Skip to main content

Advertisement

SpringerLink
Log in

Enamel Microstructure in Eocene Cetaceans from Antarctica (Archaeoceti and Mysticeti)

  • Original Paper
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

Modern baleen whales have no adult teeth, whereas dolphins and porpoises have a homodont and polydont dentition, with simplified enamel microstructure. However, archaic cetaceans (archaeocetes and early mysticetes and odontocetes) had a complex and ornamented dentition, with complex enamel microstructure as in terrestrial mammals. This study describes the morphology of teeth and enamel microstructure in two fossil cetaceans from Antarctica: a basilosaurid archaeocete from the La Meseta Formation (middle Eocene); and Llanocetus sp. from the Submeseta Formation (late Eocene), one of the oldest mysticetes known. The two teeth analyzed were lower premolars, with transversely compressed triangular crowns composed of a main cusp and accessory denticles. The enamel microstructure of the basilosaurid and Llanocetus sp. is prismatic with Hunter-Schreger bands (HSB) and an outer zone of radial enamel. In the basilosaurid, the enamel is relatively thin and measures 150–180 μm, whereas in Llanocetus sp. it is considerably thicker, measuring 830–890 μm in the cusp area and 350–380 μm near the crown base. This is one of the thickest enamel layers among cetaceans, extinct and living. Structures resembling enamel tufts and lamellae were observed in both fossils at the enamel-dentine junction (EDJ) and extending along the thickness of the enamel layer, respectively. The presence of HSB and biomechanical reinforcing structures such as tufts and lamellae suggests prominent occlusal loads during feeding, consistent with raptorial feeding habits. Despite the simplification or absence of teeth in modern cetaceans, their ancestors had complex posterior teeth typical of most mammals, with a moderately thick enamel layer with prominent HSB.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

EDJ:

Enamel-dentine junction

HSB:

Hunter-Schreger bands

IPM:

Interprismatic matrix

OES:

Outer enamel surface

PLEX:

Prismless enamel

RE:

Radial enamel

SEM:

Scanning electron microscopy

References

  • Bajpai S, Gingerich PD (1998) A new Eocene archaeocete (Mammalia, Cetacea) from India and the time of origin of whales. Proc Natl Acad Sci USA 95:15464–15468

    Article  CAS  Google Scholar 

  • Bergqvist LP (2003) The role of teeth in mammal history. Braz J Oral Sci 2:249–257

    Google Scholar 

  • Borsuk-Białynicka M (1988) New remains of Archaeoceti from the Paleogene of Antarctica. Pol Polar Res 9: 437–445

    Google Scholar 

  • Buono MR, Fernández MS, Reguero MA, Marenssi SA, Santillana SN, Mörs T (2016) Eocene basilosaurid whales from the La Meseta Formation, Marambio (Seymour) Island, Antarctica. Ameghiniana 53:296–315

    Article  Google Scholar 

  • Deméré TA, Berta A (2008) Skull anatomy of the Oligocene toothed mysticete Aetioceus weltoni (Mammalia; Cetacea): implications for mysticete evolution and functional anatomy. Zool J Linn Soc 154:308–352

    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 57:15–37

    Article  Google Scholar 

  • Fahlke JM (2012) Bite marks revisited - evidence for middle-to-late Eocene Basilosaurus isis predation on Dorudon atrox (both Cetacea, Basilosauridae). Palaeontol Electron 15: 1–16

    Google Scholar 

  • Fahlke JM, Bastl KA, Semprebon GM, Gingerich PD (2013) Paleoecology of archaeocete whales throughout the Eocene: dietary adaptations revealed by microwear analysis. Palaeogeogr Palaeoclimatol Palaeoecol 386:690–701

    Article  Google Scholar 

  • Fitzgerald EMG (2010) The morphology and systematics of Mammalodon colliveri (Cetacea: Mysticeti), a toothed mysticete from the Oligocene of Australia. Zool J Linn Soc Lond 158:367–476

    Article  Google Scholar 

  • Ford JKB, Ellis GM, Matkin CO, Wetklo MH, Barrett-Lennard LG, Withler RE (2011) Shark predation and tooth wear in a population of northeastern Pacific killer whales. Aquat Biol 11: 213–224

    Article  Google Scholar 

  • Fordyce RE (1985) Late Eocene archaeocete whale (Archaeoceti: Dorudontinae) from Waihao, South Canterbury, New Zealand. New Zeal J Geol Geop 28:351–357

    Article  Google Scholar 

  • Fordyce RE (1989) Origins and evolution of Antarctic marine mammals. Geol Soc Lond Spec Publ 47:269–281

    Article  Google Scholar 

  • Fordyce RE (2009) Cetacean evolution. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of Marine Mammals, 2nd edn. Academic Press, San Diego, pp 201–207

    Chapter  Google Scholar 

  • Fordyce RE, Marx FG (2018) Gigantism precedes filter feeding in baleen whale evolution. Curr Biol 28:1670–1676

    Article  CAS  Google Scholar 

  • Fordyce RE, Muizon C de (2001) Evolutionary history of cetaceans: a review. In: Mazin J-M, de Buffrénil V (eds) Secondary Adaptation of Tetrapods to Life in Water. Verlag Dr. Friedrich Pfeil, München, pp 169–233

  • Fostowicz-Frelik Ł (2003) An enigmatic whale tooth from the upper Eocene of Seymour Island, Antarctica. Pol Polar Res 24:13–28

    Google Scholar 

  • Geisler JH, Boessenecker RW, Brown M, Beatty BL (2017) The origin of filter feeding in whales. Curr Biol 27:2036–2042

    Article  CAS  Google Scholar 

  • Hocking DP, Marx FG, Fitzgerald EM, Evans AR (2017) Ancient whales did not filter feed with their teeth. Biol Letters 13: 20170348. https://doi.org/10.1098/rsbl.2017.0348

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Kalthoff DC (2006) Incisor enamel microstructure and its implications to higher-level systematics of Eurasian Oligocene and early Miocene hamsters (Rodentia). Palaeontographica A 277:67–80

    Google Scholar 

  • Karlsen K (1962) Development of tooth germs and adjacent structures in the whalebone whale (Balaenoptera physalus (L.)). Hvalradets Skrifter 45:1–56

    Google Scholar 

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

  • Koenigswald W von, Sander PM (1997) Glossary of terms used for enamel microstructures. In: Koenigswald W von, Sander PM (eds) Tooth Enamel Microstructure. Balkema, Rotterdam, pp 267–280

  • Loch C, Duncan WJ, 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:e0116557. https://doi.org/10.1371/journal.pone.0116557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Marx FG, Tsai CH, Fordyce RE (2015) A new Early Oligocene toothed ‘baleen’whale (Mysticeti: Aetiocetidae) from western North America: one of the oldest and the smallest. R Soc Open Sci 2: 150476

    Article  Google Scholar 

  • Marx FG, Hocking DP, Park T, Ziegler T, Evans AR, Fitzgerald EMG (2016a) Suction feeding preceded filtering in baleen whale evolution. Mem Mus Vic 75: 71–82

    Article  Google Scholar 

  • Marx FG, Lambert O, Uhen MD (2016b) Cetacean Paleobiology. John Wiley & Sons, Hoboken

    Book  Google Scholar 

  • McGowen MR, Spaulding M, Gatesy J (2009) Divergence date estimation and a comprehensive molecular tree of extant cetaceans. Mol Phylogenet Evol 53: 891–906

    Article  CAS  Google Scholar 

  • Mitchell ED (1989) A new cetacean from the late Eocene La Meseta Formation Seymour Island, Antarctic Peninsula. Can J Fish Aquat Sci 46: 2219–2235

    Article  Google Scholar 

  • Nanci A (2012) Ten Cate's Oral Histology: Development, Structure, and Function. Elsevier, St. Louis

    Google Scholar 

  • O’Leary MA, Uhen MD (1999) The time of origin of whales and the role of behavioral changes in the terrestrial-aquatic transition. Paleobiology 25:534–556

    Article  Google Scholar 

  • Peredo CM, Pyenson ND, Boersma AT (2017) Decoupling tooth loss from the evolution of baleen in whales. Front Mar Sci 4:67. https://doi.org/10.3389/fmars.2017.00067

    Article  Google Scholar 

  • Peredo CM, Peredo JS, Pyenson ND (2018) Convergence on dental simplification in the evolution of whales. Paleobiology: 1–10. https://doi.org/10.1017/pab.2018.9

    Article  Google Scholar 

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

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

    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 

  • Thewissen JGM, Sensor JD, Clementz MT, Bajpai S (2011) Evolution of dental wear and diet during the origin of whales. Paleobiology 37:655–669

    Article  Google Scholar 

  • Thewissen JGM, Williams EM, Roe LJ, Hussain ST (2001) Skeletons of terrestrial cetaceans and the relationship of whales to artiodactyls. Nature 413:277–281

    Article  CAS  Google Scholar 

  • Uhen MD (2000) Replacement of deciduous first premolars and dental eruption in archaeocete whales. J Mammal 81:123–133

    Article  Google Scholar 

  • Uhen MD (2008) New protocetid whales from Alabama and Mississippi, and a new cetacean clade, Pelagiceti. J Vertebr Paleontol 28:589–593

    Article  Google Scholar 

  • Uhen MD (2009) Evolution of cetacean dental morphology. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of Marine Mammals, 2nd edn. Academic Press, San Diego, pp 302–307

    Chapter  Google Scholar 

  • Ungar PS (2010) Mammal Teeth: Origin, Evolution and Diversity. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Werth AJ (2001) How do mysticetes remove prey trapped in baleen? Bull Mus Comp Zool 156:189–203

    Google Scholar 

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

    Article  Google Scholar 

  • Wiman C (1905) Über die alttertiären Vertebraten der Seymourinsel. Wiss Ergebn Schwed Südpol–Exp 3:1–37

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Instituto Antártico Argentino (IAA-DNA) and Fuerza Aérea Argentina as well as the Swedish Polar Research Secretariat (SPFS) for logistical support during field work in Antarctica. J. Hagström (NRM), J. Moly (MLP), J. O’Gorman (MLP), M. Reguero (MLP), and C. Tambussi (CICTERRA) are thanked for their assistance in the field. M. Reguero (MLP) provided access to dental samples. We also acknowledge the facilities as well as scientific and technical assistance from staff at the Otago Centre for Electron Microscopy (OCEM) at the University of Otago, in particular Liz Girvan. CL acknowledges the University of Otago Faculty of Dentistry for a Sir Thomas Kay Sidey Research Grant. TM acknowledges financial support from the Swedish Research Council (VR Grant 2009-4447).

Author information

Authors and Affiliations

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

    Carolina Loch

  2. Instituto Patagónico de Geología y Paleontología, CONICET, U9120ACD, Puerto Madryn, Chubut, Argentina

    Monica R. Buono

  3. Department of Zoology, Swedish Museum of Natural History, SE-104 05, Stockholm, Sweden

    Daniela C. Kalthoff

  4. Department of Paleobiology, Swedish Museum of Natural History, SE-104 05, Stockholm, Sweden

    Thomas Mörs

  5. Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, CONICET, La Plata, 1900, Buenos Aires, Argentina

    Marta S. Fernández

Authors
  1. Carolina Loch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Monica R. Buono
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daniela C. Kalthoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas Mörs
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marta S. Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carolina Loch.

Ethics declarations

No permits were required for the described study, which complied with all relevant regulations.

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Loch, C., Buono, M.R., Kalthoff, D.C. et al. Enamel Microstructure in Eocene Cetaceans from Antarctica (Archaeoceti and Mysticeti). J Mammal Evol 27, 289–298 (2020). https://doi.org/10.1007/s10914-018-09456-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-018-09456-3

Keywords

Search

Navigation