Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-24T10:35:43.985Z Has data issue: false hasContentIssue false

Multicuspid tooth morphology in a gigantic Palaeocene pycnodont fish: evolutionary and palaeoecological significance

Published online by Cambridge University Press:  08 July 2019

Romain Vullo*
Affiliation:
Univ Rennes, CNRS, Géosciences Rennes, UMR 6118, 35000 Rennes, France
Nathalie Bardet
Affiliation:
CR2P, UMR 7207, MNHN–CNRS–Sorbonne Université, Muséum National d’Histoire Naturelle, CP38, 75005 Paris, France
Emmanuel Gheerbrant
Affiliation:
CR2P, UMR 7207, MNHN–CNRS–Sorbonne Université, Muséum National d’Histoire Naturelle, CP38, 75005 Paris, France
Nour-Eddine Jalil
Affiliation:
CR2P, UMR 7207, MNHN–CNRS–Sorbonne Université, Muséum National d’Histoire Naturelle, CP38, 75005 Paris, France BioDEcos, Department of Geology, FSSM–UCAM, BP2390, Marrakesh, Morocco
*
Author for correspondence: Romain Vullo, Email: [email protected]

Abstract

A pycnodont premaxilla bearing a large incisiform tooth with an unusual crown morphology is described from the Palaeocene (Thanetian) phosphate deposits of Morocco. This peculiar tooth shows a broad, fan-shaped multicuspid crown with nine cusps, well adapted for benthic macroalgal scraping. This morph, assigned to a new species of Pycnodus (P. multicuspidatus sp. nov.), emphasizes the phenotypic plasticity of the group and documents an additional trophic specialization among Palaeogene pycnodontiform fishes. In the post-K/Pg boundary marine ecosystem of the Ouled Abdoun Basin, P. multicuspidatus sp. nov. may have opportunistically replaced Maastrichtian fish taxa with a similar front dentition and feeding behaviour, such as the putative specialized pycnodontiforms Stephanodus and Hadrodus.

Type
Rapid Communication
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agassiz, L (1833) Tableau synoptique des familles, des genres et des espèces de l’ordre des Ganoïdes. In Recherches sur les Poissons Fossiles. 1st ‘Livraison’, Vol. 2, Part I, pp. 148. Neuchâtel: Petitpierre.CrossRefGoogle Scholar
Albertson, RC, Streelman, JT and Kocher, TD (2003a) Genetic basis of adaptive shape differences in the cichlid head. Journal of Heredity 94, 291301.CrossRefGoogle ScholarPubMed
Albertson, RC, Streelman, JT and Kocher, TD (2003b) Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes. Proceedings of the National Academy of Sciences of the USA 100, 5252–7.CrossRefGoogle ScholarPubMed
Arambourg, C (1952) Les vertébrés fossiles des gisements de phosphates (Maroc – Algérie – Tunisie). Service Géologique du Maroc, Notes et Mémoires 92, 1372.Google Scholar
Arambourg, C (1964) Sur la présence d’un poisson du genre Hadrodus dans les phosphates maestrichtiens du Maroc: H. belinkoi nov. sp. Compte Rendu Sommaire des Séances de la Société Géologique de France 1964, 318–19.Google Scholar
Atukorala, ADS and Franz-Odendaal, TM (2014) Spatial and temporal events in tooth development of Astyanax mexicanus . Mechanisms of Development 134, 4254.CrossRefGoogle ScholarPubMed
Bardet, N, Gheerbrant, E, Noubhani, A, Cappetta, H, Jouve, S, Bourdon, E, Pereda Suberbiola, X, Jalil, N-E, Vincent, P, Houssaye, A, Solé, F, Elhoussaini Darif, K, Adnet, S, Rage, J-C, Lapparent de Broin, FD, Sudre, J, Bouya, B, Amaghzaz, M and Meslouh, S (2017) Les vertébrés des phosphates crétacés–paléogènes (72,1–47,8 Ma) du Maroc. Mémoires de la Société Géologique de France 180, 351452.Google Scholar
Bell, GL (1986) A pycnodont fish from the Upper Cretaceous of Alabama. Journal of Paleontology 60, 1120–6.CrossRefGoogle Scholar
Berg, LS (1937) A classification of fish-like vertebrates. Bulletin de l’Académie des Sciences de l’URSS, Classe des Sciences Mathématiques et Naturelles (série biologique) 4, 1277–80.Google Scholar
Capasso, L (2000) Tergestinia sorbinii gen. nov., sp. nov., del Paleocene inferiore di Trebiciano, Trieste (Pisces, Pycnodontiformes). Atti del Museo Civico di Storia Naturale di Trieste 48, 261–89.Google Scholar
Cappetta, H (1972) Les poissons crétacés et tertiaires du Bassin des Iullemmeden (République du Niger). Palaeovertebrata 5, 179251.Google Scholar
Cawley, JJ, Marramà, G, Carnevale, G and Kriwet, J (2018) A quantitative approach to determine the taxonomic identity and ontogeny of the pycnodontiform fish Pycnodus (Neopterygii, Actinopterygii) from the Eocene of Bolca Lagerstätte, Italy. PeerJ 6, e4809. doi: 10.7717/peerj.4809.CrossRefGoogle ScholarPubMed
Cope, ED (1887) Zittel’s Manual of Palaeontology. American Naturalist 21, 1014–19.Google Scholar
Dames, W (1883) Ueber Ancistrodon Debey. Deutschen Geologischen Gesellschaft 4, 655–70.Google Scholar
Dartevelle, E and Casier, E (1949) Les poissons fossiles du Bas-Congo et des régions voisines (deuxième partie). Annales du Musée du Congo Belge A, série 3 2, 201–56.Google Scholar
Davis, AM, Unmack, PJ, Vari, RP and Betancur, RR (2016) Herbivory promotes dental disparification and macroevolutionary dynamics in grunters (Teleostei: Terapontidae), a freshwater adaptive radiation. American Naturalist 187, 320–33.CrossRefGoogle Scholar
Debiais-Thibaud, M, Chiori, R, Enault, S, Oulion, S, Germon, I, Martinand-Mari, C, Casane, D and Borday-Birraux, V (2015) Tooth and scale morphogenesis in shark: an alternative process to the mammalian enamel knot system. BMC Evolutionary Biology 15, 292.CrossRefGoogle ScholarPubMed
De Blieux, DD and Simons, EL (2002) Cranial and dental anatomy of Antilohyrax pectidens: a Late Eocene hyracoid (Mammalia) from the Fayum, Egypt. Journal of Vertebrate Paleontology 22, 122–36.CrossRefGoogle Scholar
Dragastan, ON and Herbig, H-G (2007) Halimeda (green siphonous algae) from the Paleogene of Morocco – taxonomy, phylogeny and paleoenvironment. Micropaleontology 53, 172.CrossRefGoogle Scholar
Fishelson, L and Delarea, Y (2013) Comparison of the oral cavity architecture in surgeonfishes (Acanthuridae, Teleostei), with emphasis on the taste buds and jaw ‘retention plates’. Environmental Biology of Fishes 97, 173–85.CrossRefGoogle Scholar
Fishelson, L, Golani, D and Diamant, A (2014) SEM study of the oral cavity of members of the Kyphosidae and Girellidae (Pisces, Teleostei), with remarks on Crenidens (Sparidae), focusing on teeth and taste bud numbers and distribution. Zoology 117, 122–30.CrossRefGoogle Scholar
Fraser, GJ, Bloomquist, RF and Streelman, JT (2008) A periodic pattern generator for dental diversity. BMC Biology 6, 32.CrossRefGoogle ScholarPubMed
Fraser, GJ, Bloomquist, RF and Streelman, JT (2013) Common developmental pathways link tooth shape to regeneration. Developmental Biology 377, 399414.CrossRefGoogle ScholarPubMed
Gibson, SZ (2015) Evidence of a specialized feeding niche in a Late Triassic ray-finned fish: evolution of multidenticulate teeth and benthic scraping in †Hemicalypterus . Science of Nature 102, 10.CrossRefGoogle Scholar
Gibson, SZ (2016) Redescription and phylogenetic placement of †Hemicalypterus weiri Schaeffer, 1967 (Actinopterygii, Neopterygii) from the Triassic Chinle Formation, southwestern United States: new insights into morphology, ecological niche, and phylogeny. PLOS ONE 11, e0163657. doi: 10.1371/journal.pone.0163657.CrossRefGoogle ScholarPubMed
Gregory, JT (1950) A large pycnodont from the Niobrara Chalk. Postilla 5, 110.Google Scholar
Jackman, WR, Davies, SH, Lyons, DB, Stauder, CK, Denton-Schneider, BR, Jowdry, A, Aigler, SR, Vogel, SA and Stock, DW (2013) Manipulation of Fgf and Bmp signaling in teleost fishes suggests potential pathways for the evolutionary origin of multicuspid teeth. Evolution & Development 15, 107–18.CrossRefGoogle ScholarPubMed
Jalil, N-E and Janvier, P (2005) Les pareiasaures (Amniota, Parareptilia) du Permien supérieur du Bassin d’Argana, Maroc. Geodiversitas 27, 35132.Google Scholar
Jernvall, J, Kettunen, P, Karavanova, I, Martin, LB and Thesleff, I (1994) Evidence for the role of the enamel knot as a control center in mammalian tooth cusp formation: non-dividing cells express growth stimulating Fgf-4 gene. International Journal of Developmental Biology 38, 463–9.Google ScholarPubMed
Jernvall, J and Thesleff, I (2012) Tooth shape formation and tooth renewal: evolving with the same signals. Development 139, 3487–97.CrossRefGoogle ScholarPubMed
Kley, NJ, Sertich, JJW, Turner, AH, Krause, DW, O’Connor, PM and Georgi, JA (2010) Craniofacial morphology of Simosuchus clarki (Crocodyliformes: Notosuchia) from the Late Cretaceous of Madagascar. Society of Vertebrate Paleontology Memoir 10, Journal of Vertebrate Paleontology 30, 1398.Google Scholar
Kocsis, L, Gheerbrant, E, Mouflih, M, Cappetta, H, Yans, J and Amaghzaz, M (2014) Comprehensive stable isotope investigation of marine biogenic apatite from the late Cretaceous–early Eocene phosphate series of Morocco. Palaeogeography, Palaeoclimatology, Palaeoecology 394, 7488.CrossRefGoogle Scholar
Kriwet, J (2005) A comprehensive study of the skull and dentition of pycnodont fishes. Zitteliana A 45, 135–88.Google Scholar
Leidy, J (1873) Contributions to the extinct vertebrate fauna of the Western Territories. Report of the United States Geological Survey of the Territories 1, 14358.Google Scholar
Lima, FCT, Wosiacki, WB and Ramos, CS (2009) Hemigrammus arua, a new species of characid (Characiformes: Characidae) from the lower Amazon, Brazil. Neotropical Ichthyology 7, 153–60.CrossRefGoogle Scholar
Longbottom, AE (1984) New Tertiary pycnodonts from the Tilemsi valley, Republic of Mali. Bulletin of the British Museum (Natural History), Geology Series 38, 126.Google Scholar
Melstrom, KM (2017) The relationship between diet and tooth complexity in living dentigerous saurian. Journal of Morphology 278, 500–22.CrossRefGoogle Scholar
Nursall, JR (1996) The phylogeny of pycnodont fishes. In Mesozoic Fishes – Systematics and Paleoecology (eds Arratia, G and Viohl, G), pp. 125–52. Munich: Verlag Dr. Friedrich Pfeil.Google Scholar
Ohara, WM, Abrahão, VP and Espíndola, VC (2017a) Hyphessobrycon platyodus (Teleostei: Characiformes), a new species from the Rio Madeira basin, Brazil, with comments on how multicuspid teeth relate to feeding habits in Characidae. Journal of Fish Biology 91, 835–50.CrossRefGoogle Scholar
Ohara, WM, Mirande, JM and Lima, FCT (2017b) Phycocharax rasbora, a new genus and species of Brazilian tetra (Characiformes: Characidae) from Serra do Cachimbo, rio Tapajós basin. PLOS ONE 12, e0170648. doi: 10.1371/journal.pone.0170648.CrossRefGoogle Scholar
Ősi, A, Prondvai, E, Mallon, J and Bodor, ER (2017) Diversity and convergences in the evolution of feeding adaptations in ankylosaurs (Dinosauria: Ornithischia). Historical Biology 29, 539–70.CrossRefGoogle Scholar
Poyato-Ariza, FJ (2005) Pycnodont fishes: morphologic variation, ecomorphologic plasticity and a new interpretation of their evolutionary history. Bulletin of the Kitakyushu Museum of Natural History and Human History A 3, 169–84.Google Scholar
Poyato-Ariza, FJ (2010) Polazzodus, gen. nov., a new pycnodont fish from the Late Cretaceous of northeastern Italy. Journal of Vertebrate Paleontology 30, 650–64.CrossRefGoogle Scholar
Poyato-Ariza, FJ (2013) Sylvienodus, a new replacement genus from the Cretaceous pycnodontiform fish ‘Pycnoduslaveirensis . Comptes Rendus Palevol 12, 91100.CrossRefGoogle Scholar
Poyato-Ariza, FJ and Martín-Abad, H (2013) History of two lineages: comparative analysis of the fossil record in Amiiformes and Pycnodontiformes (Osteichthyes, Actinopterygii). Spanish Journal of Palaeontology 28, 7990.Google Scholar
Poyato-Ariza, FJ and Wenz, S (2002) A new insight into pycnodontiform fishes. Geodiversitas 24, 139248.Google Scholar
Regan, CT (1923) The skeleton of Lepidosteus, with remarks on the origin and evolution of the lower neopterygian fishes. Proceedings of the Zoological Society of London 1923, 445–61.Google Scholar
Senut, B (2003) The Macroscelididae from the Miocene of the Orange River, Namibia. Memoir of the Geological Survey of Namibia 19, 119–41.Google Scholar
Smith, MM, Johanson, Z, Butts, T, Ericsson, R, Modrell, M, Tulenko, FJ, Davis, MC and Fraser, GJ (2015) Making teeth to order: conserved genes reveal an ancient molecular pattern in paddlefish (Actinopterygii). Proceedings of the Royal Society B 282, 20142700. doi: 10.1098/rspb.2014.2700.CrossRefGoogle Scholar
Streelman, JT and Albertson, RC (2006) Evolution of novelty in the cichlid dentition. Journal of Experimental Zoology (Mol Dev Evol) 306B, 216–26.CrossRefGoogle Scholar
Streelman, JT, Webb, JF, Albertson, RC and Kocher, TD (2003) The cusp of evolution and development: a model of cichlid tooth shape diversity. Evolution & Development 5, 600–8.CrossRefGoogle ScholarPubMed
Stromer, E (1910) Reptilien- und Fischreste aus dem marinen Alttertiär von Südtogo (Westafrika). Monatsberichte der Deutschen Geologischen Gesellschaft 62, 478507.Google Scholar
Szabó, M, Gulyás, P and Ősi, A (2016) Late Cretaceous (Santonian) pycnodontid (Actinopterygii, Pycnodontidae) remains from the freshwater deposits of the Csehbánya Formation (Iharkút, Bakony Mountains, Hungary). Annales de Paléontologie 102, 123–34.CrossRefGoogle Scholar
Tabaste, N (1963) Etude de restes de poissons du Crétacé saharien. Mémoires de l’Institut Français d’Afrique Noire 68, 437–85.Google Scholar
Tintori, A (1983) Hypsisomatic Semionotidae (Pisces, Actinopterygii) from the Upper Triassic of Lombardy (N. Italy). Rivista Italiana de Paleontologia e Stratigrafia 88, 417–42.Google Scholar
Tintori, A (1998) Fish biodiversity in the marine Norian (Late Triassic) of northern Italy: the first neopterygian radiation. Italian Journal of Zoology 65, 193–8.CrossRefGoogle Scholar
Trapani, J, Yamamoto, Y and Stock, DW (2005) Ontogenetic transition from unicuspid to multicuspid oral dentition in a teleost fish: Astyanax mexicanus, the Mexican tetra (Ostariophysi: Characidae). Zoological Journal of the Linnean Society 145, 523–38.CrossRefGoogle Scholar
Tsuji, LA (2013) Anatomy, cranial ontogeny and phylogenetic relationships of the pareiasaur Deltavjatia rossicus from the Late Permian of central Russia. Earth and Environmental Science Transactions of the Royal Society of Edinburgh 104, 142.CrossRefGoogle Scholar
Vaatokari, A, Åberg, T, Jernvall, J, Keränen, S and Thesleff, I (1996) The enamel knot as a signaling center in the developing mouse tooth. Mechanisms of Development 54, 3943.CrossRefGoogle Scholar
Vullo, R, Cavin, L, Khalloufi, B, Amaghzaz, M, Bardet, N, Jalil, N-E, Jourani, E, Khaldoune, F and Gheerbrant, E (2017) A unique Cretaceous–Paleogene lineage of piranha-jawed pycnodont fishes. Scientific Reports 7, 6802. doi: 10.1038/s41598-017-06792-x.CrossRefGoogle ScholarPubMed
Wagner, PJ (2000) The quality of the fossil record and the accuracy of phylogenetic inferences about sampling and diversity. Systematic Biology 49, 6586.CrossRefGoogle ScholarPubMed
White, EI (1934) Fossil fishes of Sokoto Province. Geological Survey of Nigeria 14, 178.Google Scholar
Zittel, KA (1888) Handbuch der Palæontologie. I Abtheilung. Palæozoologie. III Band. Vertebrata (Pisces, Amphibia, Reptilia, Aves). Second Instalment. Munich and Leipzig: Druck und Verlag von R Oldenbourg, 257436 pp.Google Scholar