DOCSLIB.ORG

Trunk Neural Crest Origin of Dermal Denticles in a Cartilaginous Fish

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Trunk Neural Crest Origin of Dermal Denticles in a Cartilaginous Fish Trunk neural crest origin of dermal denticles in a cartilaginous fish J. Andrew Gillisa,b,1, Els C. Alsemaa,c, and Katharine E. Criswella,b aDepartment of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom; bWhitman Center, Marine Biological Laboratory, Woods Hole, MA 02543; and cKarolinska Institutet, SE-171 77 Stockholm, Sweden Edited by Marianne Bronner, California Institute of Technology, Pasadena, CA, and approved October 26, 2017 (received for review August 4, 2017) Cartilaginous fishes (e.g., sharks and skates) possess a postcranial odontogenic in nature (14, 15), they do not exhibit key histo- dermal skeleton consisting of tooth-like “denticles” embedded within logical features of dentine (e.g., dentine tubules), and their mode their skin. As with teeth, the principal skeletal tissue of dermal den- of development and growth is more similar to that of acellular ticles is dentine. In the head, cranial neural crest cells give rise to the bone (16, 17). We therefore sought to test the odontogenic po- dentine-producing cells (odontoblasts) of teeth. However, trunk neu- tential of trunk neural crest cells in a taxon that has retained ral crest cells are generally regarded as nonskeletogenic, and so the typical dentine in their postcranial dermal skeleton—a cartilag- embryonic origin of trunk denticle odontoblasts remains unresolved. inous fish, the little skate, Leucoraja erinacea. Here, we use expression of FoxD3 to pinpoint the specification and emigration of trunk neural crest cells in embryos of a cartilaginous Results fish, the little skate (Leucoraja erinacea). Using cell lineage tracing, The neural crest is a multipotent cell population that undergoes we further demonstrate that trunk neural crest cells do, in fact, give epithelial-to-mesenchymal transition from the developing central rise to odontoblasts of trunk dermal denticles. These findings expand nervous system of vertebrate embryos and that migrates exten- the repertoire of vertebrate trunk neural crest cell fates during nor- sively to give rise to a diversity of skeletal and nonskeletal cell mal development, highlight the likely primitive skeletogenic poten- types (18). Histological studies of shark (Scyliorhinus torazame) tial of this cell population, and point to a neural crest origin of embryos have revealed that neural crest cells begin to emigrate dentine throughout the ancestral vertebrate dermal skeleton. from the cranial neural tube at developmental stage (S)18 and from the trunk neural tube at approximately stage S19 (ref. 19, skate | neural crest | denticle | evolution | skeleton with staging according to ref. 20). To verify the timing of trunk neural crest cell emigration in skate embryos, we conducted a awed vertebrates (gnathostomes) primitively possessed an series of mRNA in situ hybridization experiments to characterize Jextensive postcranial dermal skeleton, consisting of both a expression of the transcription factor, FoxD3—a neural crest basal osteogenic component (composed of acellular bone and/or specifier that is expressed in nascent and early migratory neural lamellar bone-like tissues) and a superficial odontogenic com- crest cells (21). At S18 (Fig. 2A), we observed FoxD3-expressing ponent (composed of dentine overlain by enamel or enameloid) cells (i.e., premigratory neural crest cells) in the dorsal trunk (1). Elaboration of this dermal skeleton is closely tied to the neural tube. We observed that, as in the shark, trunk neural crest diversification of gnathostomes, but the developmental and cells begin emigrating in skate embryos at S19, based on the evolutionary origins of this skeletal system remain unresolved. A appearance FoxD3-expressing cells undergoing epithelial-to- postcranial dermal skeleton is present in several extant gna- mesenchymal transition from the dorsal trunk neural tube (Fig. 2B). thostome lineages—e.g., in the form of scales, denticles, or — scutes of fishes (2) although these elements exhibit consider- Significance able histological variation and are often much reduced relative to the dermal armor of stem gnathostomes. For example, the vast The earliest mineralized skeleton of vertebrates was the der- majority of teleost fishes possess lightly mineralized bony scales mal skeleton: superficial armor of tooth-like skeletal units that lack typical dentine or enamel and that likely derive from composed of dentine and basal bone of attachment. Remnants the osteogenic component of the primitive gnathostome dermal of this dentinous armor have been retained as teeth in the skeleton. Conversely, cartilaginous fishes (sharks, skates, and head of all jawed vertebrates and as dermal denticles in the rays) possess well-mineralized dermal denticles (Fig. 1) that are skin of cartilaginous fishes (sharks and skates). Cranial neural composed of typical dentine and enameloid, but that lack basal crest cells (NCCs) give rise to dentine-secreting odontoblasts of bone of attachment (3). teeth. However, trunk NCCs are regarded as nonskeletogenic, Bone and dentine are both mesenchymal in origin and are raising questions about the embryonic origin of postcranial secreted by osteoblasts and odontoblasts, respectively, while denticles in cartilaginous fishes. Here, we show that trunk enamel matrix is secreted by epithelial ameloblasts (with NCCs give rise to trunk denticle odontoblasts in the skate, “ ” enameloid resulting from the mineralization of mixed dentine Leucoraja erinacea. This finding expands the repertoire of and enamel matrices; ref. 4). Based on comparison with the trunk NCC fates, highlighting the primitive skeletogenic po- cranial dermal skeleton, in which much of the dermal bone (i.e., tential of this cell population. of the skull vault) and all dentine (i.e., of oral teeth) is neural crest-derived (5–7), it has long been assumed that these tissues Author contributions: J.A.G. designed research; J.A.G. and K.E.C. performed research; share a similar neural crest origin in the trunk (8, 9). However, J.A.G., E.C.A., and K.E.C. analyzed data; and J.A.G. wrote the paper. recent fate-mapping studies in teleosts have called this assump- The authors declare no conflict of interest. tion into question: cell lineage-tracing experiments in zebrafish This article is a PNAS Direct Submission. (10, 11) and medaka (12) have demonstrated a paraxial meso- Published under the PNAS license. dermal origin of scale-producing osteoblasts, leading to sugges- Data deposition: The sequence reported in this paper has been deposited in the GenBank tions that trunk neural crest cells lack skeletogenic potential in database (accession no. MF281542). fishes (10, 12, 13). However, the embryonic origin of the denti- 1To whom correspondence should be addressed. Email: [email protected]. nous component of the postcranial dermal skeleton remains This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. unresolved. While it has been suggested that teleost scales are 1073/pnas.1713827114/-/DCSupplemental. 13200–13205 | PNAS | December 12, 2017 | vol. 114 | no. 50 www.pnas.org/cgi/doi/10.1073/pnas.1713827114 Downloaded by guest on September 26, 2021 BIOLOGY DEVELOPMENTAL Fig. 1. Dermal denticles of the little skate. (A) A skate hatchling and (B) skeletal preparation exhibit prominent dorsal median (arrow) and paired dorso- lateral rows (arrowheads) of dermal denticles extending the length of the trunk. (C) These denticles (*) are recurved, with a tooth-like morphology. (D)A sagittal section through a differentiated dermal denticle (preeruption) at embryonic stage 33 reveals a pulp cavity filled with mesenchyme (Pulp in Di), a morphologically distinct layer of dentine-secreting odontoblasts (Odont. in Di) lining the wall of the pulp cavity, and a layer of cuboidal enamel-secreting ameloblasts (Amel. in Di). (Scale bars: A and B, 1 cm; C,750μm; D,20μm; Di,10μm.) This migration continues through S22 (Fig. 2C), at which point polarized secretory cells with characteristic cell processes lying ad- we also begin to observe rostral differentiation of trunk neural jacent to newly secreted dentine matrix (3) (Fig. 1D). In total, we crest derivatives (e.g., dorsal root ganglia). recovered 15 CM-DiI–labeled trunk denticle odontoblasts in em- To label premigratory trunk neural crest cells in skate embryos, bryos that were examined histologically (n = 8; Fig. 3 E and F— we microinjected the lipophilic dye CM-DiI into the lumen of the additional examples provided in Fig. S1), indicating their neural trunk neural tube at S18 (Fig. 3A). This strategy ensures focal la- crest origin. Seven out of eight examined embryos possessed CM- beling of the neural tube (including premigratory neural crest cells) DiI–labeled odontoblasts, with each positive embryo possessing and has been used extensively in other systems to test neural crest between one and four labeled cells (Table S1). CM-DiI–labeled cell fates (22–26). Five days postinjection, labeled neural crest cells odontoblasts always occurred singly, with their rarity likely due to could be observed emigrating from the trunk neural tube of CM- dilution of the label through substantial proliferation between DiI–injected skate embryos (Fig. 3B). Embryos with CM-DiI–la- labeling and analysis. beled neural tubes were left to develop for 4–5 mo (to S33, when Some embryos (n = 4) possessed CM-DiI–labeled cells within dermal denticles have differentiated within the trunk), at which tissue of the denticle pulp cavity, and some (n = 4) also possessed point, histological examination
Load more

Recommended publications
  • Barndoor Skate, Dipturus Laevis, Life History and Habitat Characteristics
    NOAA Technical Memorandum NMFS-NE-173 Essential Fish Habitat Source Document: Barndoor Skate, Dipturus laevis, Life History and Habitat Characteristics U. S. DEPARTMENT OF COMMERCE National Oceanic and Atmospheric Administration National Marine Fisheries Service Northeast Region Northeast Fisheries Science Center Woods Hole, Massachusetts March 2003 Recent Issues in This Series: 155. Food of Northwest Atlantic Fishes and Two Common Species of Squid. By Ray E. Bowman, Charles E. Stillwell, William L. Michaels, and Marvin D. Grosslein. January 2000. xiv + 138 p., 1 fig., 7 tables, 2 app. NTIS Access. No. PB2000-106735. 156. Proceedings of the Summer Flounder Aging Workshop, 1-2 February 1999, Woods Hole, Massachusetts. By George R. Bolz, James Patrick Monaghan, Jr., Kathy L. Lang, Randall W. Gregory, and Jay M. Burnett. May 2000. v + 15 p., 5 figs., 5 tables. NTIS Access. No. PB2000-107403. 157. Contaminant Levels in Muscle of Four Species of Recreational Fish from the New York Bight Apex. By Ashok D. Deshpande, Andrew F.J. Draxler, Vincent S. Zdanowicz, Mary E. Schrock, Anthony J. Paulson, Thomas W. Finneran, Beth L. Sharack, Kathy Corbo, Linda Arlen, Elizabeth A. Leimburg, Bruce W. Dockum, Robert A. Pikanowski, Brian May, and Lisa B. Rosman. June 2000. xxii + 99 p., 6 figs., 80 tables, 3 app., glossary. NTIS Access. No. PB2001-107346. 158. A Framework for Monitoring and Assessing Socioeconomics and Governance of Large Marine Ecosystems. By Jon G. Sutinen, editor, with contributors (listed alphabetically) Patricia Clay, Christopher L. Dyer, Steven F. Edwards, John Gates, Tom A. Grigalunas, Timothy Hennessey, Lawrence Juda, Andrew W. Kitts, Philip N.
    [Show full text]
  • Chondrichthyan Fishes (Sharks, Skates, Rays) Announcements
    Chondrichthyan Fishes (sharks, skates, rays) Announcements 1. Please review the syllabus for reading and lab information! 2. Please do the readings: for this week posted now. 3. Lab sections: 4. i) Dylan Wainwright, Thursday 2 - 4/5 pm ii) Kelsey Lucas, Friday 2 - 4/5 pm iii) Labs are in the Northwest Building basement (room B141) 4. Lab sections done: first lab this week on Thursday! 5. First lab reading: Agassiz fish story; lab will be a bit shorter 6. Office hours: we’ll set these later this week Please use the course web site: note the various modules Outline Lecture outline: -- Intro. to chondrichthyan phylogeny -- 6 key chondrichthyan defining traits (synapomorphies) -- 3 chondrichthyan behaviors -- Focus on several major groups and selected especially interesting ones 1) Holocephalans (chimaeras or ratfishes) 2) Elasmobranchii (sharks, skates, rays) 3) Batoids (skates, rays, and sawfish) 4) Sharks – several interesting groups Not remotely possible to discuss today all the interesting groups! Vertebrate tree – key ―fish‖ groups Today Chondrichthyan Fishes sharks Overview: 1. Mostly marine 2. ~ 1,200 species 518 species of sharks 650 species of rays 38 species of chimaeras Skates and rays 3. ~ 3 % of all ―fishes‖ 4. Internal skeleton made of cartilage 5. Three major groups 6. Tremendous diversity of behavior and structure and function Chimaeras Chondrichthyan Fishes: 6 key traits Synapomorphy 1: dentition; tooth replacement pattern • Teeth are not fused to jaws • New rows move up to replace old/lost teeth • Chondrichthyan teeth are
    [Show full text]
  • ESS 345 Ichthyology
    ESS 345 Ichthyology Evolutionary history of fishes 12 Feb 2019 (Who’s birthday?) Quote of the Day: We must, however, acknowledge, as it seems to me, that man with all his noble qualities... still bears in his bodily frame the indelible stamp of his lowly origin._______, (1809-1882) Evolution/radiation of fishes over time Era Cenozoic Fig 13.1 Fishes are the most primitive vertebrate and last common ancestor to all vertebrates They start the branch from all other living things with vertebrae and a cranium Chordata Notochord Dorsal hollow nerve cord Pharyngeal gill slits Postanal tail Urochordata Cephalochordata Craniates (mostly Vertebrata) Phylum Chordata sister is… Echinodermata Synapomorphy – They are deuterostomes Fish Evolutionary Tree – evolutionary innovations in vertebrate history Sarcopterygii Chondrichthyes Actinopterygii (fish) For extant fishes Osteichthyes Gnathostomata Handout Vertebrata Craniata Figure only from Berkeley.edu Hypothesis of fish (vert) origins Background 570 MYA – first large radiation of multicellular life – Fossils of the Burgess Shale – Called the Cambrian explosion Garstang Hypothesis 1928 Neoteny of sessile invertebrates Mistake that was “good” Mudpuppy First Vertebrates Vertebrates appear shortly after Cambrian explosion, 530 MYA – Conodonts Notochord replaced by segmented or partially segmented vertebrate and brain is enclosed in cranium Phylogenetic tree Echinoderms, et al. Other “inverts” Vertebrate phyla X Protostomes Deuterostomes Nephrozoa – bilateral animals First fishes were jawless appearing
    [Show full text]
  • An Introduction to the Classification of Elasmobranchs
    An introduction to the classification of elasmobranchs 17 Rekha J. Nair and P.U Zacharia Central Marine Fisheries Research Institute, Kochi-682 018 Introduction eyed, stomachless, deep-sea creatures that possess an upper jaw which is fused to its cranium (unlike in sharks). The term Elasmobranchs or chondrichthyans refers to the The great majority of the commercially important species of group of marine organisms with a skeleton made of cartilage. chondrichthyans are elasmobranchs. The latter are named They include sharks, skates, rays and chimaeras. These for their plated gills which communicate to the exterior by organisms are characterised by and differ from their sister 5–7 openings. In total, there are about 869+ extant species group of bony fishes in the characteristics like cartilaginous of elasmobranchs, with about 400+ of those being sharks skeleton, absence of swim bladders and presence of five and the rest skates and rays. Taxonomy is also perhaps to seven pairs of naked gill slits that are not covered by an infamously known for its constant, yet essential, revisions operculum. The chondrichthyans which are placed in Class of the relationships and identity of different organisms. Elasmobranchii are grouped into two main subdivisions Classification of elasmobranchs certainly does not evade this Holocephalii (Chimaeras or ratfishes and elephant fishes) process, and species are sometimes lumped in with other with three families and approximately 37 species inhabiting species, or renamed, or assigned to different families and deep cool waters; and the Elasmobranchii, which is a large, other taxonomic groupings. It is certain, however, that such diverse group (sharks, skates and rays) with representatives revisions will clarify our view of the taxonomy and phylogeny in all types of environments, from fresh waters to the bottom (evolutionary relationships) of elasmobranchs, leading to a of marine trenches and from polar regions to warm tropical better understanding of how these creatures evolved.
    [Show full text]
  • Florida's Fintastic Sharks and Rays Lesson and Activity Packet
    Florida's Fintastic Sharks and Rays An at-home lesson for grades 3-5 Produced by: This educational workbook was produced through the support of the Indian River Lagoon National Estuary Program. 1 What are sharks and rays? Believe it or not, they’re a type of fish! When you think “fish,” you probably picture a trout or tuna, but fishes come in all shapes and sizes. All fishes share the following key characteristics that classify them into this group: Fishes have the simplest of vertebrate hearts with only two chambers- one atrium and one ventricle. The spine in a fish runs down the middle of its back just like ours, making fish vertebrates. All fishes have skeletons, but not all fish skeletons are made out of bones. Some fishes have skeletons made out of cartilage, just like your nose and ears. Fishes are cold-blooded. Cold-blooded animals use their environment to warm up or cool down. Fins help fish swim. Fins come in pairs, like pectoral and pelvic fins or are singular, like caudal or anal fins. Later in this packet, we will look at the different types of fins that fishes have and some of the unique ways they are used. 2 Placoid Ctenoid Ganoid Cycloid Hard protective scales cover the skin of many fish species. Scales can act as “fingerprints” to help identify some fish species. There are several different scale types found in bony fishes, including cycloid (round), ganoid (rectangular or diamond), and ctenoid (scalloped). Cartilaginous fishes have dermal denticles (Placoid) that resemble tiny teeth on their skin.
    [Show full text]
  • Leucoraja Erinacea
    Little Skate − Leucoraja erinacea Overall Vulnerability Rank = Low Biological Sensitivity = Low Climate Exposure = High Data Quality = 88% of scores ≥ 2 Expert Data Expert Scores Plots Leucoraja erinacea Scores Quality (Portion by Category) Low Moderate Stock Status 2.0 2.8 High Other Stressors 1.5 1.4 Very High Population Growth Rate 2.9 2.4 Spawning Cycle 1.2 3.0 Complexity in Reproduction 1.3 2.2 Early Life History Requirements 1.1 3.0 Sensitivity to Ocean Acidification 1.5 2.8 Prey Specialization 1.2 3.0 Habitat Specialization 1.2 3.0 Sensitivity attributes Sensitivity to Temperature 2.1 3.0 Adult Mobility 2.3 2.2 Dispersal & Early Life History 1.9 2.8 Sensitivity Score Low Sea Surface Temperature 3.9 3.0 Variability in Sea Surface Temperature 1.0 3.0 Salinity 2.0 3.0 Variability Salinity 1.2 3.0 Air Temperature 1.0 3.0 Variability Air Temperature 1.0 3.0 Precipitation 1.0 3.0 Variability in Precipitation 1.0 3.0 Ocean Acidification 4.0 2.0 Exposure variables Variability in Ocean Acidification 1.0 2.2 Currents 2.1 1.0 Sea Level Rise 1.1 1.5 Exposure Score High Overall Vulnerability Rank Low Little Skate (Leucoraja erinacea) Overall Climate Vulnerability Rank: Low (88% certainty from bootstrap analysis). Climate Exposure: High. Two exposure factors contributed to this score: Ocean Surface Temperature (3.9) and Ocean Acidification (4.0). Little Skate are demersal and complete their life cycle in marine habitats. Biological Sensitivity: Low. Only one attribute scored above 2.5: Population Growth Rate (3.4).
    [Show full text]
  • Zootaxa, Marine Fish Diversity: History of Knowledge and Discovery
    Zootaxa 2525: 19–50 (2010) ISSN 1175-5326 (print edition) www.mapress.com/zootaxa/ Article ZOOTAXA Copyright © 2010 · Magnolia Press ISSN 1175-5334 (online edition) Marine fish diversity: history of knowledge and discovery (Pisces) WILLIAM N. ESCHMEYER1, 5, RONALD FRICKE2, JON D. FONG3 & DENNIS A. POLACK4 1Curator emeritus, California Academy of Sciences, San Francisco, California, U.S.A. 94118 and Research Associate, Florida Museum of Natural History, Gainesville, Florida, U.S.A. 32611. E-mail: [email protected] 2Ichthyology, Staatliches Museum für Naturkunde, Rosenstein 1, 70191 Stuttgart, Germany. E-mail: [email protected] 3California Academy of Sciences, San Francisco, California, U.S.A. 94118. E-mail: [email protected] 4P.O. Box 518, Halfway House 1685, South Africa. E-mail: [email protected] 5Corresponding Author. E-mail: [email protected] Abstract The increase in knowledge of marine fish biodiversity over the last 250 years is assessed. The Catalog of Fishes database (http://research.calacademy.org/ichthyology/catalog) on which this study is based, has been maintained for 25 years and includes information on more than 50,000 available species names of fishes, with more than 31,000 of them currently regarded as valid species. New marine species are being described at a rate of about 100–150 per year, with freshwater numbers slightly higher. In addition, over 10,000 generic names are available ones of which 3,118 are deemed valid for marine fishes (as of Feb. 19, 2010). This report concentrates on fishes with at least some stage of their life cycle in the sea. The number of valid marine species, about 16,764 (Feb.
    [Show full text]
  • Modeling the Ventilatory Behavior of the Embryos Of
    VASSAR COLLEGE | UNDERGRADUATE RESEARCH SUMMER INSTITUTE (URSI) SYMPOSIUM | 2020 MODELING THE VENTILATORY BEHAVIOR OF THE EMBRYOS OF LITTLE SKATES Connor McShaffrey (‘21, Cognitive Science) and John Long (Biology, Cognitive Science, Neuroscience & Behavior) retract freeze recoil retract freeze recoil retract recoil ventilate pulsate (L) select & pulsate ventilate return to enter tendril search ventilate & enter front- search return to faced & enter tendril Stages 30-31 Stages 31-32 Stages 32-33 Pulsate: Gradual, slow undulation without insertion. Ventilate (L): Ventilate with the body bent laterally at the base of Ventilate Front-Faced: Ventilate with the body bent sharply Search & Enter: Rapid undulation down to tail tip to the putative adult caudal fin. at the caudal fin so that the tail tip is looped back over the find and insert into a tendril. Return to Tendril: After a full recoil, return to the same tendril anterior portion of the body disk.. Ventilate: High frequency undulation within a tendril. that was being ventilated. Select & Enter: Search & Enter, but with greater efficiency Retract : An incremental pull-back from tendril relative Freeze: Upon partial disturbance during ventilation, stop of selection and insertion. to sensitivity, amplitude, and frequency. moving and wait before ventilating or moving out of the Recoil: Upon sufficient disturbance, pull the tail back tendril. to coil it around the body. ● Embryos of elasmobranch fishes (skates and some sharks) develop for up to a year in a leathery egg case, the mermaid’s purse. ● An embryo must ventilate by undulating its tail inside one of the four hollow tendrils (or horns) of the capsule to exchange deoxygenated for oxygenated water.
    [Show full text]
  • Leucoraja Naevus from Portuguese Continental Waters
    Universidade do Algarve Faculdade de Ciências e Tecnologia Reproductive biology of the species Leucoraja naevus from Portuguese continental waters Catarina Maia Master thesis submitted for the partial fulfillment of the title of Master of Marine Biology 2010 Universidade do Algarve Faculdade de Ciências e Tecnologia Reproductive biology of the species Leucoraja naevus from Portuguese continental waters Catarina Maia Master thesis submitted for the partial fulfillment of the title of Master of Marine Biology Internal supervisor: Prof. Dr. Karim Erzini External supervisor: Profa. Dra. Ivone Figueiredo 2010 Acknowledgements I would like to thank everyone who helped me in IPIMAR and University: First I would like to thank Dr. Ivone Figueiredo and Dr. Karim Erzini for the opportunity to perform this work and the availability and encouragement shown over the same; I would also like to express my immense gratitude to Dr. Barbara Serra-Pereira for the help, encouragement and support (tireless!!!!) that greatly facilitated my work; My sincere thanks to José do Lago and Neide Lagarto for their help in sampling and friendship; As Teresa, Ana Rita and Inês, Miguel and Nuno, who not only gave me the motivation but also by the availability and friendship shown. I also thank to all IPIMAR workers, including Carmo and Cristrina for their help and suggestions in histology; Tanks to PNAB that partially supported my work; My eternal gratitude to my parents and Francisco who were always by my side and supported me unconditionally. Abstract Skate populations tend to be highly vulnerable to exploitation as a result of the main life history characteristics (slow growth, late maturity and low fecundity).
    [Show full text]
  • Paleogene Origin of Planktivory in the Batoidea
    Paleogene Origin Of Planktivory In The Batoidea CHARLIE J. UNDERWOOD, 1+ MATTHEW A. KOLMANN, 2 and DAVID J. WARD 3 1Department of Earth and Planetary Sciences, Birkbeck, University of London, UK, [email protected]; 2 Department of Ecology and Evolutionary Biology, University of Toronto, Canada, [email protected]; 3Department of Earth Sciences, Natural History Museum, London, UK, [email protected] +Corresponding author RH: UNDERWOOD ET AL.—ORIGIN OF PLANKTIVOROUS BATOIDS 1 ABSTRACT—The planktivorous mobulid rays are a sister group to, and descended from, rhinopterid and myliobatid rays which possess a dentition showing adaptations consistent with a specialized durophageous diet. Within the Paleocene and Eocene there are several taxa which display dentitions apparently transitional between these extreme trophic modality, in particular the genus Burnhamia. The holotype of Burnhamia daviesi was studied through X-ray computed tomography (CT) scanning. Digital renderings of this incomplete but articulated jaw and dentition revealed previously unrecognized characters regarding the jaw cartilages and teeth. In addition, the genus Sulcidens gen. nov. is erected for articulated dentitions from the Paleocene previously assigned to Myliobatis. Phylogenetic analyses confirm Burnhamia as a sister taxon to the mobulids, and the Mobulidae as a sister group to Rhinoptera. Shared dental characters between Burnhamia and Sulcidens likely represent independent origins of planktivory within the rhinopterid – myliobatid clade. The transition from highly-specialized durophagous feeding morphologies to the morphology of planktivores is perplexing, but was facilitated by a pelagic swimming mode in these rays and we propose through subsequent transition from either meiofauna-feeding or pelagic fish-feeding to pelagic planktivory.
    [Show full text]
  • Evaluating the Potential for Grey Seal Predation to Explain Elevated Natural Mortality in Three Fish Species in the Southern Gulf of St
    Vol. 442: 149–167, 2011 MARINE ECOLOGY PROGRESS SERIES Published December 5 doi: 10.3354/meps09454 Mar Ecol Prog Ser Evaluating the potential for grey seal predation to explain elevated natural mortality in three fish species in the southern Gulf of St. Lawrence Hugues P. Benoît1,*, Douglas P. Swain1, W. Don Bowen2, Greg A. Breed3, Mike O. Hammill4, Valerie Harvey4 1Gulf Fisheries Centre, Fisheries and Oceans Canada, Moncton, New Brunswick E1C 9B6, Canada 2Bedford Institute of Oceanography, Fisheries and Oceans Canada, Dartmouth, Nova Scotia B2Y 4A2, Canada 3Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4J1, Canada 4Institut Maurice Lamontagne, Fisheries and Oceans Canada, Mont-Joli, Quebec G5H 3Z4, Canada ABSTRACT: Despite 2 decades of very low fishing levels, numerous NW Atlantic demersal fish stocks have failed to recover from collapsed states or are presently collapsing. In the southern Gulf of St. Lawrence, adult natural mortality (M) appears to be the demographic rate that most limits population productivity in at least 3 species: Atlantic cod Gadus morhua, white hake Urophycis tenuis and winter skate Leucoraja ocellata. The causes of elevated M are not well understood, though there is indirect evidence consistent with an effect of predation by grey seals Halichoerus grypus. However, direct evidence is lacking due to uncertainty in the seal diet. Consequently, Monte Carlo simulations were undertaken using data on the spatial overlap between the seals and the fishes and a seal food-consumption model, to estimate the plausibility that different seal-diet compositions could explain observed M levels. Under the simulation assumptions, we find that predation could explain up to 20 to 50% of M in adult white hake and cod even if these species comprise a small percentage of grey seal diets (<25%).
    [Show full text]
  • Rays and Skates (Batoidea) Conservation Profile Synopsis
    Rays and Skates (Batoidea) Conservation Profile Synopsis Status of Ray and Skate Populations IUCN Red List Total Species CR EN VU NT LC DD State of the Batoidea Superorder 539 14 28 65 62 114 256 Rays and skates belong to the Batoidea Superorder and consist of stingrays CR, Critically Endangered; EN, Endangered; VU, and related species (Order Myliobatiforme, 223 species), electric rays (Order Vulnerable; NT, Near Threatened; LC, Least Torpediniforme, 69 species), skates and related species (Order Rajiforme, Concern; DD, Data Deficient. 270 species), and sawfish (Order Pristiforme, 5-7 species). Most batoid species live on the sea floor and are found in a variety of ecosystems across CITES the planet: coastal, deep water (3,000 m), tropical, subtropical, temperate, Appendix 1:7 species cold-water, estuarine, marine, freshwater, and open seas. As opportunistic foragers in complex trophic webs, batoids can impact and alter ecosystems if Appendix II: 1 species 1,2 other top-predators are removed . AZA Subpopulation Several batoids are listed as endangered in US-waters for which smalltooth Marine Fishes Taxon Advisory Group sawfish have a designated critical habitat and recovery plan as of 2009. There Chair Beth Firchau is a high degree of uncertainty with respect to the status of ray and skate populations at the global level even though they are some of the world’s most vulnerable marine fishes3. Many populations are extinct, and many more are critically endangered particularly in coastal ecosystems. Primary Threats to the Species Batoids face extinction risks due to a variety of threats that include capture in nets from targeted and accidental catch.
    [Show full text]