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

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Enamel Microstructure in Eocene Cetaceans from Antarctica (Archaeoceti and Mysticeti) Journal of Mammalian Evolution https://doi.org/10.1007/s10914-018-09456-3 ORIGINAL PAPER Enamel Microstructure in Eocene Cetaceans from Antarctica (Archaeoceti and Mysticeti) Carolina Loch1 & Monica R. Buono2 & Daniela C. Kalthoff3 & Thomas Mörs4 & Marta S. Fernández5 # Springer Science+Business Media, LLC, part of Springer Nature 2019 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 com- plex and ornamented dentition, with complex enamel microstructure as in terrestrial mammals. This study describes the mor- phology 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. Keywords Archaeocetes . Hunter-Schreger bands . La Meseta formation . Mysticetes . Teeth Abbreviations PLEX Prismless enamel EDJ Enamel-dentine junction RE Radial enamel HSB Hunter-Schreger bands SEM Scanning electron microscopy IPM Interprismatic matrix OES Outer enamel surface Introduction * Carolina Loch [email protected] The evolutionary history of cetaceans - whales, dolphins, and porpoises - started with the rise of Archaeoceti, a paraphyletic 1 Sir John Walsh Research Institute, Faculty of Dentistry, University of group of stem cetaceans, in the ancient Tethys seaway during Otago, Dunedin 9054, New Zealand the early Eocene more than 50 million years ago (Bajpai and 2 Instituto Patagónico de Geología y Paleontología, CONICET, Gingerich 1998). The earliest archaeocetes - pakicetids, U9120ACD Puerto Madryn, Chubut, Argentina ambulocetids, remingtonocetids - were amphibious species 3 Department of Zoology, Swedish Museum of Natural History, from Eocene sediments of fluvial, brackish, and fully marine SE-104 05 Stockholm, Sweden origin (Thewissen et al. 2001;Marxetal.2016b). By the late 4 Department of Paleobiology, Swedish Museum of Natural History, Eocene (35–36 Ma), pelagic archaeocetes (Basilosauridae) SE-104 05 Stockholm, Sweden were widespread across the world’s oceans and gave rise to 5 Facultad de Ciencias Naturales y Museo, Universidad Nacional de La modern cetaceans (Neoceti: Odontoceti and Mysticeti) Plata, CONICET, La Plata, 1900 Buenos Aires, Argentina (Fordyce and Muizon 2001;Uhen2008;Fordyce2009). J Mammal Evol Archaeocetes had elongated rostra with a heterodont den- species (Bergqvist 2003;Ungar2010). Of particular impor- tition that was diphyodont. Although the anterior teeth were tance is the microstructure of enamel, the highly mineralized conical, with high crowns separated by prominent diastemata, cover of tooth crowns made of hydroxyapatite crystals the posterior teeth had lower crowns, were more-heavily built, (Koenigswald 1997). The pattern of organization of hydroxy- and often had multiple denticles on the mesial and distal keels apatite crystals into prisms, and the 3-dimensional organiza- (Uhen 2000, 2009). Archaeocetes had a maximum of 13 teeth tion of enamel prisms, is influenced by biomechanical/ per quadrant. Based on the morphology of the feeding appa- functional adaptation and phylogeny (Koenigswald 1997). ratus and teeth, it has been suggest that most archaeocetes Previous investigations have described details of the enamel were capable of shearing and snapping prey items (O’Leary organization in Eocene basal archaeocetes from India and and Uhen 1999; Fahlke et al. 2013). Pakistan (Maas and Thewissen 1995; Sahni and Modern mysticetes have no functional teeth, although rudi- Koenigswald 1997), Eocene and Oligocene archaeocetes and mentary teeth are produced during embryonic development odontocetes from the Southern Hemisphere (Fostowicz-Frelik (Karlsen 1962). Instead, keratinized baleen plates of epithelial 2003; Loch et al. 2015), and living odontocetes (Ishiyama origin are present in the maxillae of baleen whales, which are 1987;Lochetal.2013). So far, details on the enamel micro- used to filter marine organisms such as copepods, crustaceans, structure and its relationship with inferred feeding habits of andfish(Karlsen1962;Werth2001). Archaic mysticetes, how- early radiating toothed mysticetes are unknown. This could ever, were heterodont (e.g., Llanocetidae, Mammalodontidae, shed light on the evolution of feeding strategies in mysticetes, and Aetiocetidae) (Uhen 2009). The cheek teeth of archaic from raptorial to filter feeding (e.g., Deméré et al. 2008;Marx mysticetes were usually separated by wide diastemata, had et al. 2016a;Peredoetal.2017). prominent denticles, and were covered by ornamented enamel This study aims to describe the microstructural arrange- (Uhen 2009). The teeth of the late Eocene mysticete Llanocetus ment of the enamel layer in two Eocene whales from denticrenatus had a peculiar and distinctive morphology. The Antarctica, an undetermined basilosaurid and the toothed anterior teeth were conical and pointed, whereas the posterior mysticete Llanocetus sp. We discuss the functional and bio- cheek teeth had a palmate crown, composed of a main cusp and mechanical implications of the enamel organization in these widely-spaced denticles anteroposteriorly splayed out in the early clades, and also the potential phylogenetic signals of the dorsal surface of the crown (Mitchell 1989;Fordyceand enamel characters observed. Marx 2018). The analysis of tooth morphology and key cranial and mandibular characters suggests that toothed mysticetes employed a variety of feeding strategies prior to the origin of Materials and Methods the baleen-assisted filter feeding. These were suction feeding (e.g., mammalodontids; Fitzgerald 2010) and suction-assisted Materials Analyzed raptorial feeding (e.g., llanocetids and aetiocetids; Marx et al. 2015; Fordyce and Marx 2018). Teeth of Eocene Pelagiceti (Basilosauridae + Neoceti, sensu Teeth make up a prominent part of the fossil record of Uhen 2008) from Marambio (=Seymour) Island, Antarctic mammals due to the high mineral content of enamel and den- Peninsula, were analyzed. The sample consisted of a fragment tine (Bergqvist 2003). The study of the morphology and mi- of the crown of a p2 tooth (in situ) of a Basilosauridae indet. crostructure of mammalian teeth can elucidate the feeding (MLP 11-II-21-3; Buono et al. 2016), and a fragment of an ecology, functional morphology, and phylogenetic relation- isolated premolar cheek tooth (lower left p3; MLP 12-XI-1- ships of fossil and recent mammal species, shedding light on 10b) of a toothed Mysticeti, Llanocetus sp. (Table 1). MLP 11- the paleobiology of extinct and otherwise poorly known II-21-3 was collected from La Meseta Formation (Cucullaea I Table 1 Specimens analysed in this study Species Collection number Tooth type Geographic location and stratigraphic provenance Basilosauridae indet. MLP 11-II-21-3 Premolar (p2) Marambio (=Seymour) Island, Antarctic Peninsula; (DVP 2/84; 64°13′ 53.58” S; 56°39′ 13.74” W); La Meseta Formation (Cucullaea I Allomember middle Eocene; Lutetian–Bartonian) Llanocetus sp. MLP 12-XI-1-10 Premolar (p3) Marambio (=Seymour) Island, Antarctic Peninsula; (DVP 13/84; 64°14′ 37” S; 56°36′ 01” O); Submeseta Formation (TELM 7; Late Eocene; Priabonian) JMammalEvol Allomember; middle Eocene) and MLP 12-XI-1-10b was col- Japan) operating at 5 kV and 10 μA. The JEOL JSM-6700F lected from Submeseta Formation (Submeseta II SEM is housed at the Otago OCEM, University of Otago, Allomember; late Eocene) (Table 1). Both specimens were New Zealand. Magnifications in the SEM ranged from 25X made available for destructive sampling from the Museo de to 2500X. MLP 11-II-21-3 was also studied using a Hitachi La Plata (MLP) fossil collections (La Plata, Argentina). S-4300 SEM operating at 15 kV and 10 μA and at magni- fications from 200 to × 2,000x. The SEM is located at the Methods Swedish Museum of Natural History in Stockholm (NRM). Preparation followed the proceedures described in Kalthoff Sample Preparation and Microscopy Due to the rarity of the (2006). material and the destructive nature of the preparation methods, representative tooth fragments were used for anal- Data availability All data for this study are included in the ysis. Fragments were surface-cleaned with ethanol and em- publication or available upon reasonable
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