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Enamel ultrastructure of fossil and modern pinnipeds: evaluating hypotheses of feeding adaptations in the extinct walrus Pelagiarctos

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Abstract

This study aimed to assess the enamel ultrastructure in modern otariid pinnipeds and in the extinct walrus Pelagiarctos. Teeth of the New Zealand fur seal (Arctocephalus forsteri), sea lion (Phocarctos hookeri), and fossil walrus Pelagiarctos thomasi were embedded, sectioned, etched, and analyzed via scanning electron microscopy. The enamel of NZ otariids and Pelagiarctos was prismatic and moderately thick, measuring 150–450 μm on average. It consisted of transversely oriented Hunter-Schreger bands (HSBs) from the enamel-dentine junction (EDJ) to near the outer surface, where it faded into prismless enamel less than 10 μm thick. The width of HSB was variable and averaged between 6 and 10 prisms, and they presented an undulating course both in longitudinal and cross sections. The overall organization of the enamel was similar in all teeth sampled; however, the enamel was thicker in canines and postcanines than in incisors. The crowns of all teeth sampled were uniformly covered by enamel; however, the grooved incisors lacked an enamel cover on the posterior side of the buccal face. Large tubules and tuft-like structures were seen at the EDJ. HSB enamel as well as tubules and tufts at the EDJ suggest increased occlusal loads during feeding, a biomechanical adaptation to avoid enamel cracking and failure. Despite overall simplification in tooth morphology and reduced mastication, the fossil and modern pinnipeds analyzed here retained the complex undulating HSB structure of other fossils and living Carnivora, while other marine mammals such as cetaceans developed simplified radial enamel.

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References

  • Armfield BA, Zheng Z, Bajpaj S, Vinyard CJ, Thewissen JGM (2013) Development and evolution of the unique cetacean dentition. PeerJ 1:e24

    Article  PubMed  PubMed Central  Google Scholar 

  • Barnes LG (1977) Outline of eastern North Pacific fossil cetacean assemblages. Syst Zool 25:321–343

    Article  Google Scholar 

  • Barnes LG (1988) A new fossil pinniped (Mammalia: Otariidae) from the Middle Miocene Sharktooth Hill Bonebed, California. Contr Sci Mus Nat His Los Angeles 396:1–11

    Google Scholar 

  • Berta A (2002) Pinnipedia, overview. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic, San Diego, pp 903–911

    Google Scholar 

  • Berta A, Adam PJ (2001) Evolutionary biology of pinnipeds. In: Mazin J-M, de Buffrénil V (eds) Secondary adaptation of tetrapods to life in water. Verlag Dr. Friedrich Pfeil, München, pp 235–260

    Google Scholar 

  • Boessenecker RW (2011) New records of the fur seal Callorhinus (Carnivora: Otariidae) from the Plio-Pleistocene Rio Dell Formation of Northern California and comments on otariid dental evolution. J Vert Paleont 31:454–467

    Article  Google Scholar 

  • Boessenecker RW, Churchill M (2013) A reevaluation of the morphology, paleoecology, and phylogenetic relationships of the enigmatic walrus Pelagiarctos. PloS One 8(1):e54311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carlson SJ, Krause DW (1985) Enamel ultrastructure of multituberculate mammals: an investigation of variability. Michigan Univ Mus Paleo Cont 27(1):1–50

    Google Scholar 

  • Churchill M, Clementz MT (2015a) Functional implications of variation in tooth spacing and crown size in Pinnipedimorpha (Mammalia: Carnivora). Anat Rec 298(5):878–902

    Article  Google Scholar 

  • Churchill M, Clementz MT (2015b) Was Enaliarctos (Carnivora: Pinnipedimorpha) a pierce feeder? Insights from tooth spacing and crown size. J Evolution Biol. doi: 10.1111/jeb.12783

  • Churchill M, Boessenecker RW, Clementz MT (2014) Colonization of the southern hemisphere by fur seals and sea lions (Carnivora: Otariidae) revealed by combined evidence phylogenetic and Bayesian biogeographical analysis. Zoo J Linn Soc 172(1):200–225

    Article  Google Scholar 

  • Cobb WM (1933) The dentition of the walrus, Odobenus obesus. Proc Zool Soc Lond 103:645–668

    Article  Google Scholar 

  • Deméré TA, Berta A (2001) A reevaluation of Proneotherium repenningi from the Miocene Astoria Formation of Oregon and its position as a basal odobenid (Pinnipedia: Mammalia). J Vert Paleo 21(2):279–310

    Article  Google Scholar 

  • Deméré TA, McGowen MR, Berta A, Gatesy J (2008) Morphological and molecular evidence for a stepwise evolutionary transition from teeth to baleen in mysticete whales. Syst Biol 57(1):15–37

    Article  PubMed  Google Scholar 

  • Drehmer CJ, Sanfelice D, Loch C (2015) Dental anomalies in pinnipeds (Carnivora: Otariidae and Phocidae): occurrence and evolutionary implications. Zoomorphology 134(2):325–338

    Article  Google Scholar 

  • Fordyce RE (1982) Dental anomaly in a fossil squalodont dolphin from New Zealand, and the evolution of polydonty in whales. NZ J Zool 9(4):419–426

    Article  Google Scholar 

  • Gatesy J, Geisler JH, Chang J, Buell C, Berta A, Meredith RW, Springer MS, McGowen MR (2013) A phylogenetic blueprint for a modern whale. Mol Phylogenet Evol 66(2):479–506

    Article  PubMed  Google Scholar 

  • Gingerich PD, Ul Haq M, Zalmout IS, Khan IH, Malkani MS (2001) Origin of whales from early artiodactyls: hands and feet of Eocene Protocetidae from Pakistan. Science 293:2239–2242

    Article  CAS  PubMed  Google Scholar 

  • Holwerda FM, Beatty BL, Schulp AS (2013) Dental macro-and microwear in Carinodens belgicus, a small mosasaur from the type Maastrichtian. Neth J Geosci 92(04):267–274

    Google Scholar 

  • Ishiyama M (1987) Enamel structure in odontocete whales. Scan Microsc 1:1071–1079

    CAS  Google Scholar 

  • Kohno N, Barnes LG, Hirota K (1995) Miocene fossil pinnipeds of the genera Prototaria and Neotherium (Carnivora; Otariidae; Imagotariinae) in the North Pacific Ocean: evolution, relationships and distribution. Isl Arc 3(4):285–308

    Article  Google Scholar 

  • Loch C, Duncan W, Simões-Lopes PC, Kieser JA, Fordyce RE (2013) Ultrastructure of enamel and dentine in extant dolphins (Cetacea: Delphinoidea and Inioidea). Zoomorphology 132:215–225

    Article  Google Scholar 

  • Loch C, Kieser JA, Fordyce RE (2015) Enamel ultrastructure in fossil cetaceans (Cetacea: Archaeoceti and Odontoceti). PLoS One 10(1):e0116557

    Article  PubMed  PubMed Central  Google Scholar 

  • Maas MC, Dumont ER (1999) Built to last: the structure, function, and evolution of primate dental enamel. Evol Anthropol 8:133–152

    Article  Google Scholar 

  • Maas MC, Thewissen JGM (1995) Enamel microstructure of Pakicetus (Mammalia: Archaeoceti). J Paleontol 69:1154–1163

  • Marshall CD, Rosen DAS, Trites AW (2015) Feeding kinematics and performance of basal otariid pinnipeds, Steller sea lions and northern fur seals: implications for the evolution of mammalian feeding. J Exp Biol 218:3229–3240

    Article  PubMed  Google Scholar 

  • McGraw WS, Pampush JD, Daegling DJ (2012) Brief communication: enamel thickness and durophagy in mangabeys revisited. Am J Phy Anthropol 147:326–333

    Article  Google Scholar 

  • Mitchell ED (1965) History of research at Sharktooth Hill, Kern County, California. Kern Co Hist Soc Spec Paper 1:1–45

    Google Scholar 

  • Pauly D, Trites AW, Capuli E, Christensen V (1998) Diet composition and trophic levels of marine mammals. ICES J Mar Sci 55:467–481

    Article  Google Scholar 

  • Prothero DR, Liter MR, Barnes LG, Wang X, Mitchell ED, McLeod SA, Whistler DP, Tedford RH, Ray CE (2008) Land mammals from the Middle Miocene Sharktooth Hill Bonebed, Kern County, California. New Mexico Mus Nat Hist Sci Bull 44:299–314

    Google Scholar 

  • Pyenson ND, Irmis RB, Lipps JH, Barnes LG, Mitchell ED, McLeod SA (2009) Origin of a widespread marine bonebed deposited during the Middle Miocene Climatic Optimum. Geology 37:519–522

    Article  Google Scholar 

  • Sahni A, Von Koenigswald W (1997) The enamel structure of some fossil and recent whales from the Indian subcontinent. In: Von Koenigswald W, Sander PM (eds) Tooth enamel microstructure. Balkema, Rotterdam, pp 177–191

    Google Scholar 

  • Stefen C (1999) Enamel microstructure of recent and fossil Canidae (Carnivora: Mammalia). J Vert Paleontol 19:576–587

    Article  Google Scholar 

  • Stefen C (2001) Enamel structure of arctoid Carnivora: Amphicyonidae, Ursidae, Procyonidae, and Mustelidae. J Mammal 82(2):450–462

    Article  Google Scholar 

  • Stefen C, Rensberger JM (1999) The specialized structure of hyaenid enamel: description and development within the lineage—including percrocutids. Scan Microsc 13:363–380

    Google Scholar 

  • Von Koenigswald W (1997) Evolutionary trends in the differentiation of mammalian enamel ultrastructure. In: Von Koenigswald W, Sander PM (eds) Tooth enamel microstructure. Balkema, Rotterdam, pp 203–235

    Google Scholar 

  • Von Koenigswald W (2000) Two different strategies in enamel differentiation: Marsupialia versus Eutheria. In: Teaford MF, Smith MM, Ferguson MW (eds) Development, function and evolution of teeth. Cambridge University Press, Cambridge, pp 107–118

    Chapter  Google Scholar 

  • Von Koenigswald W, Clemens W (1992) Levels of complexity in the microstructure of mammalian enamel and their application in studies of systematics. Scan Microsc 6:195–218

    CAS  Google Scholar 

  • Werth AJ (2000) Feeding in marine mammals. In: Schwenk K (ed) Feeding: form, function and evolution in tetrapod vertebrates. Academic, San Diego, pp 487–526

    Chapter  Google Scholar 

  • Werth AJ (2006) Mandibular and dental variation and the evolution of suction feeding in Odontoceti. J Mammal 87(3):579–588

    Article  Google Scholar 

Download references

Acknowledgments

This study benefited from constructive comments by O. Lambert and the three anonymous reviewers. We would like to thank J.P. Cavigelli for donating TATE 2694 and facilitating a loan to MC. We appreciate the permission granted to us by S. Dawson (Department of Marine Sciences, University of Otago), Ewan Fordyce (Department of Geology, University of Otago), and J.P. Cavigelli (Tate Geological Museum) for the destructive sampling. Thanks are also extended to Sarah Chew (Summer Studentship, Faculty of Dentistry, University of Otago) for the help with sample polishing, Ludwig Jansen van Vuuren (Oral Rehabilitation, University of Otago) for the support in the sample embedding process, Liz Girvan (OCEM, University of Otago) for the technical assistance with SEM facilities, and G. Kieser for the editorial comments. C. Loch acknowledges the Sir John Walsh Research Institute for a Postdoctoral Fellowship and the late Jules A. Kieser for his inspirational mentoring and support in life and research.

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Authors and Affiliations

  1. Sir John Walsh Research Institute, Faculty of Dentistry, University of Otago, Dunedin, 9054, New Zealand

    Carolina Loch & Jules Kieser

  2. Department of Geology and Environmental Geosciences, College of Charleston, Charleston, 29424, SC, USA

    Robert W. Boessenecker

  3. University of California Museum of Paleontology, University of California, Berkeley, 94720, CA, USA

    Robert W. Boessenecker

  4. Department of Anatomy, New York Institute of Technology College of Osteopathic Medicine, Old Westbury, 11568, New York, USA

    Morgan Churchill

Authors
  1. Carolina Loch
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  2. Robert W. Boessenecker
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  3. Morgan Churchill
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  4. Jules Kieser
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Corresponding author

Correspondence to Robert W. Boessenecker.

Additional information

Communicated by: Sven Thatje

Jules Kieser is deceased.

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Loch, C., Boessenecker, R.W., Churchill, M. et al. Enamel ultrastructure of fossil and modern pinnipeds: evaluating hypotheses of feeding adaptations in the extinct walrus Pelagiarctos . Sci Nat 103, 44 (2016). https://doi.org/10.1007/s00114-016-1366-z

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  • DOI: https://doi.org/10.1007/s00114-016-1366-z

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