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Rostral Densification in Beaked Whales: Diverse Processes for A C. R. Palevol 10 (2011) 453–468 Contents lists available at ScienceDirect Comptes Rendus Palevol www.sciencedirect.com General palaeontology, systematics and evolution (Vertebrate palaeontology) Rostral densification in beaked whales: Diverse processes for a similar pattern La densification du rostre des baleines à bec : des processus variés pour un résultat similaire Olivier Lambert a,∗,b, Vivian de Buffrénil a, Christian de Muizon a a Département histoire de la terre, Muséum national d’histoire naturelle, UMR 7207 (paléobiodiversité et paléoenvironnements), (MNHN, CNRS, UPMC), CP 38, 57, rue Cuvier, 75005 Paris, France b Département de paléontologie, institut royal des sciences naturelles de Belgique, Bruxelles, Belgium article info abstract Article history: As compared to other odontocetes (toothed whales), the rostrum of beaked whales (family Received 24 September 2010 Ziphiidae) often displays extensive changes in the shape, thickness, and density of its con- Accepted after revision 21 March 2011 stituent bones. Previous morphological observations suggested that these modifications Available online 31 May 2011 appeared in parallel in different ziphiid lineages. However, very few data were available on the compactness and histology of these rostral bones, which precluded the study of the pro- Written on invitation of the Editorial Board. cesses at work for the development of such structures, as well as the interpretation of their functional implications. In this work we review the bibliographic data on the anatomy of the Keywords: ziphiid rostrum and we add new observations on adults of several extinct and extant taxa. Odontoceti Ziphiidae These observations are based on CT scans and transverse histological sections. Our results Beaked whales confirm that different bones (vomer, mesethmoid, premaxilla, maxilla) are involved in the Pachyostosis various morphologies displayed by ziphiid rostra. Strong density contrasts are detected Osteosclerosis between bones and/or inside the bones themselves; for example, parts of the rostrum Computed tomography reach densities in the range of Neoceti ear bones, which are among the densest bones Bone histology known hitherto. Furthermore, the histology of the pachyostotic and osteosclerotic bones proves to change from one taxon to the other; the degree of Haversian remodeling varies strongly between species: it can be absent (e.g. Aporotus recurvirostris), partial (e.g. aff. Ziphi- rostrum), or complete (e.g., Mesoplodon densirostris). The atypical secondary osteons known to be responsible for bone hypermineralization in the rostrum of M. densirostris occurred also in Choneziphius sp. Confronted with a phylogenetic framework, these anatomical and histological observations indicate that the acquisition of compact (osteosclerotic) and/or swollen (pachyostotic) bone is the result of a broad convergence between taxa, in response to common selective pressures. The functional dimension of this question is discussed with respect to what is known about extant ziphiid ecology. © 2011 Académie des sciences. Published by Elsevier Masson SAS. All rights reserved. résumé Mots clés : Comparé aux autres odontocètes (cétacés à dents), le rostre des baleines à bec (famille des Odontoceti Ziphiidae) est souvent sujet à d’importantes modifications de la forme, de l’épaisseur, et Ziphiidae de la densité des os qui le constituent. Des observations préliminaires ont suggéré que Baleines à bec ces modifications se sont développées en parallèle dans plusieurs lignées de ziphiidés. Pachyostose Cependant, très peu de données étaient disponibles sur la compacité et l’histologie des os du ∗ Corresponding author. E-mail address: [email protected] (O. Lambert). 1631-0683/$ – see front matter © 2011 Académie des sciences. Published by Elsevier Masson SAS. All rights reserved. doi:10.1016/j.crpv.2011.03.012 454 O. Lambert et al. / C. R. Palevol 10 (2011) 453–468 Ostéosclérose rostre, ce qui a empêché l’étude des processus à l’œuvre dans le développement de Tomographie informatisée telles structures, ainsi que l’interprétation des implications fonctionnelles de celles-ci. Histologie osseuse Dans ce travail, nous passons en revue les données bibliographiques sur l’anatomie du rostre des ziphiidés et ajoutons des observations nouvelles sur les adultes de plusieurs taxons éteints et actuels. Ces observations ont été collectées à l’aide de deux moyens : la tomographie informatisée et la confection de lames minces transversales. Nos résul- tats confirment que des os différents (vomer, mésethmoïde, prémaxillaire, maxillaire) sont impliqués dans les changements morphologiques variés, observés dans différents taxons de ziphiidés. De forts contrastes de densité sont également détectés entre les os et/ou au sein des os eux-mêmes ; certaines parties du rostre atteignent, par exem- ple, des densités similaires à celle des os de l’oreille des Neoceti, qui figurent parmi les plus denses connus. De plus, l’histologie des os pachyostotiques et ostéosclérotiques s’est avérée changer d’un taxon à l’autre ; le degré du remaniement haversien varie fortement entre les espèces : il peut être nul (e.g., Aporotus recurvirostris), partiel (e.g., aff. Ziphi- rostrum), ou complet (e.g., Mesoplodon densirostris). Des ostéones secondaires atypiques, connus comme étant responsables d’une hyperminéralisation osseuse dans le rostre de M. densirostris, sont également détectés dans Choneziphius sp. Confrontées à un cadre phy- logénétique, ces observations anatomiques et histologiques indiquent que l’acquisition d’os compacts (ostéosclérotiques) et/ou renflés (pachyostotiques) est le résultat d’une conver- gence entre taxons, en réponse à des pressions de sélection communes. L’aspect fonctionnel de cette question est discuté, en rapport avec ce qui est connu de l’écologie des ziphiidés actuels. © 2011 Académie des sciences. Publié par Elsevier Masson SAS. Tous droits réservés. 1. Introduction 1997; Zylberberg et al., 1998). In several extinct taxa, the mesorostral groove is dorsally closed by the thickened and Beaked whales (Ziphiidae) form a diversified fam- compact premaxillae, which, in some cases, form elevated ily of odontocetes (toothed whales), including 21 extant longitudinal crests (Lambert, 2005), whereas large rostral species and six genera. Predominantly teuthophagous, maxillary crests are observed at the rostrum base of the most ziphiids are considered as deep divers, with dive extant Hyperoodon spp. At least in Hyperoodon ampullatus records at more than 1800 m for some species (Hooker the development of these crests is a sexually dimorphic and Baird, 1999; Schreer and Kovacs, 1997; Tyack et al., character (Mead, 1989b). 2006), depths at which prey are detected by echolocation The preliminary observation of the diverse morpholog- (Johnson et al., 2004). With exception for Tasmace- ical peculiarities of ziphiid rostra leads to the assumption tus shepherdi, all extant ziphiids display an important that pachyosteosclerosis, the combination of pachyostosis, reduction of their dentition related to suction feeding or swollen, protuberant periosteal cortices, and osteoscle- (Heyning and Mead, 1996; Werth, 2006): only one or rosis, an increase in bone inner compactness (de Buffrénil two pairs of mandibular teeth are retained, modified in and Rage, 1993; de Ricqlès and de Buffrénil, 2001), was a tusks that generally erupt in adult males only. Dental common feature in ziphiids, occurring independently in reduction is similarly observed in several of the extinct multiple lineages (Bianucci et al., 2007; Lambert, 2005). species known hitherto, whereas others (e.g., Messapicetus However, this assumption was based on a superficial obser- spp., Ninoziphius platyrostris) retain numerous homod- vation of the skulls, lacking a detailed analysis of their inner ont rostral and mandibular teeth (Bianucci et al., 2007, organization and histological features. Furthermore, vari- 2010; de Muizon, 1984; Lambert, 2005; Lambert et al., ous potential function(s) of a pachyosteosclerotic rostrum 2009). in ziphiids have been proposed in the past, in relation- In addition, the ziphiid skull, and specially its rostral ship with three different ecological or behavioral traits of region, is often modified, as compared to the typical con- extant taxa: echolocation, deep diving, and intraspecific dition of other odontocetes (Bianucci et al., 2007; Heyning, fights between males (de Buffrénil et al., 2000; Heyning, 1989a; Lambert, 2005). Various changes in the general 1984; Lambert et al., 2010a; MacLeod, 2002). Until now, shape, thickness, and inner compactness of its constituent none of these functional hypotheses can explain the full bones have been described in both extinct and extant range of patterns observed. taxa. The most common modification is a filling of the The present study investigates, from morphological and mesorostral groove by the thickened vomer (Bianucci et al., structural points of view, the diversity of forms displayed 2007; Fraser, 1942; Heyning, 1989b; Mead, 1989a). In the by the ziphiid rostrum bones. The aim is to elucidate the extant species Mesoplodon densirostris, the only ziphiid growth processes at work in the different lineages, and to to have been studied in detail from an osteohistological bring new data that could enrich the discussion of func- point of view, the filling of the groove is accompanied tional hypotheses. In addition to a review of published by a strong increase of the compactness and mineral- data, we bring new information on bone compactness
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