Bony Outgrowths on the Jaws of an Extinct Sperm Whale Support Macroraptorial Feeding in Several Stem Physeteroids

Naturwissenschaften (2014) 101:517–521 DOI 10.1007/s00114-014-1182-2

SHORT COMMUNICATION

Bony outgrowths on the jaws of an extinct sperm whale support macroraptorial feeding in several stem physeteroids

Olivier Lambert & Giovanni Bianucci & Brian L. Beatty

Received: 13 March 2014 /Revised: 28 April 2014 /Accepted: 3 May 2014 /Published online: 13 May 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract Several extinct sperm whales (stem Physeteroidea) buttresses, strengthening the teeth when facing intense occlu- were recently proposed to differ markedly in their feeding sal forces. These buccal exostoses further support a raptorial ecology from the suction-feeding modern sperm whales feeding technique for Acrophyseter and, indirectly, for other Kogia and Physeter. Based on cranial, mandibular, and dental extinct sperm whales with a similar oral apparatus morphology, these Miocene forms were tentatively identified (Brygmophyseter, Livyatan, Zygophyseter). With a wide size as macroraptorial feeders, able to consume proportionally range, these Miocene stem physeteroids were major marine large prey using their massive teeth and robust jaws. However, macropredators, occupying ecological niches nowadays most- until now, no corroborating evidence for the use of teeth ly taken by killer whales. during predation was available. We report on a new specimen of the stem physeteroid Acrophyseter, from the late middle to Keywords Cetacea . Physeteroidea . Buccal exostoses . early late Miocene of Peru, displaying unusual bony out- Feeding . Macroraptorial growths along some of the upper alveoli. Considering their position and outer shape, these are identified as buccal maxillary exostoses. More developed along posterior teeth and in Introduction tight contact with the high portion of the dental root outside the bony alveoli, the exostoses are hypothesized to have Feeding strategies of extinct cetaceans are generally difficult developed during powerful bites; they may have worked as to assess firmly without direct evidence of feeding events. Such direct evidence can take the form of preserved stomach contents (Uhen 2004), bite marks on bones (Fahlke 2012), or Communicated by: Sven Thatje predator and prey fossilized together. Among odontocetes O. Lambert (*) (echolocating toothed cetaceans), extinct members of modern Direction Opérationnelle Terre et Histoire de la Vie, Institut Royal lineages are often proposed to feed in a way roughly similar to des Sciences Naturelles de Belgique, 29 rue Vautier, Brussels 1000, Belgium related extant species, a simple assumption recently chal- e-mail: [email protected] lenged for several Miocene fossil sperm whales (superfamily Physeteroidea) (Bianucci and Landini 2006; Lambert et al. G. Bianucci 2008, 2010). These animals were suggested to feed differently Dipartimento di Scienze della Terra, Università di Pisa, 53 via S. Maria, Pisa 56126, Italy from the suction-feeding extant sperm whales Physeter macrocephalus (large sperm whale) and Kogia spp. (pygmy B. L. Beatty and dwarf sperm whales). Morphological correlates for this NYIT College of Osteopathic Medicine, Northern Blvd, Old feeding technique are conspicuous in both genera: reduction Westbury, NY 11568, USA of the upper dentition, slender mandibles, and small temporal B. L. Beatty fossae for a reduced temporal musculature (Werth 2004; Department of Paleobiology, National Museum of Natural History, Bloodworth and Marshall 2005). Smithsonian Institution, Washington, DC 20560, USA The cranial and mandibular osteology of the Miocene stem B. L. Beatty physeteroids Acrophyseter, Brygmophyseter, Livyatan, and Virginia Museum of Natural History, Martinsville, VA 24112, USA Zygophyseter contrasts strongly with Kogia and Physeter: 518 Naturwissenschaften (2014) 101:517–521

Fig. 1 Skull and mandible of Acrophyseter sp. MUSM 1399. a Left position of buccal exostoses. Numbers indicate the position of upper lateral view. b Detail of the left upper tooth row. c Detail of the right upper teeth/alveoli. Dotted lines indicate the original position of exostoses tooth row. d Zoom on the posterior right upper teeth and alveoli. e Detail relative to ventrally shifted teeth. Scale bar for a 100 mm, for b,c,d,e of the right upper tooth row in ventrolateral view. Arrows indicate the 50 mm Naturwissenschaften (2014) 101:517–521 519 robust upper and lower teeth, strong mandibles, and large Results temporal fossae. Taken together, these features suggest a different, macroraptorial predation style, with the teeth being The bizygomatic width (usually corresponding to the maxi- used to catch large prey and possibly to tear flesh pieces mum skull width, indicative of the body size in neocetes) of (Bianucci and Landini 2006; Lambert et al. 2008, 2010). this robust skull is estimated at 385 mm. The supracranial However, until now, no stomach contents, no bite marks on basin is deep on the cranium. The vast temporal fossa (Fig. 1a) contemporary marine vertebrates, and no tooth wear analyses is subcircular in lateral view (maximum length and height unambiguously corroborated this proposed predation style. 230 mm) and transversely deep. Seven alveoli are preserved We report here on a new stem physeteroid from the on each maxilla, with part of the corresponding teeth only Miocene of the Pisco Basin, Peru. The skull displays slightly ventrally shifted in their alveoli. The teeth bear a short unusual bone structures around some of the upper alve- crown covered with enamel, a proportionally slender distal oli providing additional clues about the feeding strate- part of the root (partly due to wear of the region originally gies of extinct sperm whales and their role in Miocene outside gums), and an inflated proximal portion. Long occlu- marine ecosystems. sal facets are observed along distal/mesial surfaces of roots. The mandible is robust. Unusual bony outgrowths resembling buccal exostoses are observed around posterior maxillary alveoli (Fig. 1a,b,c,d,e). A Material and methods thick exostosis is located mesiolabial to each of the three last alveoli and distolabial to the last alveolus on the left maxillary Institutional abbreviation MUSM, Museo de Historia Natu- tooth row, whereas exostoses are mesiolabial to each of the six ral, Universidad Nacional Mayor de San Marco, Lima, Peru. posterior alveoli and distolabial to the last alveolus on the right side. On both sides, the dorsoventrally thickest and Specimen MUSM 1399, a subcomplete skull with associated mesiodistally longest exostoses occur along alveoli 2 and 3. mandible, teeth, hyoid bones, and atlas/axis. Apex of the For example, the exostosis mesiolabial to left tooth 2 is 30 mm rostrum and right orbit region missing. Found by M. Urbina long and 22 mm thick. A forward decrease of the size of the in the locality of Cerro la Bruja, Pisco Basin (geographic exostoses is conspicuous on the right side, with the anteriormost coordinates: S 14° 31' 27.9''–W 75° 40' 13.0''). Lower level exostosis being a small bud (9 mm long mesiodistally and 6 mm (CLB) of the Pisco Formation, late middle to early late Mio- thick) between teeth 6 and 7. The surface of the exostoses is cene (ca.13–11 Ma; de Muizon 1988). Closely related to indented with pits and grooves, but the general outline is round- Acrophyseter deinodon, this specimen is provisionally identi- ed and the bone is at least superficially compact. The observa- fied as Acrophyseter sp., pending a more detailed comparison. tion of a well-defined depression on the root of the slightly ventrally shifted left teeth 2 and 3, matching the outline of the Tooth count The anterior of the rostrum being absent, the corresponding exostosis, indicates an originally tight exostosis- tooth counts in the description below start from the posterior to-tooth contact and suggests that these exostoses developed end of the tooth rows. concomitantly to the growth of the corresponding teeth.

Fig. 2 Schematic left lateral view of the skull and mandible of Acrophyseter sp. MUSM 1399. Dotted lines and uniform shaded areas correspond to reconstructed parts; parallel hatching indicates break surfaces; cross hatching indicates sediment. E effort force resulting from joined action of adductor muscles; R resistance force applied on upper teeth during bite; r resistance lever arm from craniomandibular joint to a given upper tooth; mm masseter muscles; tm temporalis muscles. Scale bar 100 mm 520 Naturwissenschaften (2014) 101:517–521

Discussion pressure exerted on upper teeth at various levels of the upper jaw (resistance force, R), it is obvious that during a bite, the Based on their nodular shape and their position along the posterior teeth and surrounding bone tissue will undergo a maxillary alveoli, these exostoses are identified as buccal higher pressure than more anterior teeth. Indeed, the resistance maxillary exostoses, benign oral bony outgrowths common force at one level will be inversely proportional to the length in some human populations (Horning et al. 2000; Pechenkina of the resistance lever arm (r)(Seagars1982). Therefore, if and Benfer 2002; Sawair et al. 2009). Although buccal exos- buccal exostoses around the teeth indeed correspond to a toses are reported in various carnivorans (Verstraete et al. reaction to intense occlusal forces, posterior exostoses are 1996; Schandorff 1997), these exostoses do not resemble expected to be larger than the more anterior exostoses, a any of the bony growths or pathologies in odontocetes condition observed in MUSM 1399. (Miles and Grigson 1990). Well-studied in humans, the etiol- Finally, a buttressing hypothesis would be especially rele- ogy of buccal exostoses is not completely known, involving vant if a large part of the tooth is outside the bony alveolus. both genetic predisposition and environmental factors, includ- This is the case in many archaeocetes and odontocetes (e.g., ing on one hand, damage/inflammation of the gingival tissue Fordyce 1994;Uhen2004), but even more pronounced in and on the other hand, severe occlusal stress (Pechenkina and physeteroids due to continuous deposition of cement on the Benfer 2002). A prevailing hypothesis of its etiology in outer surface of the root. Consequently, a large part of the root humans is a regular increased lateral pressure from the roots is held in the less rigid gum (Bianucci and Landini 2006), of the underlying teeth (Pechenkina and Benfer 2002), and increasing the stresses on the alveolus margins if the tooth cases of buccal exostosis formation following trauma exist undergoes transverse loads. Moderately thickened portions of (Bhusari et al. 2011). However, some evidence points to the the maxilla on the labial side of anterior upper alveoli of old role of periodontal ischemia in the alveolar bone playing the individuals of the delphinids Orcinus orca (killer whale) and more significant role (Horning et al. 2000). Gardner’ssyn- Pseudorca crassidens (false killer whale) (pers. obs.) may drome, an autosomal dominant polyposis, can cause osteomas correspond to similar stresses on the anterior part of the jaws. to form in the maxillofacial region (Fonseca et al. 2007; Therefore, we propose occlusal stress as the main Cankaya et al. 2012), but these osteomas are readily distin- factor leading to the development of buccal exostoses guishable and much less regular than the exostoses in MUSM in MUSM 1399. If correct, this interpretation would 1399. Furthermore, in MUSM 1399 local damage or inflam- constitute direct evidence for heavy forces exerted on mation of the gingival tissue seems an unlikely cause, due to teeth and surrounding tissues in this animal, corroborat- (a) the regular spacing and position of the exostoses, (b) their ing the important bite forces suggested by the size of regular shape and well-defined boundaries, (c) their presence the temporal fossae and the robustness of the teeth and on both sides, and (d) the absence of damage on adjoining jaws. To conclude, we think that buccal exostoses ob- dental roots. served in MUSM 1399 provide corroborating evidence In humans, if gingival damage is excluded, buccal for a macroraptorial feeding interpretation of the stem exostoses are proposed to work as buttresses, strength- physeteroid Acrophyseter. Contrasting with the suction- ening the alveolar processes facing excessive occlusal feeding modern sperm whales, Acrophyseter and several forces (Pechenkina and Benfer 2002; Sathya et al. morphologically similar other Miocene raptorial sperm 2012). Considering the oral morphology of MUSM whales were major marine macropredators. Among ma- 1399, such a mechanical explanation, would imply sev- rine tetrapods, a similar ecological niche is nowadays eral features. First, the exostoses should be located in predominantly filled by the cosmopolitan medium-size areas where the transverse loads are the most important. killer whale, while during the middle to late Miocene, Due to the narrow space between succeeding teeth and macroraptorial sperm whales displayed a broad size the close fit of opposing teeth in Acrophyseter,asindi- range, from medium size (Acrophyseter 4–4.5 m), to cated by long occlusion facets, labial and lingual sides larger (Brygmophyseter and Zygophyseter 6.5–7m), are the most adequate for additional buttressing of the and even giant (Livyatan 13.5–17.5 m) forms teeth. Although we only have partial access to the (Bianucci and Landini 2006; Lambert et al. 2008, 2010). lingual portion of the tooth row, visible exostoses seem to have their maximum extent on the labial side. Acknowledgments We thank W Aguirre, E Díaz, R Salas- Secondly, if we consider a simplified lever arm model for Gismondi, and M Urbina for giving us access to the specimen the bite of odontocetes (Turnbull 1970; Seagars 1982; and for its final preparation. Constructive comments from C de Westneat 2004)(Fig.2), with the craniomandibular joint as Muizon, ND Pyenson, and two anonymous reviewers considerably axis of rotation, different adductor muscles (temporal, masse- enhanced the quality of the article. This work was financially supported by MIUR grant (PRIN 2012YJSBM, resp. GB), SYNT ter, and pterygoid muscles) providing the directions for the HESYS grant (BE-TAF-2842, GB), and Return Grant of the Bel- exerted bite forces (mean effort force, E), and the resulting gian Federal Science Policy Office (2012–April 2013, OL). Naturwissenschaften (2014) 101:517–521 521

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