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Feeding in the Devonian antiarch placoderm fishes: a study based upon morphofunctional analysis of jaws

Published online by Cambridge University Press:  14 July 2022

Oleg A. Lebedev Open the ORCID record for Oleg A. Lebedev [Opens in a new window] ,
Zerina Johanson ,
Alexander N. Kuznetsov ,
Alekey Tsessarsky ,
Kate Trinajstic  and
Farkhad B. Isakhodzayev Open the ORCID record for Farkhad B. Isakhodzayev [Opens in a new window]
Oleg A. Lebedev
Affiliation:
A.A. Borissiak Palaeontological Institute of the Russian Academy of Sciences, Moscow 117997, Russia
Zerina Johanson*
Affiliation:
Natural History Museum, London UK SW7 5BD, United Kingdom
Alexander N. Kuznetsov
Affiliation:
A.A. Borissiak Palaeontological Institute of the Russian Academy of Sciences, Moscow 117997, Russia
Alekey Tsessarsky
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, Moscow 119071, Russia
Kate Trinajstic
Affiliation:
School of Molecular and Life Sciences, Curtin University, Perth, WA, Australia
Farkhad B. Isakhodzayev
Affiliation:
All-Russian Scientific Research Geological Petroleum Institute, Aprelevka, Moscow Region 143360, Russia
*
*Corresponding author.
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Abstract

Antiarch placoderm fishes were an abundant component of the Middle Paleozoic vertebrate assemblages. Despite a large number of known taxa and specimens, the morphology and function of the skeletal elements of their jaws is inadequately known. Because of this, questions regarding their feeding modes and their roles in the trophic webs remain open. We present a skeletomuscular model of the antiarch jaw apparatus with an attempt to reconstruct its potential biomechanical function. The position of the upper jaw suborbital bones within the plane of the ventral side of the fish armor is suggested to represent the natural “mouth closed” position. During mouth opening, the suborbitals rotated rostrally with simultaneous depression and inward rotation of the infragnathals. The ball-and-socket jaw articulation might ensure this combined movement. Recently described lower jaw elements of Livnolepis zadonica (Obrucheva, 1983) and Bothriolepis sp. from the Upper Devonian (lower Famennian) of Central Russia demonstrating very deep and porous blades of the oral division of the infragnathals queried the structure of these bones in other antiarchs. Observed porosity reflects intense vascularization to supply blood to a connective tissue underlying a supposed keratinous sheath, which protected and strengthened the jaws, as well as made possible scraping tough food objects, such as thallus algae, from the substrate.

Having evolved during the Silurian in the Pan-Cathaysian zoogeographical province, antiarchs migrated to Gondwana during the Emsian and later to Euramerica during the Eifelian. Supposedly, antiarchs became the first macrophytophagous vertebrates occupying the trophic level of primary consumers during the late Silurian–Early Devonian. This event diversified the only previously existing predator–prey interrelationships between filter-feeding agnathans and predatory gnathostomes.

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Journal of Paleontology , Volume 96 , Issue 6 , November 2022 , pp. 1413 - 1430
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Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of The Paleontological Society

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References

Agrawal, N., and Mittal, A.K., 1992, Structural organization and histochemistry of the epithelia of the lips and associated structures of a common Indian carp, Cirrhina mrigala: Canadian Journal of Zoology, v. 70, p. 71–78.CrossRefGoogle Scholar
Béchard, I., Arsenault, F., Cloutier, R., and Kerr, J., 2014, The Devonian placoderm fish Bothriolepis canadensis revisited with three-dimensional digital imagery: Palaeontologia Electronica, v. 17.1.2A, 19 p., https://doi.org/10.26879/417Google Scholar
Bonacci, A., Brunelli, E., Sperone, E., and Tripepi, S., 2008, The oral apparatus of tadpoles of Rana dalmatina, Bombina variegata, Bufo, and Bufo viridis (Anura): Zoologischer Anzeiger-A Journal of Comparative Zoology, v. 247, p. 47–54.CrossRefGoogle Scholar
Boulenger, G.A., 1896, Descriptions of new batrachians in the British Museum: Annals and Magazine of Natural History, ser. 6, v. 17, p. 401–406.CrossRefGoogle Scholar
Candioti, M.F.V., 2007, Anatomy of anuran tadpoles from lentic water bodies: systematic relevance and correlation with feeding habits: Zootaxa, v. 1600, 175 p.Google Scholar
Cloutier, R., 2013, Great Canadian Lagerstätten 4. The Devonian Miguasha biota (Quebec): an UNESCO World Heritage, a time capsule in the early history of vertebrates: Geoscience Canada, v. 40, p. 149–163.CrossRefGoogle Scholar
Cloutier, R., Proust, J.N., and Tessier, B., 2011, The Miguasha Fossil-Fish-Lagerstätte: a consequence of the Devonian land–sea interactions: Palaeobiodiversity and Palaeoenvironments, v. 91, p. 293–323.CrossRefGoogle Scholar
Davit-Béal, T., Tucker, A.S., and Sire, J.Y., 2009, Loss of teeth and enamel in tetrapods: fossil record, genetic data and morphological adaptations: Journal of Anatomy, v. 214, p. 477–501.CrossRefGoogle ScholarPubMed
Denison, R.H., 1941, The soft anatomy of Bothriolepis: Journal of Paleontology, v. 15, p. 553–561.Google Scholar
Denison, R.H., 1961, Feeding mechanisms of Agnatha and early gnathostomes: American Zoologist, v. 1, p. 177–181.CrossRefGoogle Scholar
de Jongh, H.J., 1968, Functional morphology of the jaw apparatus of larval and metamorphosing Rana temporaria L: Netherlands Journal of Zoology, v. 18, 103 p.Google Scholar
Eichwald, E., 1840, Die Tier- und Pflanzenreste des alten roten Sandsteins und Bergkalks im Nowgorodschen Gouvernement: Saint Petersburg Academy Imperial of Sciences, Bulletin of Sciences, v. 7, p. 78–91.Google Scholar
Frey, L., Coates, M.I., Tietjen, K., Rücklin, M., and Klug, C., 2020, A symmoriiform from the Late Devonian of Morocco demonstrates a derived jaw function in ancient chondrichthyans: Communications Biology, v. 3, n. 681, https://doi.org/10.1038/s42003-020-01394-2CrossRefGoogle ScholarPubMed
Grassé, P.-P., 1958, Peau, in Grasse, P.-P., ed., Traité de Zoologie. Anatomie, Systématique, Biologie. Tome XIII. Agnathes et Poissons: Anatomie, Éthologie, Systématique, 3 fasc., p. 2606.Google Scholar
Gray, J.E., 1844, Catalogue of Tortoises, Crocodilians, and Amphisbaenians in the Collection of the British Museum: London, British Museum (Natural History), viii + 80 p.Google Scholar
Gross, W., 1933, Die Fische des Baltischen Devons: Palaeontographica Abteilung A, v. 79, p. 1–74.Google Scholar
Gross, W., 1941, Die Bothriolepis-Arten der Cellulosa-Mergel Lettlands: Kungliga Svenska Vetenskaps-akademiens Handlingar, v. 19, no. 5, p. 1–79.Google Scholar
Haas, A., Pohlmeyer, J., McLeod, D.S., Kleinteich, T., Hertwig, S.T., Das, I., and Buchholz, D.R., 2014, Extreme tadpoles II: the highly derived larval anatomy of Occidozyga baluensis (Boulenger, 1896), an obligate carnivorous tadpole: Zoomorphology, v. 133, p. 321–342.CrossRefGoogle Scholar
Hamilton, F., 1822, An Account of Fishes Found in the River Ganges and Its Branches: Edinburgh, Hurst, Robinson, and Company, p. 312–389.Google Scholar
Hemmings, S.K., 1978, The Old Red Sandstone antiarchs of Scotland: Pterichthyodes and Microbrachius: Palaeontographical Society Monographs, v. 131, 64 p.Google Scholar
Janvier, P., 2008, Early jawless vertebrates and cyclostome origins: Zoological Science, v. 25, p. 1045–1056.CrossRefGoogle ScholarPubMed
Jarvik, E., 1980, Basic Structure and Evolution of Vertebrates, Volume 1, 2: London, Academic Press, 575 p.Google Scholar
Jessen, H., 1972, Schultergürtel und Pectoralflosse bei Actinopterygiern: Fossils and Strata, v. 1, p. 1–101.Google Scholar
Johanson, Z., 1995, New information on jaw elements of Remigolepis (Placodermi; Antiarchi) from Canowindra, NSW, Australia (Upper Devonian): Geobios, v. 28, p. 103–107.CrossRefGoogle Scholar
Johanson, Z., 1997, New Remigolepis (Placodermi; Antiarchi) from Canowindra, New South Wales, Australia: Geological Magazine, v. 134, p. 813–846.CrossRefGoogle Scholar
Johanson, Z., 1998, The Upper Devonian fish Bothriolepis (Placodermi: Antiarchi) from near Canowindra, New South Wales, Australia: Records of the Australian Museum, v. 50, p. 315–348.CrossRefGoogle Scholar
Keyserling, A., 1846, Wissenschaftliche Beobachtungen auf einer Reise in das Petschora-Land: Saint-Petersburg, Buchdruckerei der Kaiserlische Akademia der Wissenschaften, 106 p.Google Scholar
Kimura, Y., and Nikaido, M., 2021, Conserved keratin gene clusters in ancient fish: an evolutionary seed for terrestrial adaptation: Genomics, v. 113, p. 1120–1128.CrossRefGoogle Scholar
Lebedev, O.A., and Zakharenko, G.V., 2010, Global vertebrate-based palaeozoogeographical subdivision for the Givetian–Famennian (Middle–Late Devonian): endemism–cosmopolitanism spectrum as an indicator of interprovincial faunal exchanges: Palaeoworld, v. 19, p. 186–205.CrossRefGoogle Scholar
Linnaeus, C., 1758, Systema Naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis, Volume 1 (10th revised edition): Holmiae, Laurentius Salvius, 824 p.Google Scholar
Louchart, A., and Viriot, L., 2011, From snout to beak: the loss of teeth in birds: Trends in Ecology and Evolution, v. 26, p. 663–673.CrossRefGoogle ScholarPubMed
Lukševičs, E., 2001, Bothriolepid antiarchs (Vertebrata, Placodermi) from the Devonian of the north-western part of the East European Platform: Geodiversitas, v. 23, p. 489–609.Google Scholar
Lyarskaya, L.A., 1981, Fossil Fishes from the Devonian of the Baltic Region: Asterolepididae: Riga, Zinatne, 51 p. [in Russian]Google Scholar
Lyovin, B.A., 2007, Convergence and phonetic analogies in the scrapers of the family Cyprinidae (Osteichthyes), in Rubtsov, A.S., and Samokhina, I.Yu., eds., Modern Problems of Biological Evolution: Conference Materials. Dedicated to the 100th anniversary of the State Darwin Museum. September 17–20, 2007, Moscow: Moscow, SDM Publishing, p. 51–53. [in Russian]Google Scholar
Mallatt, J., 1996, Ventilation and the origin of jawed vertebrates: a new mouth: Zoological Journal of the Linnean Society, v. 117, p. 329–404.Google Scholar
Martens, T., 1996, Conchostraca (Phyllopoda, Crustacea) from the Escuminac Formation, in Schultze, H.-P., and Cloutier, R., eds., Devonian Fishes and Plants of Miguasha, Quebec, Canada: Munich, Verlag Dr. Friedrich Pfeil, p. 112–113.Google Scholar
Miller, H. 1841, The Old Red Sandstone or new walks in an old field: Edinburgh, John Johnstone, 275 pp.Google Scholar
Moloshnikov, S., 2004, Crested antiarch Bothriolepis zadonica H.D. Obrucheva from the lower Famennian of Central European Russia: Acta Palaeontologica Polonica, v. 49, p. 135–146.Google Scholar
Moloshnikov, S.V., 2008, Devonian antiarchs (Pisces, Antiarchi) from central and southern European Russia: Paleontological Journal, v. 42, p. 691–773.CrossRefGoogle Scholar
Nilsson, T., 1941, The Downtonian and Devonian vertebrates of Spitsbergen. VII. Order Antiarchi: Skrifter om Svalbard og Ishavet, v. 82, p. 1–54.Google Scholar
Obrucheva, H.D., 1983, A new bothriolepid species from the Zadonskian Regional Stage of the Central Devonian Field, in Novitskaya, L.I., ed., Problems of Modern Paleoichthyology: Materials of the Conference Dedicated to D.V. Obruchev, Moscow, Nauka, p. 36–42.Google Scholar
Pander, Ch., 1857, Über die Placodermen des devonischen Systems: St. Petersburg, Kaiserlichen Akademie des Wissenschaften, 106 p.Google Scholar
Patten, W., 1904, New facts concerning Bothriolepis: The Biological Bulletin, v. 7, p. 113–124.CrossRefGoogle Scholar
Pinky, M., Mittal, S., Yashpal, M., Ojha, J., Mittal, A.K., 2004, Occurrence of keratinization in the structures associated with lips of a hill stream fish Garra lamta (Hamilton) (Cyprinidae, Cypriniformes): Journal of Fish Biology, v. 65, p. 1165–1172.CrossRefGoogle Scholar
Qi, D., Chao, Y., Guo, S., Zhao, L., Li, T., Wei, F., Zhao, X., 2012, Convergent, parallel and correlated evolution of trophic morphologies in the subfamily Schizothoracinae from the Qinghai–Tibetan Plateau: PLoS ONE, v. 7, n. e34070, https://doi.org/10.1371/journal.pone.0034070CrossRefGoogle ScholarPubMed
Romer, A.S., and Grove, B.H., 1935, Environment of the early vertebrates: American Midland Naturalist, v. 16, p. 805–856.CrossRefGoogle Scholar
Rücklin, M., Donoghue, P.C., Johanson, Z., Trinajstic, K., Marone, F., and Stampanoni, M., 2012, Development of teeth and jaws in the earliest jawed vertebrates: Nature, v. 491, p. 748–751.CrossRefGoogle ScholarPubMed
Schweigger, A.F., 1812, Prodromus Monographia Cheloniorum auctore Schweigger: Königsberg, Archiv Naturwissenschaften Mathematik, p. 271–368, 406–458.Google Scholar
Sobolev, N.N., and Evdokimova, I.O., 2008, Devonian System, in Zhamoida, A.I., and Petrov, O.V., eds., State of Knowledge of Precambrian and Phanerozoic Stratigraphy in Russia. Aims for Further Studies: Decisions of the Interdepartmental Stratigraphic Committee and its Permanent Commissions, v. 38, p. 52–60. [in Russian]Google Scholar
Stensiö, E.A., 1931, Upper Devonian vertebrates from East Greenland, collected by the Danish Greenland expedition in, 1929 and, 1930: Meddelelser øm Grønland, v. 86, p. 3–213.Google Scholar
Stensiö, E.A., 1948, On the Placodermi of the Upper Devonian of East Greenland. II: Antiarchi: subfamily Bothriolepinae: Palaeozoologica Groenlandica, v. 2, 622 p.Google Scholar
Stensiö, E.A., 1969, Elasmobranchiomorphi Placodermata Arthrodires, in Piveteau, J., ed., Traité de Paléontologie, Volume 4: Paris, Masson, p. 71–692.Google Scholar
Traquair, R.H., 1888, Article: LXIV.—On the structure and classification of the Asterolepidae: The Annals and Magazine of Natural History, ser. 6, v. 2, no. 7–12, p. 485–504.CrossRefGoogle Scholar
Traquair, R.H., 1893, Achanarras revisited: Proceedings of the Royal Philosophical Society of Edinburgh, v. 11, p. 283–286.Google Scholar
Traquair, R.H., 1894, A monograph of the fishes of the Old Red Sandstone of Britain. Part II, No. 1. The Asterolepidae: Monographs of the Palaeontographical Society, v. 48, p. 63–90.CrossRefGoogle Scholar
Tridico, S.R., Rigby, P., Kirkbride, K.P., Haile, J., and Bunce, M., 2014, Megafaunal split ends: microscopical characterisation of hair structure and function in extinct woolly mammoth and woolly rhino: Quaternary Science Reviews, v. 83, p. 68–75.CrossRefGoogle Scholar
Tripathi, P., and Mittal, A.K., 2010, Essence of keratin in lips and associated structures of a freshwater fish Puntius sophore in relation to its feeding ecology: histochemistry and scanning electron microscope investigation: Tissue and Cell, v. 42, p. 223–233.Google ScholarPubMed
Upeniece, I., 2001, The unique fossil assemblage from the Lode quarry (Upper Devonian, Latvia): Fossil Record, v. 4, p. 101–119.CrossRefGoogle Scholar
Upeniece, I., 2011, Paleoecology and juvenile individuals of the Devonian placoderm and acanthodian fishes from Lode Site, Latvia [Ph.D. dissertation]: Riga, University of Latvia, 221 p.Google Scholar
Venesky, M.D., Wassersug, R.J., Jorgensen, M.E., Riddle, M., and Parris, M.J., 2011, Comparative feeding kinematics of temperate pond-dwelling tadpoles (Anura, Amphibia): Zoomorphology, v. 130, p. 31–38.CrossRefGoogle Scholar
Vostradovsky, J., 1973, Freshwater Fishes: London, The Hamlyn Publishing Group, 252 p.Google Scholar
Wang, Y., and Zhu, M., 2018, Redescription of Phymolepis cuifengshanensis (Antiarcha: Yunnanolepididae) using high-resolution computed tomography and new insights into anatomical details of the endocranium in antiarchs: PeerJ, v. 6, n. e4808, https://doi.org/10.7717/peerj.4808CrossRefGoogle ScholarPubMed
Wang, Y., and Zhu, M., 2021, New data on the headshield of Parayunnanolepis xitunensis (Placodermi, Antiarcha), with comments on nasal capsules in antiarchs: Journal of Vertebrate Paleontology, v. 40, n. e1855189, https://doi.org/10.1080/02724634.2020.1855189CrossRefGoogle Scholar
Watson, D.M.S., 1961, Some additions to our knowledge of antiarchs: Palaeontology, v. 4, p. 210–220.Google Scholar
Whiteaves, J.F., 1880, On a new species of Pterichthys, allied to Bothriolepis ornata, from the Devonian rocks of the north side of the Baie des Chaleurs: American Journal of Science, v. 3, p. 132–136.CrossRefGoogle Scholar
Whiteaves, J.F., 1887, Illustrations of the fossil fishes of the Devonian rocks of Canada. Part I: Transactions of the Royal Society of Canada, v. 4, p. 101–110.Google Scholar
Woodward, A.S., 1891, The Devonian fish-fauna of Spitsbergen: Annual Magazine of Natural History, v. 8, no. 43, p. 1–15.CrossRefGoogle Scholar
Woodward, A.S., 1892, Further contributions to knowledge of the Devonian fish fauna of Canada: Geological Magazine, v. 9, p. 481–485.CrossRefGoogle Scholar
Young, G.C., 1984, Reconstruction of the jaws and braincase in the Devonian placoderm fish Bothriolepis: Palaeontology, v. 27, p. 635–661.Google Scholar
Young, G.C., 1990, New antiarchs (Devonian placoderm fishes) from Queensland, with comments on placoderm phylogeny and biogeography: Memoirs of the Queensland Museum, v. 28, p. 35–50.Google Scholar
Young, G.C., 2008, The relationships of antiarchs (Devonian placoderm fishes)—evidence supporting placoderm monophyly: Journal of Vertebrate Paleontology, v. 28, p. 626–636.CrossRefGoogle Scholar
Young, G.C., 2010, Placoderms (armored fish): dominant vertebrates of the Devonian period: Annual Review of Earth and Planetary Sciences, v. 38, p. 523–550.CrossRefGoogle Scholar
Young, G.C., and Zhang, G., 1996, New information on the morphology of yunnanolepid antiarchs (placoderm fishes) from the Early Devonian of South China: Journal of Vertebrate Paleontology, v. 16, p. 623–641.CrossRefGoogle Scholar
Young, G.C., Burrow, C.J., Long, J.A., Turner, S., and Choo, B., 2010, Devonian macrovertebrate assemblages and biogeography of East Gondwana (Australasia, Antarctica): Palaeoworld, v. 19, p. 55–74.CrossRefGoogle Scholar
Zhang, G.-R., 1978, The antiarchs from the Early Devonian of Yunnan: Vertebrata Palasiatica, v. 16, p. 147–186. [in Chinese with English summary]Google Scholar
Zhang, G.-R., Wang, J.-Q., and Wang, N.-Zh., 2001, The structure of pectoral fin and tail in Yunnanolepidoidei, with a discussion of the pectoral fin of chuchinolepids: Vertebrata Palasiatica, v. 39, p. 1–13. [in Chinese with English summary]Google Scholar
Zhao, W.J., and Zhu, M., 2010, Siluro-Devonian vertebrate biostratigraphy and biogeography of China: Palaeoworld, v. 19, p. 4–26.CrossRefGoogle Scholar
Zhu, M., 1996, The phylogeny of Antiarcha (Placodermi, Pisces), with the description of Early Devonian antiarchs from Qujing, Yunnan, China: Bulletin de la Muséum National d'Histoire Naturelle, ser. 4, v. 18, p. 233–347.Google Scholar
Zhu, Y.A., Giles, S., Young, G.C., Hu, Y., Bazzi, M., Ahlberg, P.E., Zhu, M., and Lu, J., 2021, Endocast and bony labyrinth of a Devonian “placoderm” challenges stem gnathostome phylogeny: Current Biology v. 31, p. 1112–1118.CrossRefGoogle ScholarPubMed