S., Greaves, M., and Elderfield, H. (2003). A study of cleaning procedures used for foraminiferal Mg/Ca paleothermometry. Geochem. Geophys. Geosyst. 4:8407. doi: 10.1029/2003GC000559

Beniash, E., Aizenberg, J., Addadi, L., and Weiner, S. (1997). Amorphous calcium carbonate transforms into calcite during sea urchin larval spicule growth. Proc. R. S. B Biol. Sci. 264, 461�.

Beretta, L., and Santaniello, A. (2016). Nearest neighbor imputation algorithms: a critical evaluation. BMC Med. Inform. Decis. Mak. 16(Suppl 3):74. doi: 10.1186/s12911-016-0318-z

Borowitzka, M. A., and Larkum, A. W. D. (1987). Calcification in algae: mechanisms and the role of metabolism. Crit. Rev. Plant Sci. 6, 1�. doi: 10.1080/07352688709382246

Boyle, E. A., Huested, S. S., and Jones, S. P. (1981). On the distribution of copper, nickel, and cadmium in the surface waters of the North Atlantic and North Pacific Ocean. J. Geophys. Res. 86, 8048�. doi: 10.1029/jc086ic09p08048

Brand, U., and Veizer, J. (1980). Chemical diagenesis of a multicomponent carbonate system – 1: trace Elements. J. Sediment. Petrol. 50, 1219�. doi: 10.1306/212f7df6-2b24-11d7-8648000102c1865d

Branson, O. (2018). 𠇋oron incorporation into marine CaCO3,” in Advances in Isotope Geochemistry, eds H. Marschall and G. Foster (Cham: Springer), 71�. doi: 10.1007/978-3-319-64666-4_4

Branson, O., Redfern, S. A. T., Elmore, A. C., Read, E., Valencia, S., and Elderfield, H. (2018). The distribution and coordination of trace elements in Krithe ostracods and their implications for paleothermometry. Geochim. Cosmochim. Acta 236, 230�. doi: 10.1016/j.gca.2017.12.005

Brecevic, L., and Nielsen, A. E. (1989). Solubility of amorphous calcium carbonate. J. Cryst. Growth 98, 504�.

Broecker, W. S., and Peng, T. H. (1983). Tracers in the SEA. Palisades, NY, Eldigio Press, 23�.

Bruland, K. (1983). Trace Elements in Seawater. Chemical Oceanography, 2nd Edn, Vol. 8, eds J. P. Riley and R. Chester (London: Academic).

Burdett, J. W., Arthur, M. A., and Richardson, M. (1989). A Neogene seawater sulfur isotope age curve from calcareous pelagic microfossils. Earth Planet. Sci. Lett. 94, 189�. doi: 10.1016/0012-821X(89)90138-6

Canty, A., and Ripley, B. (2020). boot: Bootstrap R (S-Plus) Functions. R package version 1.3-25.

Chan, V. B. S., Toyofuku, T., Wetzel, G., Saraf, L., Thiyagarajan, V., and Mount, A. S. (2015a). Direct deposition of crystalline aragonite in the controlled biomineralization of the calcareous tubeworm. Front. Mar. Sci. 2:97. doi: 10.3389/fmars.2015.00097

Chan, V. B. S., Vinn, O., Li, C., Lu, X., Kudryavtsev, A. B., Schopf, J. W., and Thiyagarajan, V. (2015b). Evidence of compositional and ultrastructural shifts during the development of calcareous tubes in the biofouling tubeworm, Hydroides elegans. Journal of Structural Biology, 189(3), 230�. doi: 10.1016/j.jsb.2015.01.004

Chavé, K. E. (1954). Aspects of the biogeochemistry of magnesium 1. Calcareous marine organisms. J. Geol. 62, 266�. doi: 10.1086/626162

Cohen, A. L., and McConnaughey, T. A. (2003). Geochemical perspectives on coral mineralization. Rev. Mineral. Geochem. 54, 151�. doi: 10.2113/0540151

Constantz, B. R. (1986). Coral skeleton construction: a physicochemically dominated process. Palaios 1, 152�. doi: 10.2307/3514508

Constantz, B. R., and Meike, A. (1989). “Origin, evolution, and modern aspects of biomineralization in plants and animals,” in Origin, Evolution, and Modern Aspects of Biomineralization in Plants and Animals, ed. R. E. Crick (New York, NY: Springer Science+Business Media), 201�. doi: 10.1007/978-1-4757-6114-6

Cornwall, C. E., Comeau, S., and McCulloch, M. T. (2017). Coralline algae elevate pH at the site of calcification under ocean acidification. Glob. Change Biol. 23, 4245�. doi: 10.1111/gcb.13673

Cuif, J.-P., Dauphin, Y., and Sorauf, J. E. (2013). Biominerals and Fossils Through Time. Journal of Chemical Information and Modeling, Vol. 53. Cambridge: Cambridge University Press, doi: 10.1017/CBO9781107415324.004

Dang, H., Wang, T., Qiao, P., Bassinot, F., and Jian, Z. (2019). The B/Ca and Cd/Ca of a subsurface-dwelling foraminifera Pulleniatina obliquiloculata in the tropical Indo-Pacific Ocean: implications for the subsurface carbonate chemistry estimation. Acta Oceanol. Sin. 38, 138�. doi: 10.1007/s13131-019-1406-6

Davison, A. C., and Hinkley, D. V. (1997). Bootstrap Methods and Their Applications. Cambridge: Cambridge University Press.

Dawber, C. F., and Tripati, A. (2012). Relationships between bottom water carbonate saturation and element/Ca ratios in coretop samples of the benthic foraminifera Oridorsalis umbonatus. Biogeosciences 9, 3029�. doi: 10.5194/bg-9-3029-2012

De Choudens-Sánchez, V., and González, L. A. (2009). Calcite and aragonite precipitation under controlled instantaneous supersaturation: elucidating the role of CACO 3 saturation state and Mg/Ca ratio on calcium carbonate polymorphism. J. Sediment. Res. 79, 363�. doi: 10.2110/jsr.2009.043

de Villiers, S., Greaves, M., and Elderfield, H. (2002). An intensity ratio calibration method for the accurate determination of Mg/Ca and Sr/Ca of marine carbonates by ICP-AES. Geochem. Geophys. Geosyst. 3, 623�. doi: 10.1029/2001gc000169

De Yoreo, J. J., Gilbert, P. U. P. A., Sommerdijk, N. A. J. M., Penn, R. L., Whitelam, S., Joester, D., et al. (2015). Crystallization by particle attachment in synthetic, biogenic, and geologic environments. Science 349:aaa6760. doi: 10.1126/science.aaa6760

DeCarlo, T. M., Gaetani, G. A., Holcomb, M., and Cohen, A. L. (2015). Experimental determination of factors controlling U/Ca of aragonite precipitated from seawater: implications for interpreting coral skeleton. Geochim. Cosmochim. Acta 162, 151�. doi: 10.1016/j.gca.2015.04.016

Delaney, M. L., and Boyle, E. A. (1985). Li, Sr, Mg, and Na in foraminiferal calcite shells from laboratory culture, sediment traps, and sediment cores. Deep Sea Res. Part B Oceanogr. Lit. Rev. 32:1025. doi: 10.1016/0198-0254(85)93853-1

Delaney, M. L., Popp, B. N., Lepzelter, C. G., and Anderson, T. F. (1989). Lithium-to-calcium ratios in modern Cenozoic, and Paleosoic articulate brachiopod shells. Paleoceanography 4, 681�.

Dellinger, M., West, A. J., Paris, G., Adkins, J. F., Pogge von Strandmann, P. A. E., Ullmann, C. V., et al. (2018). The Li isotope composition of marine biogenic carbonates: patterns and mechanisms. Geochim. Cosmochim. Acta 236, 315�. doi: 10.1016/j.gca.2018.03.014

DePaolo, D. J. (2011). Surface kinetic model for isotopic and trace element fractionation during precipitation of calcite from aqueous solutions. Geochim. Cosmochim. Acta 416, 67�. doi: 10.1016/j.gca.2010.11.020

Dillaman, R., Hequembourg, S., and Gay, M. (2005). Early pattern of calcification in the dorsal carapace of the blue crab, Callinectes sapidus. J. Morphol. 263, 356�. doi: 10.1002/jmor.10311

Donald, H. K., Ries, J. B., Stewart, J. A., Fowell, S. E., and Foster, G. L. (2017). Boron isotope sensitivity to seawater pH change in a species of Neogoniolithon coralline red alga. Geochim. Cosmochim. Acta 217, 240�. doi: 10.1016/j.gca.2017.08.021

Dove, P. M. (2010). The rise of skeletal biominerals. Elements 6, 37�. doi: 10.2113/gselements.6.1.37

Drake, J. L., Mass, T., Stolarski, J., Von Euw, S., van de Schootbrugge, B., and Falkowski, P. G. (2020). How corals made rocks through the ages. Glob. Change Biol. 26, 31�. doi: 10.1111/gcb.14912

Elderfield, H., and Rickaby, R. E. M. (2000). Oceanic Cd/P ratio and nutrient utilization in the glacial Southern Ocean. Nature 405, 305�. doi: 10.1038/35012507

Elderfield, H., Bertram, C. J., and Erez, J. (1996). A biomineralization model for the incorporation of trace elements into foraminiferal calcium carbonate. Earth Planet. Sci. Lett. 142, 409�. doi: 10.1016/0012-821x(96)00105-7

Endrizzi, F., and Rao, L. (2014). Chemical speciation of uranium(VI) in marine environments: complexation of calcium and magne- sium ions with [(UO2)(CO3)3]4? and the effect on the extraction of uranium from seawater. Chem. Eur. J. 20, 14499�.

Erez, J. (2003). The source of ions for biomineralization in foraminifera and their implications for paleoceanographic proxies. Rev. Mineral. Geochem. 54, 115�. doi: 10.2113/0540115

Evans, D., Gray, W. R., Rae, J. W. B., Greenop, R., Webb, P. B., Penkman, K., et al. (2020). Trace and major element incorporation into amorphous calcium carbonate (ACC) precipitated from seawater. Geochim. Cosmochim. Acta 290, 293�. doi: 10.1016/j.gca.2020.08.034

Farmer, J. R., Branson, O., Uchikawa, J., Penman, D. E., Hönisch, B., and Zeebe, R. E. (2019). Boric acid and borate incorporation in inorganic calcite inferred from B/Ca, boron isotopes and surface kinetic modeling. Geochim. Cosmochim. Acta 244, 229�. doi: 10.1016/j.gca.2018.10.008

Feng, J., Lee, J. Y., Reeder, R. J., and Phillips, B. L. (2006). Observation of bicarbonate in calcite by NMR spectroscopy. Am. Mineral. 91, 957�. doi: 10.2138/am.2006.2206

Finch, A. A., and Allison, N. (2008). Mg structural state in coral aragonite and implications for the paleoenvironmental proxy. Geophys. Res. Lett. 35:L08704. doi: 10.1029/2008GL033543

Frieder, C. A., Gonzalez, J. P., and Levin, L. A. (2014). Uranium in larval shells as a barometer of molluscan ocean acidification exposure. Environ. Sci. Technol. 48, 6401�. doi: 10.1021/es500514j

Gabitov, R. I., Sadekov, A., and Leinweber, A. (2014). Crystal growth rate effect on Mg/Ca and Sr/Ca partitioning between calcite and fluid: an in situ approach. Chem. Geol. 367, 70�. doi: 10.1016/j.chemgeo.2013.12.019

Gabitov, R. I., Schmitt, A. K., Rosner, M., McKeegan, K. D., Gaetani, G. A., Cohen, A. L., et al. (2011). In situ δ 7 Li, Li/Ca, and Mg/Ca analyses of synthetic aragonites. Geochem. Geophys. Geosystems 12, 1�. doi: 10.1029/2010GC003322

Gabitov, R., Sadekov, A., Yapaskurt, V., Borrelli, C., Bychkov, A., Sabourin, K., et al. (2019). Elemental uptake by calcite slowly grown from seawater solution: an In-situ study via depth profiling. Front. Earth Sci. 7:51. doi: 10.3389/feart.2019.00051

Gaetani, G. A., Cohen, A. L., Wang, Z., and Crusius, J. (2011). Rayleigh-based, multi-element coral thermometry: a biomineralization approach to developing climate proxies. Geochim. Cosmochim. Acta 75, 1920�. doi: 10.1016/j.gca.2011.01.010

Gagnon, A. C., Adkins, J. F., and Erez, J. (2012). Seawater transport during coral biomineralization. Earth Planet. Sci. Lett. 32, 150�. doi: 10.1016/j.epsl.2012.03.005

Gazeau, F., Parker, L. M., Comeau, S., Gattuso, J.-P. J.-P., O𠆜onnor, W. A., Martin, S., et al. (2013). Impacts of ocean acidification on marine shelled molluscs. Mar. Biol. 160, 2207�. doi: 10.1007/s00227-013-2219-3

Gillikin, D. P., Dehairs, F., Lorrain, A., Steenmans, D., Baeyens, W., and André, L. (2006). Barium uptake into the shells of the common mussel (Mytilus edulis) and the potential for estuarine paleo-chemistry reconstruction. Geochim. Cosmochim. Acta 70, 395�. doi: 10.1016/j.gca.2005.09.015

Giuffre, A. J., Gagnon, A. C., De Yoreo, J. J., and Dove, P. M. (2015). Isotopic tracer evidence for the amorphous calcium carbonate to calcite transformation by dissolution-reprecipitation. Geochim. Cosmochim. Acta 165, 407�. doi: 10.1016/j.gca.2015.06.002

Guillermic, M., Misra, S., Eagle, R., Villa, A., Chang, F., and Tripati, A. (2020). Seawater pH reconstruction using boron isotopes in multiple planktonic foraminifera species with different depth habitats and their potential to constrain pH and pCO 2 gradients. Biogeosciences 17, 3487�.

Harper, E. M., Palmer, T. J., and Alphey, J. R. (1997). Evolutionary response by bivalves to changing Phanerozoic sea-water chemistry. Geol. Mag. 134, 403�. doi: 10.1017/s0016756897007061

Hastie, T. J., and Tibshirani, R. J. (1990). Generalized Additive Models, Vol. 43. Boca Raton, FL: CRC press.

Hastie, T., Tibshirani, R., Narasimhan, B., and Gilbert, C. (2020). impute: Imputation for Microarray data. R Package. doi: 10.18129/B9.bioc.impute

Havach, S. M., Chandler, G. T., Wilson-Finelli, A., and Shaw, T. J. (2001). Experimental determination of trace element partition coefficients in cultured benthic foraminifera. Geochim. Cosmochim. Acta 65, 1277�. doi: 10.1016/S0016-7037(00)00563-9

Haynes, L. L., Hönisch, B., Holland, K., Rosenthal, Y., and Eggins, S. M. (2019). Evaluating the planktic foraminiferal B/Ca proxy for application to deep time paleoceanography. Earth Planet. Sci. Lett. 528, 115824. doi: 10.1016/j.epsl.2019.115824

Heinemann, F., Launspach, M., Gries, K., and Fritz, M. (2011). Gastropod nacre: structure, properties and growth – Biological, chemical and physical basics. Biophys. Chem. 153, 126�. doi: 10.1016/j.bpc.2010.11.003

Hemming, N. G., and Hanson, G. N. (1992). Boron isotopic composition and concentration in modern marine carbonates. Geochim. Cosmochim. Acta 56, 537�. doi: 10.1016/0016-7037(92)90151-8

Ho, L. S. T., Ane, C., Lachlan, R., Tarpinian, K., Feldman, R., Yu, Q., et al. (2016). Package ‘Phylolm’. Available online at: http://cran. r-project. org/web/packages/phylolm/index. html (accessed February, 2018).

Holcomb, M., DeCarlo, T. M., Gaetani, G. A., and McCulloch, M. (2016). Factors affecting B/Ca ratios in synthetic aragonite. Chem. Geol. 437, 67�. doi: 10.1016/j.chemgeo.2016.05.007

Holtmann, W. C. (2013). Sea Urchin Membrane Transport Mechanisms for Calcification and pH Homeostasis. Kiel: Christian Albrechts University.

Hope, R. M. (2013). Rmisc: Rmisc: Ryan Miscellaneous. R package version 1.5. Available online at: https://CRAN.R-project.org/package=Rmisc (accessed October 22, 2013).

Iglikowska, A., Beᐭowski, J., Cheᐬhowski, M., Chierici, M., K⊝ra, M., Przytarska, J., et al. (2016). Chemical composition of two mineralogically contrasting Arctic bivalves’ shells and their relationships to environmental variables. Mar. Pollut. Bull. 114, 903�. doi: 10.1016/j.marpolbul.2016.10.071

Immenhauser, A., Schöne, B. R., Hoffmann, R., and Niedermayr, A. (2016). Mollusc and brachiopod skeletal hard parts: intricate archives of their marine environment. Sedimentology 63, 1�. doi: 10.1111/sed.12231

Ives, A. R. (2018). R 2 s for correlated data: phylogenetic models, LMMs, and GLMMs. Syst. Biol. 68, 234�. doi: 10.1093/sysbio/syy060

Ives, A. R., and Li, D. (2018). rr2: an R package to calculate R 2 s for regression models. J. Open Source Softw. 3:1028.

Jacob, D. E., Wirth, R., Agbaje, O. B. A., Branson, O., and Eggins, S. M. (2017). Planktic foraminifera form their shells via metastable carbonate phases. Nat. Commun. 8:1265. doi: 10.1038/s41467-017-00955-0

Jurikova, H., Ippach, M., Liebetrau, V., Gutjahr, M., Krause, S., Büsse, S., et al. (2020). Incorporation of minor and trace elements into cultured brachiopods: implications for proxy application with new insights from a biomineralisation model. Geochim. Cosmochim. Acta 286, 418�. doi: 10.1016/j.gca.2020.07.026

Keul, N., Langer, G., de Nooijer, L. J., Nehrke, G., Reichart, G.-J., and Bijma, J. (2013). Incorporation of uranium in benthic foraminiferal calcite reflects seawater carbonate ion concentration. Geochem. Geophys. Geosyst. 14, 102�. doi: 10.1029/2012GC004330

Kondo, H., Toyofuku, T., and Ikeya, N. (2005). Mg/Ca ratios in the shells of cultured specimens and natural populations of the marine ostracode Xestoleberis hanaii (Crustacea). Palaeogeogr. Palaeoclimatol. Palaeoecol. 225, 3�. doi: 10.1016/j.palaeo.2004.05.026

Konrad, F., Purgstaller, B., Gallien, G., Mavromatis, V., Gane, P., and Dietzel, M. (2018). Influence of aqueous Mg concentration on the transformation of amorphous calcium carbonate. J. Cryst. Growth 498, 381�. doi: 10.1016/j.jcrystgro.2018.07.018

Kunioka, D., Shirai, K., Takahata, N., Sano, Y., Toyofuku, T., and Ujiie, Y. (2006). Microdistribution of Mg/Ca, Sr/Ca, and Ba/Ca ratios in Pulleniatina obliquiloculata test by using a NanoSIMS: implication for the vital effect mechanism. Geochem. Geophys. Geosyst. 7:Q1220. doi: 10.1029/2006GC001280

Lavigne, M., Hill, T. M., Sanford, E., Gaylord, B., Russell, A. D., Lenz, E. A., et al. (2013). The elemental composition of purple sea urchin (Strongylocentrotus purpuratus) calcite and potential effects of pCO2 during early life stages. Biogeosciences 10, 3465�. doi: 10.5194/bg-10-3465-2013

Le, N., Zidek, J., White, R., Cubranic, D., Sampson, P. D., Guttorp, P., et al. (2015). EnviroStat: Statistical Analysis of Environmental Space-Time Processes. R package version 0.4-2. Available online at: https://CRAN.R-project.org/package=EnviroStat (accessed June 03, 2015).

Lea, D. W. (2013). Elemental and Isotopic Proxies of Past Ocean Temperatures. Treatise on Geochemistry, 2nd Edn, Vol. 8. Oxford: Elsevier Ltd, doi: 10.1016/B978-0-08-095975-7.00614-8

Letunic, I., and Bork, P. (2019). Interactive tree Of Life (iTOL) v4: recent updates and new development. Nucleic Acids Res. 47, 256�.

Levi-Kalisman, Y., Raz, S., Weiner, S., Addadi, L., and Sagi, I. (2002). Structural differences between biogenic amorphous calcium carbonate phases using X-ray absorption spectroscopy. Adv. Funct. Mater. 12, 43�. doi: 10.1002/1616-3028(20020101)12:1㱃::AID-ADFM43σ.0.CO2-C

Liu, Y.-W. W., Sutton, J. N., Ries, J. B., and Eagle, R. A. (2020). Regulation of calcification site pH is a polyphyletic but not always governing response to ocean acidification. Sci. Adv. 6, 7𠄸. doi: 10.1126/sciadv.aax1314

Long, X., Ma, Y., and Qi, L. (2014). Biogenic and synthetic high magnesium calcite – A review. Journal of Structural Biology 185, 1�. doi: 10.1016/j.jsb.2013.11.004

Lorens, R. B., and Bender, M. L. (1977). Physiological exclusion of magnesium from Mytilus edulis calcite. Nature 269, 793�.

Lorens, R. B., and Bender, M. L. (1980). The impact of solution chemistry on Mytilus edulis calcite and aragonite. Geochim. Cosmochim. Acta 44, 1265�. doi: 10.1016/0016-7037

Loste, E., Wilson, R. M., Seshadri, R., and Meldrum, F. C. (2003). The role of magnesium in stabilising amorphous calcium carbonate and controlling calcite morphologies. J. Cryst. Growth 254, 206�. doi: 10.1016/S0022-0248(03)01153-9

Lowenstam, H. A. (1981). Minerals formed by weathering. Science 211, 1126�.

Luquet, G. (2012). Biomineralizations: insights and prospects from crustaceans. ZooKeys 176, 103�. doi: 10.3897/zookeys.176.2318

Marchitto, T. M., Oppo, D. W., and Curry, W. B. (2002). Paired benthic foraminiferal Cd/Ca and Zn/Ca evidence for a greatly increased presence of Southern Ocean Water in the glacial North Atlantic. Paleoceanography 17:1038. doi: 10.1029/2000PA000598

Märkel, K., Röser, U., Mackenstedt, U., and Klostermann, M. (1986). Ultrastructural investigation of matrix-mediated biomineralization in echinoids (Echinodermata, Echinoida). Zoomorphology 106, 232�. doi: 10.1007/BF00312044

Marra, G., and Wood, S. N. (2011). Practical variable selection for generalized additive models. Comput. Stat. Data Anal. 55, 2372�. doi: 10.1016/j.csda.2011.02.004

Mason, A. Z., and Nott, J. A. (1981). The role of intracellular biomineralized granules in the regulation and detoxification of metals in gastropods with special reference to the marine prosobranch Littorina littorea. Aquat. Toxicol. 1, 239�. doi: 10.1016/0166-445X(81)90018-7

Mass, T., Giuffre, A. J., Sun, C.-Y. Y., Stifler, C. A., Frazier, M. J., Neder, M., et al. (2017). Amorphous calcium carbonate particles form coral skeletons. Proc. Natl. Acad. Sci. U.S.A. 114, E7670�. doi: 10.1073/pnas.1707890114

Mavromatis, V., Goetschl, K. E., Grengg, C., Konrad, F., Purgstaller, B., and Dietzel, M. (2018). Barium partitioning in calcite and aragonite as a function of growth rate. Geochim. Cosmochim. Acta 237, 65�. doi: 10.1016/j.gca.2018.06.018

Mavromatis, V., Montouillout, V., Noireaux, J., Gaillardet, J., and Schott, J. (2015). Characterization of boron incorporation and speciation in calcite and aragonite from co-precipitation experiments under controlled pH, temperature and precipitation rate. Geochim. Cosmochim. Acta 150, 299�. doi: 10.1016/j.gca.2014.10.024

McCulloch, M. T., D’Olivo, J. P., Falter, J., Holcomb, M., and Trotter, J. A. (2017). Coral calcification in a changing World and the interactive dynamics of pH and DIC upregulation. Nat. Commun. 8, 1𠄸. doi: 10.1038/ncomms15686

Menadakis, M., Maroulis, G., and Koutsoukos, P. G. (2009). Incorporation of Mg 2+ , Sr 2+ , Ba 2+ and Zn 2+ into aragonite and comparison with calcite. J. Math. Chem. 46, 484�. doi: 10.1007/s10910-008-9490-4

Mergelsberg, S. T., De Yoreo, J. J., Miller, Q. R. S., Marc Michel, F., Ulrich, R. N., and Dove, P. M. (2020). Metastable solubility and local structure of amorphous calcium carbonate (ACC). Geochim. Cosmochim. Acta 289, 196�. doi: 10.1016/j.gca.2020.06.030

Mergelsberg, S. T., Ulrich, R. N., Xiao, S., and Dove, P. M. (2019). Composition systematics in the exoskeleton of the american lobster, Homarus americanus and implications for malacostraca. Front. Earth Sci. 7:69. doi: 10.3389/feart.2019.00069

Meseck, S. L., Mercaldo-Allen, R., Kuropat, C., Clark, P., and Goldberg, R. (2018). Variability in sediment-water carbonate chemistry and bivalve abundance after bivalve settlement in Long Island Sound, Milford, Connecticut. Mar. Pollut. Bull. 135, 165�. doi: 10.1016/j.marpolbul.2018.07.025

Montagna, P., McCulloch, M., Douville, E., López Correa, M., Trotter, J., Rodolfo-Metalpa, R., et al. (2014). Li/Mg systematics in scleractinian corals: calibration of the thermometer. Geochim. Cosmochim. Acta 132, 288�. doi: 10.1016/j.gca.2014.02.005

Mucci, A., and Morse, J. W. (1983). The incorporation of Mg 2+ and Sr 2+ into calcite overgrowths: influences of growth rate and solution composition. Geochim. Cosmochim. Acta 47, 217�. doi: 10.1016/0016-7037(83)90135-7

Nassif, N., Pinna, N., Gehrke, N., Antonietti, M., Jäger, C., and Cölfen, H. (2005). Amorphous layer around aragonite platelets in nacre. Proc. Natl. Acad. Sci. U.S.Am. 102, 12653�. doi: 10.1073/pnas.0502577102

Nguyen, T. T. (2013). Li/Ca, B/Ca, and Mg/Ca Composition of Cultured Sea Urchin Spines and Paleo-Echinoderms Measured Using a Secondary Ion Mass Spectrometer. Los Angeles, CA: University of California.

Ogilvie, M. (1896). Corals: microscopic and systematic study of Madreporarian types of corals. Phil. Trans. R Soc. Lond. 187, 83�.

Oksanen, J., Kindt, R., Legendre, P., O’Hara, B., Simpson, G. L., Solymos, P. M., et al. (2008). The Vegan Package. Community Ecology Package, (January). 190. Available online at: https://bcrc.bio.umass.edu/biometry/images/8/85/Vegan.pdf (accessed January, 2008).

Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature 401, 877�.

Park, W. K., Ko, S. J., Lee, S. W., Cho, K. H., Ahn, J. W., and Han, C. (2008). Effects of magnesium chloride and organic additives on the synthesis of aragonite precipitated calcium carbonate. J. Cryst. Growth 310, 2593�. doi: 10.1016/j.jcrysgro.2008.01.023

Piwoni-Piórewicz, A., Strekopytov, S., Humphreys-Williams, E., and Kukliński, P. (2021). The patterns of elemental concentration (Ca, Na, Sr, Mg, Mn, Ba, Cu, Pb, V, Y, U and Cd) in shells of invertebrates representing different CaCO3 polymorphs: a case study from the brackish Gulf of Gdañsk (the Baltic Sea). Biogeosciences 18, 707�. doi: 10.5194/bg-18-707-2021

Purgstaller, B., Goetschl, K. E., Mavromatis, V., and Dietzel, M. (2019). Solubility investigations in the amorphous calcium magnesium carbonate system. Cryst. Eng. Commun. 21, 155�. doi: 10.1039/c8ce01596a

Purgstaller, B., Mavromatis, V., Immenhauser, A., and Dietzel, M. (2016). Transformation of Mg-bearing amorphous calcium carbonate to Mg-calcite – In situ monitoring. Geochim. Cosmochim. Acta 174, 180�. doi: 10.1016/j.gca.2015.10.030

R Core Team (2019). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.

Rahman, M. A., Halfar, J., Adey, W. H., Nash, M., Paulo, C., and Dittrich, M. (2019). The role of chitin-rich skeletal organic matrix on the crystallization of calcium carbonate in the crustose coralline alga Leptophytum foecundum. Sci. Rep. 9:11869. doi: 10.1038/s41598-019-47785-2

Raitzsch, M., Due༚s-Bohórquez, A., Reichart, G.-J., de Nooijer, L. J., and Bickert, T. (2010). Incorporation of Mg and Sr in calcite of cultured benthic foraminifera: impact of calcium concentra- tion and associated calcite saturation state. Biogeosciences 7, 869�. doi: 10.5194/bg-7-869-2010

Raz, S., Weiner, S., and Addadi, L. (2000). Formation of high-magnesian calcites via an amorphous precursor phase: possible biological implications. Adv. Mater. 12, 38�. doi: 10.1002/(SICI)1521-4095(200001)12:1㰸::AID-ADMA38σ.0.CO2-I

Reeder, R. J. (1983). Crystal chemistry of the rhombohedral carbonates. Rev. Mineral. 11, 1�.

Revell, L. J. (2009). Size-correction and principal components for interspecific comparative studies. Evolution 63, 3258�.

Revell, L. J. (2012). phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217�.

Ries, J. B. (2006). Mg fractionation in crustose coralline algae: geochemical, biological, and sedimentological implications of secular variation in the Mg/Ca ratio of seawater. Geochim. Cosmochim. Acta 70, 891�. doi: 10.1016/j.gca.2005.10.025

Ries, J. B. (2009). Effects of secular variation in seawater Mg/Ca ratio (calcite-aragonite seas) on CaCO3 sediment production by the calcareous algae Halimeda, Penicillus and Udotea – Evidence from recent experiments and the geological record. Terra Nova 21, 323�. doi: 10.1111/j.1365-3121.2009.00899.x

Ries, J. B. (2010). Review: geological and experimental evidence for secular variation in seawater Mg/Ca (calcite-aragonite seas) and its effects on marine biological calcification. Biogeosciences 7, 2795�. doi: 10.5194/bg-7-2795-2010

Ries, J. B. (2011). Skeletal mineralogy in a high-CO2 world. J. Exp. Mar. Biol. Ecol. 403, 54�. doi: 10.1016/j.jembe.2011.04.006

Ries, J. B., Cohen, A. L., and McCorkle, D. C. (2009). Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37, 1131�. doi: 10.1130/G30210A.1

Ries, J. B., Ghazaleh, M. N., Connolly, B., Westfield, I., and Castillo, K. D. (2016). Impacts of seawater saturation state (㪚=0.4𠄴.6) and temperature (10, 25 ଌ) on the dissolution kinetics of whole-shell biogenic carbonates. Geochim. Cosmochim. Acta 192, 318�. doi: 10.1016/j.gca.2016.07.001

Roer, R., and Dillaman, R. (1984). The structure and calcification of the crustacean cuticle. Integr. Comp. Biol. 24, 893�. doi: 10.1093/icb/24.4.893

Rosenheim, B. E., Swart, P. K., and Thorrold, S. R. (2005). Minor and trace elements in sclerosponge Ceratoporella nicholsoni: biogenic aragonite near the inorganic endmember? Palaeogeogr. Palaeoclimatol. Palaeoecol. 228, 109�. doi: 10.1016/j.palaeo.2005.03.055

Rosenthal, Y., Boyle, E. A., and Slowey, N. (1997). Temperature control on the incorporation of magnesium, strontium, fluorine, and cadmium into benthic foraminiferal shells from Little Bahama Bank: prospects for thermocline paleoceanography. Geochim. Cosmochim. Acta 61, 3633�.

Russell, A. D., Hönisch, B., Spero, H. J., and Lea, D. W. (2004). Effects of seawater carbonate ion concentration and temperature on shell U, Mg, and Sr in cultured planktonic foraminifera. Geochim. Cosmochim. Acta 68, 4347�. doi: 10.1016/j.gca.2004.03.013

Schöne, B. R., Zhang, Z., Jacob, D., Gillikin, D. P., Tütken, T., Garbe-Schönberg, D., et al. (2010). Effect of organic matrices on the determination of the trace element chemistry (Mg, Sr, Mg/Ca, Sr/Ca) of aragonitic bivalve shells (Arctica islandica) – comparison of ICP-OES and LA-ICP-MS data. Geochem. J. 44, 23�. doi: 10.2343/geochemj.1.0045

Shen, G. T., Campbell, T. M., Dunbar, R. B., Wellington, G. M., Colgan, M. W., and Glynn, P. W. (1991). Paleochemistry of manganese in corals from the Galapagos Islands. Coral Reefs 10, 91�.

Short, J., Foster, T., Falter, J., Kendrick, G. A., and McCulloch, M. T. (2015). Crustose coralline algal growth, calcification and mortality following a marine heatwave in Western Australia. Cont. Shelf Res. 106, 38�. doi: 10.1016/j.csr.2015.07.003

Simkiss, K., Taylor, M., and Greaves, G. N. (1986). Amorphous structure of intracellular mineral granules. Biochem. Soc. Trans. 14, 549�. doi: 10.1042/bst0140549

Sinclair, D. J., and Risk, M. J. (2006). A numerical model of trace-element coprecipitation in a physicochemical calcification system: application to coral biomineralization and trace-element “vital effects.”. Geochim. Cosmochim. Acta 70, 3855�. doi: 10.1016/j.gca.2006.05.019

Stanley, S. M., and Hardie, L. A. (1999). Hypercalcification: paleontology links plate tectonics. GSA Today 9, 1𠄷.

Stumpp, M., Hu, M. Y., Melzner, F., Gutowska, M. A., Dorey, N., Himmerkus, N., et al. (2012). Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification. Proc. Natl. Acad. Sci. U.S.A. 109, 18192�. doi: 10.1073/pnas.1209174109

Suchard, M. A., Lemey, P., Baele, G., Ayres, D. L., Drummond, A. J., and Rambaut, A. (2018). Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4:vey016.

Sugawara, A., and Kato, T. (2000). Aragonite CaCO3 thin-film formation by cooperation of Mg2+ and organic polymer matrices. Chem. Commun. 6, 487�. doi: 10.1039/A909566G

Sutton, J. N., Liu, Y. W., Ries, J. B., Guillermic, M., Ponzevera, E., and Eagle, R. A. (2018). � as monitor of calcification site pH in divergent marine calcifying organisms. Biogeosciences 15, 1447�. doi: 10.5194/bg-15-1447-2018

Tambutté, E., Tambutté, S., Segonds, N., Zoccola, D., Venn, A., Erez, J., et al. (2011). Calcein labelling and electrophysiology: insights on coral tissue permeability and calcification. Proc. R. Soc. B Biol. Sci. 279, 19�. doi: 10.1098/rspb.2011.0733

Tripati, A. K., Roberts, C. D., and Eagle, R. A. (2009). Coupling of CO2 and Ice sheet stability over major climate transitions of the last 20 million years. Science 326, 1394�. doi: 10.1126/science.1178296

Tripati, A. K., Roberts, C. D., Eagle, R. A., and Li, G. (2011). A 20 million year record of planktic foraminiferal B/Ca ratios: systematics and uncertainties in pCO2 reconstructions. Geochim. Cosmochim. Acta 75, 2582�. doi: 10.1016/j.gca.2011.01.018

Venn, A. A., Bernardet, C., Chabenat, A., Tambutté, E., and Tambutté, S. (2020). Paracellular transport to the coral calcifying medium: effects of environmental parameters. J. Exp. Bio. 223:jeb227074. doi: 10.1242/jeb.227074

Von Euw, S., Zhang, Q., Manichev, V., Murali, N., Gross, J., Feldman, L. C., et al. (2017). Biological control of aragonite formation in stony corals. Science 356, 933�. doi: 10.1126/science.aam6371

Watson, E. B. (2004). A conceptual model for near-surface kinetic controls on the trace- element and stable isotope composition of abiogenic calcite crystals. Geochim. Cosmochim. Acta 68, 1473�. doi: 10.1016/j.gca.2003.10.003

Weiner, S., and Dove, P. M. (2003). An overview of biomineralization processes and the problem of the vital effect. Rev. Mineral. Geochem. 54, 1�. doi: 10.2113/0540001

Weiss, I. M., Tuross, N., Addadi, L., and Weiner, S. (2002). Mollusc larval shell formation: amorphous calcium carbonate is a precursor phase for aragonite. J. Exp. Zool. 293, 478�. doi: 10.1002/jez.90004

Wickham, H. (2009). ggplot2: Elegant Graphics for Data Analysis – Hadley Wickham – Google Books. Springer Science & Business Media. Houston, TX: Springer Nature. doi: 10.1007/978-3-319-24277-4

Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis. New York, NY: Springer-Verlag.

Wickins, J. F. (1984). The effect of reduced pH on carapace calcium, strontium and magnesium levels in rapidly growing prawns (Penaeus monodon fabricius). Aquaculture 41, 49�. doi: 10.1016/0044-8486(84)90389-2

Wilbur, K. M., Colinvaux, L. H., and Watabe, N. (1969). Electron microscope study of calcification in the alga Halimeda (order Siphonales). Phycologia 8, 27�. doi: 10.2216/i0031-8884-8-1-27.1

Wilke, C. O. (2020). ggtext: Improved Text Rendering Support for ‘ggplot2’. R package version 0.1.0. Available online at: https://CRAN.R-project.org/package=ggtext (accessed Dec 17, 2020).

Wilt, F. H. (2002). Biomineralization of the spicules of sea urchin embryos. Zool. Sci. 19, 253�. doi: 10.2108/zsj.19.253

Wood, S.N. (2011). Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J. R. Stat. Soc. B 73, 3�.

Wood, S. N. (2017). Generalized Additive Models: An Introduction with R, 2nd Edn. Boca Raton, FL: Chapman and Hall, doi: 10.1201/9781315370279

Yu, J., Day, J., Greaves, M., and Elderfield, H. (2005). Determination of multiple element/calcium ratios in foraminiferal calcite by quadrupole ICP-MS. Geochem. Geophys. Geosyst. 6:Q0801. doi: 10.1029/2005GC000964

Yu, J., Elderfield, H., and Hönisch, B. (2007). B/Ca in planktonic foraminifera as a proxy for surface seawater pH. Paleoceanography 22:A2202. doi: 10.1029/2006PA001347

Yu, J., Foster, G. L., Elderfield, H., Broecker, W. S., and Clark, E. (2010). An evaluation of benthic foraminiferal B/Ca and � for deep ocean carbonate ion and pH reconstructions. Earth Planet. Sci. Lett. 293, 114�. doi: 10.1016/j.epsl.2010.02.029

Zacherl, D. C., Paradis, G., and Lea, D. W. (2003). Barium and strontium uptake into larval protoconchs and statoliths of the marine neogastropod Kelletia kelledi. Geochim. Cosmochim. Acta 67, 4091�.

Zeileis, A., and Hothorn, T. (2002). Diagnostic checking in regression relationships. R News 2, 7�.

Keywords : marine calcification, calcite, aragonite, trace elements, ocean acidification, biomineralization, phylogeny

Citation: Ulrich RN, Guillermic M, Campbell J, Hakim A, Han R, Singh S, Stewart JD, Román-Palacios C, Carroll HM, De Corte I, Gilmore RE, Doss W, Tripati A, Ries JB and Eagle RA (2021) Patterns of Element Incorporation in Calcium Carbonate Biominerals Recapitulate Phylogeny for a Diverse Range of Marine Calcifiers. Front. Earth Sci. 9:641760. doi: 10.3389/feart.2021.641760

Received: 14 December 2020 Accepted: 24 March 2021
Published: 04 May 2021.

Claire Rollion-Bard, UMR 7154 Institut de Physique du Globe de Paris (IPGP), France

Toshihiro Yoshimura, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Japan
Dong Feng, Shanghai Ocean University, China

Copyright © 2021 Ulrich, Guillermic, Campbell, Hakim, Han, Singh, Stewart, Román-Palacios, Carroll, De Corte, Gilmore, Doss, Tripati, Ries and Eagle. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.


4 DISCUSSION

We spatially described and quantified echinoderm populations on Georges Bank at a spatial resolution of square kilometers (improving available spatial resolution by at least an order of magnitude). Abundance and distribution varied significantly among the four echinoderm groups and between management areas. Brittle stars were mainly restricted to the northern edge of the bank, between CAI and CAII. Sand dollars dominated the central areas of the bank as well as the central portion of NLSA. Sea stars dominated the southern edge of the bank and were highly aggregated in the southern non-fishing portion of NLSA and in the adjacent southern open areas. Sea urchins were found in all sampled areas of the bank with the exception of the southern edge. The lack of overlap in the density hotspots of these echinoderm groups suggest that echinoderm populations in Georges Bank are habitat-specific.

Echinoderms are ubiquitous, persistent, dominant, and resilient organisms but have distinct patterns of habitat preference (Cusson & Bourget, 2005 Ellis & Rogers, 2000 Freeman & Rogers, 2003 Thouzeau et al., 1991 ). All of these were characteristics observed in this study. The preferred environmental conditions (driven primarily by depth, sediment stability, and temperature), along with predator abundance, were the most important factors in explaining the patterns of echinoderm assemblage on Georges Bank. These environmental descriptors of echinoderm habitat generally agreed with related literature. For example, an examination of global patterns of marine benthic macroinvertebrate production determined that temperature was the most important variable explaining the variance of echinoderm populations (Cusson & Bourget, 2005 ). Kostylev et al. ( 2001 ) found a strong association of echinoderm taxa with depth and specific hydrodynamic conditions of Browns Bank on the southwestern Scotian Shelf, off the Canadian Atlantic coast. The influence of management area in our study was also significant. Thus, higher abundances of echinoderms in closed areas than in adjacent open areas that share similar biological and environmental conditions may be indicative of an indirect, positive effect of reduced fishing over these populations.

Sediment stability and temperature were strongly related with the distribution of sea stars and sea urchins. Stable sediments reduce the potential of suffocation and burial of these organisms in comparison with highly unstable sediments (Aronson, 1992 Hinchey, Schaffner, Hoar, Vogt, & Batte, 2006 ). Strong currents and high shear stress also compromise the directional swimming ability of sea urchin larvae (Sameoto, Ross, & Metaxas, 2010 ). Conversely, sand dollars were the only echinoderm associated with relatively unstable sediments (sediment index >1), but their density decreased in the most unstable regimes (sediment index >3). Feeding of these flat sand dollars is actually enhanced under unstable conditions, because more food in the form of suspended particles is readily available (O'Neill, 1978 ). However, at higher water velocities associated with a storm surge event, sand dollars bury themselves for protection (O'Neill, 1978 ), and these storm events may negatively influence their survival. Stable sediments and temperatures ranging 7–13°C appeared to be related to the narrow center of distribution of sea stars in the southern areas of the bank. Sea star distribution on the North Atlantic coast may be controlled by temperature (Khanna & Yadav, 2005 ). Furthermore, mortality of Asterias vulgaris Verrill 1866, one of the most representative species of this ecosystem (Bigelow & Schroeder, 2002 Link & Almeida, 2000 Theroux & Wigley, 1998 ), is associated with temperatures >25°C (Khanna & Yadav, 2005 ). For sea urchins, temperatures >15°C have a considerable detrimental effect on the development of larvae (Stephens, 1972 ) and increased mortality of adults (Scheibling & Stephenson, 1984 ).

Predator abundance was as strongly correlated with echinoderm abundance as the environmental factors. High densities of American plaice and brittle stars were observed in the same northern areas of the bank. Brittle stars are a preferred prey of American plaice in this ecosystem (Link & Almeida, 2000 Packer et al., 1994 ). Similarly, haddock prey on sand dollars (Link & Almeida, 2000 ), and their densities were also positively correlated. We were expecting to observe a stronger correlation between ocean pout and sand dollars, because they are a preferred prey (Buzulutskaya, 1983 Link & Almeida, 2000 ). The weakly negative correlation may have resulted from a stronger association between ocean pout and urchins because both share similar substrates (e.g., cobble, boulder). Ocean pout distribution may be related to coarse sediments because their fertilized eggs are laid in rocky crevices (Steimle, Morse, Berrien, Johnson, & Zetlin, 1999 ).

Sea scallops and sea star distribution were weakly associated, although previous studies indicate that sea star distribution can be influenced by the location of their prey (Marino et al., 2009 ). Predator and prey densities are influenced by the spatial scale used in the analysis (Rose & Leggett, 1990 ). Stronger species-specific relationships may only be determined at local scales, rather than at the regional scales used in our analysis. Georges Bank is considered a predator-controlled ecosystem (Worm & Myers, 2003 ) and our results support this hypothesis, because the influence of predators in echinoderm populations was stronger than that of prey availability. Therefore, a stronger association between sea stars and scallops may only be discernible by analyzing these populations separately.

Several studies indicate that the establishment of MPAs leads to significant differences in invertebrate populations after a period of time, with a general consensus that abundance, biomass, and diversity are modified as a result of diminishing the impacts of fishing disturbance (Ashworth, Ormond, & Sturrock, 2004 Collie et al., 1997 Hermsen et al., 2003 Marino et al., 2007 Stokesbury, 2002 ). The types of fishing disturbance include direct removal of invertebrates by fishing gear, body breakage, enhanced predation and migration rates, along with modification of sediments via re-suspension of finer particles or dispersion of coarser sediments (Asch & Collie, 2008 Prena et al., 1999 Stokesbury & Harris, 2006 ).

Initially, brittle stars were expected to be more abundant in undisturbed areas than in open areas, because there would likely be less removal, burial, or body breakage caused by bottom fishing gear (Collie et al., 1997 Hansson, Lindegarth, Valentinsson, & Ulmestrand, 2000 Prena et al., 1999 ). The high abundance of brittle stars in open areas seen in the present study may have several explanations, including a possible reduction in predation pressure, and the capacity of brittle stars (with the capability to regenerate lost arms and portions of the central disk Hendler, Miller, Pawson, & Kier, 1995 Kaiser & Spencer, 1995 ) to survive damage induced by bottom trawls. Furthermore, trawling may increase food availability in the form of damaged organisms and disturbed sediment particles, and thus may be beneficial to brittle stars (Ramsay, Kaiser, & Hughes, 1998 Tuck, Hall, Robertson, Armstrong, & Basford, 1998 ).

Estimates of brittle star density were limited by the distribution of survey stations, which provided few records within brittle star habitat. The SMAST video survey was designed primarily to examine the distribution and abundance of scallops, thus habitats outside their distribution range were not sampled. These include stations with depths >160 m. Brittle stars may be found in waters well below the 100 m isobath. Therefore, brittle star habitat is underrepresented in the present study and unambiguous evidence about the lack of impact of MPAs on these populations cannot be adequately evaluated.

Sand dollars have high survival rates when they are discarded from bottom trawls, and may have the ability to recover fast from potential damage inflicted on the test during trawling. Sand dollars also re-aggregate rapidly after a disruption of their beds (Murawski & Serchuk, 1989 ). Therefore, the presence and high-density aggregation of sand dollars in different areas of Georges Bank, regardless of the presence of fishing pressure, was expected. However, some studies have also found significantly lower biomasses in trawled areas compared to undisturbed sites (Murawski & Serchuk, 1989 Prena et al., 1999 ). The unusual high density observed inside the closed portion of CAI is likely the result of a high recruitment and survivorship of sand dollars prior to 2008. High survivorship may be partly related to low fishing disturbance in this area, while retention of larvae in this area is primarily determined by current and wind patterns (Tian et al., 2009 ). Higher density of sand dollars observed in the non-fishing portion of NLSA compared to the partial access area, also suggests a positive effect of the closure itself. Higher densities inside closed areas, in combination with preferred habitat conditions, may indicate a positive effect of the closure via enhanced reproduction (improving the external fertilization rate in undisturbed beds) and higher recruitment (Highsmith, 1982 Merrill & Hobson, 1970 ).

A caveat of the sand dollar population estimates in open areas is that the center of the bank was not sampled. Based on their distribution, it is likely that densities in this area are high and therefore sand dollar abundance is underestimated in open areas. Nevertheless, the SMAST video survey covers an important part of the distribution range of these individuals because sea scallops (the target species of study in this survey) and sand dollars share similar habitats (Stokesbury & Harris, 2006 ).

Highest densities of sea stars were found inside NLSA. The environmental conditions (e.g., temperature and sediment stability) found inside this closed area are similar to those observed in the adjacent southern open areas, suggesting a direct positive impact of this MPA on these populations. Reducing the impacts of fishing disturbance may enhance recruitment of sea stars in this area. This hypothesis is supported by the presence of smaller individuals inside closed areas compared to open areas (Marino et al., 2007 Rosellon-Druker, 2017 ). As with sand dollars, sea stars were also persistent and abundant in open areas, indicating natural resilience. Furthermore, fishing activities in open areas may provide food for scavenging sea stars in the form of other damaged animals that are left in the track of a trawl or dredge (Ramsay et al., 1998 ).

The similarity in density of sea urchins among management areas was expected, since these organisms were strongly associated with hard bottoms (Meidel & Scheibling, 1998 ), which are found both in closed and open areas (Harris & Stokesbury, 2010 ) and are generally avoided by fishing gears (Collie et al., 1997 ). Sea urchin population estimations in this study are uncertain because of the small sample size. Sea urchins were the most difficult echinoderm to identify in the video survey, since they can be confounded with the substrate (e.g., pebbles and small rocks).

In conclusion, we provided the first estimates of density and absolute abundance of the main echinoderm taxa of Georges Bank at a spatial resolution of kilometers, allowing the examination of these populations in relation with different management regimes. This spatial and temporal characterization of echinoderm populations on Georges Bank has important ecological applications. Echinoderm beds, with hundreds of individuals per square meter, may directly and indirectly affect other species (Fujita & Ohta, 1989 Highsmith, 1982 Howell et al., 2002 Merrill & Hobson, 1970 ). Indirect impacts of these echinoderm aggregations include physical alterations to the habitats where they are present, such as the mechanical disruption of sediments by burrowing (Smith, 1981 ). Direct impacts of echinoderm aggregations include the intensification of biological interactions with other species that might be of economic importance. For example, the average annual density of sand dollars at Georges Bank (35 individuals per m 2 ) was 30-fold greater than the density of scallops (0.14 individuals per m 2 ) in the same time period (2005–2012), while the average annual density of sea stars (six individuals per m 2 ) was sixfold greater than scallops. Sand dollars and scallops share essential habitats (Stokesbury, 2002 Stokesbury et al., 2004 ), and thus competitive exclusion for space may be occurring. Sea stars are main predators of scallops (Marino et al., 2009 ), and therefore location of hotspots of sea star density may help to delineate areas where consumption is enhanced.

Finally, an important management application of this work is the incorporation of these echinoderm population estimates into stock assessment models. Echinoderms are not commonly included in available models because of limited information about the distribution and abundance of these organisms at appropriate temporal and spatial scales (Schückel, Ehrich, Kröncke, & Reiss, 2010 ). The improved spatial resolution of echinoderm density provided here can remove some of these constraints, and has important implications for implementation of multispecies models and, as a result, ecosystem-based fisheries management.


Watch the video: Feather Stars and Their Animal Invaders. Nat Geo Wild (February 2023).