As compared to other odontocetes (toothed whales), the rostrum of beaked whales (family Ziphiidae) often displays extensive changes in the shape, thickness, and density of its constituent bones. Previous morphological observations suggested that these modifications 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 processes 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 ziphiid rostrum and we add new observations on adults of several extinct and extant taxa. These observations are based on CT scans and transverse histological sections. Our results confirm that different bones (vomer, mesethmoid, premaxilla, maxilla) are involved in the various morphologies displayed by ziphiid rostra. Strong density contrasts are detected between bones and/or inside the bones themselves; for example, parts of the rostrum reach densities in the range of Neoceti ear bones, which are among the densest bones 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. Ziphirostrum), 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.
Comparé aux autres odontocètes (cétacés à dents), le rostre des baleines à bec (famille des Ziphiidae) est souvent sujet à d’importantes modifications de la forme, de l’épaisseur, et de la densité des os qui le constituent. Des observations préliminaires ont suggéré que ces modifications se sont développées en parallèle dans plusieurs lignées de ziphiidés. Cependant, très peu de données étaient disponibles sur la compacité et l’histologie des os du rostre, ce qui a empêché l’étude des processus à l’œuvre dans le développement de telles structures, ainsi que l’interprétation des implications fonctionnelles de celles-ci. 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 résultats 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 exemple, 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. Ziphirostrum), 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 phylogénétique, ces observations anatomiques et histologiques indiquent que l’acquisition d’os compacts (ostéosclérotiques) et/ou renflés (pachyostotiques) est le résultat d’une convergence 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.
Odontoceti, Ziphiidae, Beaked whales, Pachyostosis, Osteosclerosis, Computed tomography, Bone histologyOdontoceti, Ziphiidae, Baleines à bec, Pachyostose, Ostéosclérose, Tomographie informatisée, Histologie osseusepresentedWritten on invitation of the Editorial Board.Introduction
Beaked whales (Ziphiidae) form a diversified family of odontocetes (toothed whales), including 21 extant species and six genera. Predominantly teuthophagous, most ziphiids are considered as deep divers, with dive records at more than 1800 m for some species (Hooker and Baird, 1999, Schreer and Kovacs, 1997 and Tyack et al., 2006), depths at which prey are detected by echolocation (Johnson et al., 2004). With exception for Tasmacetus shepherdi, all extant ziphiids display an important reduction of their dentition related to suction feeding (Heyning and Mead, 1996 and Werth, 2006): only one or two pairs of mandibular teeth are retained, modified in tusks that generally erupt in adult males only. Dental reduction is similarly observed in several of the extinct species known hitherto, whereas others (e.g., Messapicetus spp., Ninoziphius platyrostris) retain numerous homodont rostral and mandibular teeth (Bianucci et al., 2007, Bianucci et al., 2010, de Muizon, 1984, Lambert, 2005 and Lambert et al., 2009).
In addition, the ziphiid skull, and specially its rostral region, is often modified, as compared to the typical condition of other odontocetes (Bianucci et al., 2007, Heyning, 1989a and Lambert, 2005). Various changes in the general shape, thickness, and inner compactness of its constituent bones have been described in both extinct and extant taxa. The most common modification is a filling of the mesorostral groove by the thickened vomer (Bianucci et al., 2007, Fraser, 1942, Heyning, 1989b and Mead, 1989a). In the extant species Mesoplodon densirostris, the only ziphiid to have been studied in detail from an osteohistological point of view, the filling of the groove is accompanied by a strong increase of the compactness and mineralization rate of all rostrum bones (maxillae, premaxillae, and vomer), with strong implications for their mechanical properties (de Buffrénil and Casinos, 1995, Zioupos et al., 1997 and Zylberberg et al., 1998). In several extinct taxa, the mesorostral groove is dorsally closed by the thickened and compact premaxillae, which, in some cases, form elevated longitudinal crests (Lambert, 2005), whereas large rostral maxillary crests are observed at the rostrum base of the extant Hyperoodon spp. At least in Hyperoodon ampullatus the development of these crests is a sexually dimorphic character (Mead, 1989b).
The preliminary observation of the diverse morphological peculiarities of ziphiid rostra leads to the assumption that pachyosteosclerosis, the combination of pachyostosis, or swollen, protuberant periosteal cortices, and osteosclerosis, an increase in bone inner compactness (de Buffrénil and Rage, 1993 and de Ricqlès and de Buffrénil, 2001), was a common feature in ziphiids, occurring independently in multiple lineages (Bianucci et al., 2007 and Lambert, 2005). However, this assumption was based on a superficial observation of the skulls, lacking a detailed analysis of their inner organization and histological features. Furthermore, various potential function(s) of a pachyosteosclerotic rostrum in ziphiids have been proposed in the past, in relationship with three different ecological or behavioral traits of extant taxa: echolocation, deep diving, and intraspecific fights between males (de Buffrénil et al., 2000, Heyning, 1984, Lambert et al., 2010a and MacLeod, 2002). Until now, none of these functional hypotheses can explain the full range of patterns observed.
The present study investigates, from morphological and structural points of view, the diversity of forms displayed by the ziphiid rostrum bones. The aim is to elucidate the growth processes at work in the different lineages, and to bring new data that could enrich the discussion of functional hypotheses. In addition to a review of published data, we bring new information on bone compactness and histology in several extinct and extant taxa thanks to two techniques: computed tomography (or CT scans) and ground sections.
Material and methodsRemarks on information sources
Two information sources were exploited, bibliographic data and first hand observations.
Bibliographical data
A rich set of bibliographic information dealing with rostrum anatomy in various extant and extinct ziphiids, and specially stressing the relationships between the modified rostral bones (premaxillae, maxillae, vomer, and mesethmoid), was considered (Besharse, 1971, Bianucci et al., 2007, Bianucci et al., 2008, Bianucci et al., 2010, Fraser, 1942, Glaessner, 1947, Hardy, 2005, Heyning, 1984, Heyning, 1989a, Heyning, 1989b, Lambert, 2005, Lambert et al., 2010a, Lambert et al., 2010b, Leidy, 1877, MacCann, 1965, MacLeod and Herman, 2004, Mead, 1975a, Mead, 1989a, Mead, 1989b, Miyazaki and Hasegawa, 1992, Moore, 1968, Post et al., 2008, Raven, 1942, Reyes et al., 1991 and True, 1910). A second set of published works focusing on the histology and mechanical properties of the rostrum of the extant M. densirotris was also considered (de Buffrénil and Casinos, 1995, de Buffrénil et al., 2000, Rogers and Zioupos, 1999, Zioupos et al., 1997 and Zylberberg et al., 1998). Finally, a few recent works investigating the anatomy of some extant ziphiid skulls by means of X-ray analyses were also taken into account (Cozzi et al., 2010 and Cranford et al., 2008).
First hand observation
New information, mainly dealing with the inner structure of the rostral region of ziphiid skulls, was collected along two main axes:
three-dimensional mapping of bone density using computed tomography;
histological examinations based on ground sections.
Biological sample and analyses performedExtinct ziphiids
New observations of fossil material were made on the five taxa listed below. Aporotus recurvirostris (Neogene of Antwerp area, Belgium) IRSNB 3810-M. 2012 a–b, right part of the rostrum, including the subcomplete premaxilla and adjacent remnants of the maxilla, ground sections; Choneziphius planirostris (Late Miocene of Antwerp area, Belgium) IRSNB 3775-M.1883, partial skull including rostrum and facial area, figured in Lambert, 2005, CT scan; Choneziphius sp. (Neogene of Antwerp area, Belgium) MB CR-15, apex of rostrum, ground sections; aff. “Mesplodon” longirostris (Neogene of Antwerp area, Belgium) IRSNB 3804, partial skull including rostrum and facial area, ground sections; aff. “M.” longirostris (Neogene of Antwerp area, Belgium) MB CR-9, left part of the rostrum, ground sections; aff. “M.” longirostris (Neogene of Antwerp area, Belgium) MB CR-10, anterior part of the rostrum, ground sections; Ziphirostrum marginatum (Neogene of Antwerp area, Belgium) MB CR-13, rostrum base fragment, right side, ground sections; Z. recurvus (Neogene of Antwerp area, Belgium) IRSNB 3805-M.544, rostrum, figured in Lambert, 2005, CT scan; aff. Ziphirostrum (Neogene of Antwerp area, Belgium), rostrum base fragment, right side, ground sections. Based on the complete closure of the sutures between rostral bones, we estimate that all the specimens examined were adult.
The stratigraphic context is unfortunately not known precisely for many of the fossil specimens discussed here. Either they have been reworked and found in basal gravel layers, or they were dredged from the bottom of the sea (Bianucci et al., 2007 and Lambert, 2005). Therefore, for most of them we can give only an approximate geological age.
Even if the extinct species “M.” longirostris and “M.” tumidirostris have been described from isolated rostrum elements (Cuvier, 1823 and Miyazaki and Hasegawa, 1992) that were shown to be of low diagnostic value (Bianucci et al., 2007), we choose to maintain the original attribution to the genus Mesoplodon (between quoting marks) to stress their obvious affinities with this genus. We agree that the final genus and species attribution of the specimens displaying similarities with the original material of these taxa will depend of the description of more complete skulls, from the same stratigraphic levels.
Each skull was scanned with a standard medical X-ray tomograph (Siemens AS + 128 slices), producing transverse slices of 0.6 mm thickness. For all specimens, the scanner was operated at 120 kV, 350 mAs. Mimics software (version 13.1) allowed the extraction of transverse sections and three-dimensional reconstructions of the skulls based on the sections.
In addition to the identification of sutures between bones (when not fused), CT scans provide access to bone mineral density (BMD), a morphometric parameter commonly used in medicine, combining local bone compactness (or trabecular volume) and mineral content of the osseous tissue (Meunier and Boivin, 1997). This parameter was not quantified in the present study (not calibrated with rods of known density), but considered in qualitative terms only, through a visual assessment of the local variation of X-ray opacity (white or grey values). For example, a roughly similar X-ray opacity could be noted between the ear bones and some portions of the rostrum in ziphiids. Neoceti (Odontoceti + Mysticeti) ear bones are made of one of the densest bone tissues described hitherto (Currey, 2002, de Buffrénil et al., 2004 and Nummela et al., 1999). Using the threshold algorithm in Mimics we isolated parts of the skull displaying a given density range and produced three-dimensional reconstructions of these high-density parts, in a way similar to Cranford et al. (2008).
Ground sections
Ground sections were made from rostrum fragments from extinct taxa (see list above), according to the classic technique for this kind of preparations (de Buffrénil and Mazin, 1989). All sections were made transversely, i.e., perpendicular to the longitudinal axis of the rostrum. They were observed at low (25×) and medium (200×) power magnification of a microscope, in natural and polarized light. The quantification of bone compactness, or parameter C, was performed on sketches of the sections made with a camera lucida (magnification 40–50×; minimum size of cavities: 20 μm), using the software Bone Profiler (Girondot and Laurin, 2003). Because all the sections were relatively large (at least 8–12 cm2) and displayed a very homogeneous compactness, measurements were made for each section in six to nine fields 2.5 × 2.5 mm, evenly distributed within the sectional area, and finally averaged to give a mean indication.
The terminology used in this study for describing bone structure and histology refers to Francillon-Vieillot et al. (1990).
Phylogeny
The phylogenetic background of the discussion is a composite phylogeny based on several phylogenetic analyses available in literature (Bianucci et al., 2007, Bianucci et al., 2010 and Lambert, 2005). It must be noted that the phylogenies taken into account refer to morphological characters only, including those related to the closure or filling of the mesorostral groove by rostral bones. The main features discussed in the text can be summarized as four characters:
char. 1, filling of the mesorostral groove: vomer (0) – absent (1) – mesethmoid (2);
char. 2, dorsal closure of the mesorostral groove by the thickened premaxillae: absent (0) – present (1);
char. 3, degree of remodeling of the compact rostrum bones: absent (0); partial (1); complete (2);
Character states are given in Table 1. Using MacClade 4 (Maddison and Maddison, 2005), we optimized the characters 1–3 on the composite tree under linear parsimony (see Swofford and Maddison, 1987). The derived state for character 4 is for now observed only in two taxa. Finally, with Mesquite (Maddison and Maddison, 2010) we used random taxon reshuffling on the reference phylogeny to assess the presence of a phylogenetic signal for each of the characters above (Laurin, 2004), a method that can also be used for discrete characters (Laurin, 2005). Ten thousands trees were randomly generated, and the number of steps for the given character has been compared between the reference phylogeny and the random trees. If the number of steps is lower in the reference tree than in at least 95% of the generated trees, it can be concluded that a phylogenetic signal is detected for the studied character (Laurin, 2004).
Institutional abbreviations
IRSNB: Institut Royal des Sciences Naturelles de Belgique, Brussels, Belgium; MB CR: private collection of Mark Bosselaers, Berchem, Belgium; MNHN: Muséum National d’Histoire Naturelle, Paris, France; SAM: Iziko South African Museum, Cape Town, South Africa; USNM: United States National Museum of Natural History, Washington DC, USA.
Results
By far the most common (and much likely plesiomorphic) condition of the rostrum in odontocetes is a mesorostral groove void of bone or other mineralized tissue (Fig. 1a, b) and only filled with the mesorostral cartilage, an anterior extension of the nasal septum (Cozzi et al., 2010 and Mead and Fordyce, 2009). The groove is laterally and ventrally bordered by the vomer, which is usually thin on the lateral walls of the groove (Fig. 1a, b). Dorsally, the groove is often partly overhung by the dorsal portion of the premaxillae that forms a thin plate with a transversely convex, smooth and hard dorsal surface (i.e., porcelanous part in Mead and Fordyce, 2009). This porcelanous part is often made of compact, intensely remodeled bone (de Buffrénil and Lambert, 2011), contrasting with the more spongy aspect of the ventral part of the premaxilla and of the maxilla, with exception for the palatal cortex of this bone (e.g. Delphinus delphis).
Different bones, different shapes
A synthesis of previous works (Bianucci et al., 2007 and Lambert, 2005), new external observations of the skull anatomy, and CT scans altogether suggest that the diverse modifications of the rostrum shape in ziphiids can be classified in several distinct groups. However, we acknowledge that the limits of these groups are not always sharply defined. For example, in some cases where the premaxillae dorsally close the mesorostral groove (e.g., Choneziphius), the vomer is significantly thickened in the groove, and the maxillae display an increased width lateral and dorsolateral to the groove. In other cases the inner sutures are fused and the degree of involvement of each rostral bone is difficult to establish (e.g., M. densirostris; de Buffrénil and Casinos, 1995). The classification proposed here is the following.
Filling of the mesorostral groove by the vomer
Africanacetus †, Ihlengesi †, Izikoziphius †, Khoikhoicetus †, Mesoplodon, “M.” longirostris †, “M.” tumidirostris †, Microberardius †, Pterocetus †, Xhosacetus †, Ziphius (Fig. 2; char. 1, state 0). Sexual dimorphism has been demonstrated for this character in Ziphius cavirostris and at least some species of Mesoplodon, in which the filling is more advanced in adult males than in young males and females (Heyning, 1984, Heyning, 1989b, MacLeod and Herman, 2004 and Mead, 1989a). Nevertheless, it should be noted that some degree of filling has been observed in adult females of some species (Reyes et al., 1991). An incipient development of this condition is observed in a sexually mature female Tasmacetus shepherdi (USNM 484878, Mead and Payne, 1975), in which the lateral walls of the vomer in the posterior region of the mesorostral groove are distinctly thickened. This condition provides to the mesorostral groove a V-shaped section (Fig. 3), instead of a U-shaped section as is commonly observed in odontocetes with an unmodified groove (e.g., Delphinus, Ninoziphius). Unfortunately we could not perform a CT scan of the skull of Tasmacetus during this study. In some cases the vomer reaches a dorsal level considerably higher than the premaxillary margins of the mesorostral groove (e.g. the extant Mesoplodon carlhubbsi, Heyning, 1984). The high elevation of the vomer above the mesorostral groove at the rostrum base is associated with a distinct bulge in the extinct species “M.” tumidirostris (Miyazaki and Hasegawa, 1992).
No thickening or filling (char. 1, state 1; char. 2, state 0)
Indopacetus, Nazcacetus †, Ninoziphius †. Among the six described specimens of the extant Indopacetus pacificus, including only one possible adult male, none displays an extensive filling of the mesorostral groove (Dalebout et al., 2003). Only one specimen of Nazcacetus urbinai and two specimens of Ninoziphius platyrostris were observed. The small samples available for these two extinct species leave open the question of sexual dimorphism; it is possible that only females were discovered until now.
Partial filling of the mesorostral groove by the mesethmoid
Berardius, Microberardius? †, Nenga † (Fig. 4; char. 1, state 2). In the specimens of Berardius arnuxii in which this feature has been observed, the outer surface of the mesethmoid is made of spongy bone.
Dorsal closure of the mesorostral groove by the thickened premaxillae
Aporotus †, Beneziphius †, Choneziphius †, Messapicetus †, Tusciziphius †, Ziphirostrum † (Fig. 5; char. 2, state 1). A mesorostral canal remains open, although its diameter varies from one species, or one specimen, to another. Above the canal, the premaxillae either remain separated (e.g. Aporotus), or more often display a sutural contact, with a varying degree of fusion between the premaxillae (Fuller and Godfrey, 2007, fig. 4). In some cases the premaxillae either form joined high longitudinal crests, in contact with (but not fused to) each other, as exemplified by Aporotus, or a single medial crest on the rostrum (e.g., Tusciziphius). In both cases, the volume of the premaxillae is significantly increased.
Combination of filling of the mesorostral groove by the vomer and dorsal closure by the thickened premaxillae (char. 1, state 0; char. 2, state 1)
Z. recurvus †. In this case the mesorostral groove is completely closed and the rostrum is massive and much higher than wide (see description of growth marks farther in the text and Lambert, 2005, fig. 15).
Development of high rostral maxillary crests, at the rostrum base
Hyperoodon (Fig. 6). Sexual dimorphism has been demonstrated for this character in at least H. ampullatus; adult males bear much higher crests (Hardy, 2005 and Mead, 1989b). Here again, the increase in bone volume is very important. Considerably lower crests medial or lateral to the antorbital notch have been described in various extinct and extant ziphiids (Mead and Fordyce, 2009, Diagram 2); the most conspicuous dome-like crests, in the extinct Africanacetus ceratopsis, are much less developed than in Hyperoodon spp. (Bianucci et al., 2007).
Bone compactness
Based on the one hand, on CT scans of specimens of extant species and, on the other hand, on ground sections of fossil specimens, we obtained, respectively, qualitative and quantitative compactness assessments for the different bones constituting the rostrum.
As mentioned above, for rostrum bones in non-ziphiid odontocetes (e.g., D. delphis, M. monoceros) and in ziphiid specimens devoid of conspicuous local specialization of skull bones (e.g., female M. bidens MNHN 1975-112), compact bone is often observed at the level of the thin premaxillae above the mesorostral groove and on the palatal portion of the maxillae (Fig. 1b).
In adult males of M. layardii and Z. cavirostris, the mesorostral groove is filled by the vomer, and the dorsal part of the vomer and the dorsomedial part of the premaxillae are much more compact than the surrounding bones (Fig. 7 and Fig. 8). In both cases, the limits of the bones do not match the marked changes in compactness. Compact bone extends on the posterior part of the premaxilla, until the vertex, as observed in Z. cavirostris by Cranford et al. (2008). However, compact bone is predominantly concentrated in the rostrum, becoming thinner towards the vertex. An in situ periotic (ear bone) in the scanned skull of Z. cavirostris fits the range of compactness of the most compact rostrum bones of this specimen.
As already suggested by Hardy (2005), the maxillary crests of the young H. ampullatus are much less compact than the thin plate of premaxilla overhanging the mesorostral groove and than the ear bones (Fig. 9). Unfortunately, due to size constraints we could not scan the skull of a large adult male of this species (MNHN 1872-491), but the external surface of its crests is distinctly spongy (Fig. 6b), corroborating the scans of the young specimen.
A previous study based on ground sections of M. densirostris (de Buffrénil and Casinos, 1995) yielded an extremely high value of compactness (99%) for all the bones of the rostrum, with completely fused sutures. Compactness is similarly high in rostrum fragments from Choneziphius sp. and aff. Ziphirostrum, and in the whole rostrum of two specimens of the extinct aff. “M.” longirostris, where only some of the sutures can be distinguished on the sections. In the rostrum of A. recurvirostris, a different condition is observed: the hyperplasic premaxilla (i.e. the cortex of this bone is much more developed than in other taxa, which induces a swollen aspect) is very compact (96.8–98.8%), whereas the maxilla is made of cancellous bone (C: 40–65%; de Buffrénil and Lambert, 2011).
Skull parts that are most commonly preserved in fossil ziphiids are the rostrum and the dorsal part of the cranium, sometimes including the vertex (Bianucci et al., 2007, Bianucci et al., 2008, Lambert, 2005 and Leidy, 1877). This typical preservation is much more frequent than in any other extinct odontocete group, and much likely results from the high compactness of these areas of the skull. More spongy bones simply disappear in the course of deposition, burial, and fossilization.
Bone histology
In the compact rostrum of the extant M. densirostris, all hypermineralized bones consist of a dense Haversian tissue, the secondary osteons of which display atypical features intermediate between parallel-fibered and woven-fibered bone (this tissue is monorefringent in transverse sections). This structure is very different from that of the lamellar bone usually observed in the walls of secondary osteons in adult mammals (de Buffrénil et al., 2000; Fig. 10e,f). In M. densirostris, the osseous tissue forming the walls of the osteons is characterized by a drastic reduction of its collagenous network, a feature that could explain the extremely high mineralization rate and physical density of the rostrum (2.612 to 2.686 g/cm3; de Buffrénil and Casinos, 1995 and Zylberberg et al., 1998). In addition to its exceptional mineralization rate, this kind of bone proved to be the stiffest and hardest ever observed, with a corresponding high brittleness (Zioupos et al., 1997).
Similar histological features are observed in a transverse section from the anterior part of the rostrum of Choneziphius sp. Here again the bone is completely remodeled, with the same type of atypical, longitudinally oriented secondary osteons made of monorefringent, non-lamellar osseous tissue (Fig. 10).
In the extinct aff. “M.” longirostris, a part of the sutures between rostral bones (vomer-maxilla and vomer-premaxilla) is not fused (Fig. 11). The dorsal portion of the vomer in the mesorostral groove is distinctly less remodeled than the ventral portion, the maxilla, and the premaxilla. This upper part of the vomer is mostly made of a fibrolamellar complex with a predominantly vertical orientation of the primary osteons (equivalent to a radial orientation in a tubular long bone). The secondary osteons observed in the rest of the rostral bones are more often longitudinally or obliquely oriented. They differ strikingly from the secondary osteons observed in M. densirostris and Choneziphius sp. because they display an alternate birefringence in polarized light, indicative of a true lamellar bone tissue characterized by an orthogonal alternation of lamellae (Fig. 11 g).
The association of non-remodeled and strongly remodeled compact bone is similarly observed in a dorsal fragment of the rostrum base of aff. Ziphirostrum. The location of these two types of tissue roughly corresponds to the premaxilla and the maxilla, respectively (Fig. 12). The clear alternate birefringence of the numerous longitudinally oriented secondary osteons forming the dense Haversian tissue indicates that osteon walls are made of typical lamellar bone.
From the medial area to the peripheral dorsolateral region of the swollen, hyperplasic premaxilla of A. recurvirostris, bone tissue type changes, within the general frame of fibrolamellar complexes, from reticular to laminar, and finally radiating bone, according to vascular orientation (Fig. 13). This succession likely reflects changes in the accretion rates of the bone tissue, with an initial high rate (reticular bone), an intermediate lower rate (laminar bone), and a final increase of the accretion rate (radiating bone). In the laminar bone, growth marks are conspicuous. The thickness of the growth layer groups (GLG) tends to increase from deep to superficial layers in the dorsal and dorsolateral parts of the bone. This indicates that sub-periosteal accretion rate was particularly fast in these directions, with a tendency to get still faster in time (de Margerie et al., 2002 and de Margerie et al., 2004). The premaxilla of Aporotus is entirely made of primary bone devoid of any kind of inner (especially Haversian) remodeling, with exception for a narrow zone along the medial wall of the bone. Conversely, the spongy maxilla of the same specimen was intensely remodeled (Fig. 13e), as is the general condition for this bone in mammals. Remodeling of the maxilla in A. recurvirostris is a first argument against the hypothesis of an age-related non-remodeling of the premaxilla. A second argument is the observation of 8 to 9 GLGs in this specimen, each of them supposed to represent one year in the life of the animal (de Buffrénil and Lambert, 2011). Therefore, this specimen must have died in its 9th or 10th year. Among extant ziphiids, the few data available indicate that sexual maturity is reached at 7–11 dental GLGs in Hyperoodon ampullatus (Benjaminsen and Christensen, 1979), and occurred at 9 GLGs in one female M. densirostris (Ross, 1984). These comparative elements suggest that the studied specimen of A. recurvirostris was a young adult or, at least, a late subadult. Furthermore, an absence or a low degree of remodeling is commonly observed in the laminar bone tissue of adults in other mammals, for example artiodactyls (Currey, 2002).
The macroscopic examination of fracture surfaces in the hyperplasic premaxillae of aff. Aporotus dicyrtus and Choneziphius planirostris (Fig. 14a–c; Lambert, 2005, fig. 18), and the examination of CT scan sections of the premaxilla of Z. recurvus (Fig. 14d) reveal clear growth marks in complete sequences. Therefore, it must be concluded that these bones were not remodeled, like those of A. recurvirostris.
To summarize, the degree of remodeling in ziphiid rostra strongly differs between taxa: secondary osteons can be developed in the whole rostrum (M. densirostris), or only in some bones (aff. “M.” longirostris, aff. Ziphirostrum). They can also be absent from the bones (otherwise pachyostotic and osteosclerotic) of other species (A. recurvirostris). Remodeling can also be restricted to a part only of a bone (e.g., vomer of aff. “M.” longirostris that is only remodeled in its ventral portion). With the exception of the atypical osteons of Choneziphius sp. and M. densirostris, secondary osteons in ziphiid rostra display a normal lamellar organization in transverse section. In all rostra for which ground sections of compact bone were available, a complete or subcomplete occlusion of vascular canals occurs. Since the precursor cells of the osteoclasts, the monocytes, are brought in situ via blood vessels, this observation would mean that the remodeling process of ziphiid rostral bones, though potentially intense, cannot proceed after canal closure and is thus limited in time (there is a trend to self-blockage of remodeling). This inference is confirmed by the lack or great sparseness of open erosion bays in all the taxa investigated.
Confrontation with phylogenetic framework
The data compiled here are summarized in a composite phylogenetic tree in Fig. 15. The optimization of the ancestral state for the characters 1–4 gave the following results. The ancestral state for char. 1 (filling of the mesorostral groove) is equivocal, depending on the choice of the Accelerated Transformation (AccTran) or Deleted Transformation (DelTran) hypothesis; either the filling by the vomer is ancestral (DelTran), subsequently lost in several clades and re-appearing in the clade Izikoziphius + Ziphius, or it appeared independently (AccTran) in numerous clades (Z. recurvus but not the other species of the genus Ziphirostrum, Tasmacetus, Izikoziphius + Ziphius, Xhosacetus, Pterocetus, Africanacetus + Ihlengesi + Mesoplodon + aff. “M.” longirostris). The derived filling of the groove by the mesethmoid appears in the clade Berardius + Microberardius (unknown in Archaeoziphius). However, it should be noted that when assessing the phylogenetic signal for char. 1, the number of steps in the reference tree is lower than in 94.61% of the randomly generated trees (probability 0.0539, Table 2), which is at the very limit of reliability for this character optimization. For char. 2 (dorsal closure of the groove by the thickened premaxillae) the ancestral state is similarly equivocal; either the closure occurs in the common ancestor of all ziphiids (AccTran) and is lost in several clades, or it appears independently (DelTran) in three clades (Aporotus + Beneziphius + Messapicetus + Ziphirostrum, Choneziphius, Tusciziphius). For this character the assessment of the phylogenetic signal provides a probability of 0.0104, which indicates a reliable character optimization. The ancestral state for char. 3 (degree of remodeling of compact rostral bone) is much likely a partial remodeling. Optimization proposes the absence of remodeling in Aporotus and possibly Beneziphius + Messapicetus, and complete remodeling in Mesoplodon and possibly Africanacetus + Ihlengesi. However, with a probability of 1 the optimization cannot be considered reliable. A similar unreliable result is achieved for char. 4 (presence of atypical osteons in remodeled bone), only observed for now in two distantly related taxa (Choneziphius and Mesoplodon).
Discussion
Although occurring in most ziphiids, be they extinct or extant, the morphological specialization of rostral bones is expressed in distinct ways among the various lineages. From an anatomical point of view, the bones involved in the changes of shape of the rostrum (vomer, mesethmoid, maxilla, premaxilla) differ considerably from one taxon to another. Furthermore, the optimization of ancestral states indicates a complex history with several convergences and reversions (Fig. 15). From a histological point of view, the limited sample of adult specimens studied hitherto suggests that the remodeling pattern of compact cortices also varies among taxa (no remodeling, partial remodeling, complete remodeling). In a same lineage, the extent of bone remodeling may deeply change from one taxon to another (Fig. 15; Aporotus and Ziphirostrum, M. densirostris and aff. “M.” longirostris). Furthermore, similar, atypical (monorefringent) secondary osteons can be observed in two taxa belonging to distantly related lineages (Choneziphius sp. and M. densirostris). Due to the preservation state of fossil specimens and the difficulty to gain access to samples of extant species, hypermineralization could be demonstrated for now only in M. densirostris (Zylberberg et al., 1998). With the exception of Choneziphius sp., the other taxa studied display osteons made of typical lamellar bone, a tissue known to have a high collagen content and a relatively low mineralization rate (Boivin and Meunier, 2002). However, further investigation of the mineral and collagen content of extant ziphiid rostra would be necessary to confirm this potentially important difference.
The high variation, at different levels of bone organization (at least anatomical and histological), of the detailed phenotypical expressions of rostrum specializations in the Ziphiidae strongly suggests that distinct processes were at work for the acquisition of such features in the various ziphiid lineages. Indeed, even if, as proposed by character optimization, the ancestral condition might be a mesorostral groove filled by the vomer or dorsally closed by the thickened premaxillae (both results equivocal), a great diversity of anatomical and histological specializations appears within this clade. These features do not simply represent a plesiomorphic feature inherited from stem-ziphiids; they would rather reflect a broad convergence between most ziphiid taxa (but not all taxa; cf. the cases of Indopacetus, Nazcacetus, and Ninoziphius), in response to (a) common selective pressure(s) arising from similar, but possibly not fully identical, ecological specializations (Bianucci et al., 2008).
This consideration raises, of course, the question of the functional implication(s) of the rostral specializations. A basic observation is that, beyond the diversity of processes, there is an obvious, factual result: increasing bone mass, stiffness, and physical density in the rostral region of the skull.
Several functions have been proposed for the compact rostrum bones of extant and extinct ziphiids. The most convincing hypotheses can be classified into three categories, related to three main functional and ecological features: acoustics, deep diving, and intraspecific fights between males (Cozzi et al., 2010, de Buffrénil et al., 2000, Heyning, 1984 and MacLeod, 2002).
In odontocetes, the production of echolocation sounds occurs in the forehead and the transmission is made through the melon (Cranford et al., 1996 and Mead, 1975b). Air sacs surrounding the phonic lips, the sound-producing organs in the forehead, may act as acoustic mirrors for echolocation and communication sounds. In the case of deep-diving ziphiids (for example, individuals of M. densirostris and Z. cavirostris have been recorded at depths up to 1251 and 1888 m, with dive durations reaching 57 and 85 min, respectively; Tyack et al., 2006), hydrostatic pressure strongly reduces the volume of air spaces. Density disparity between forehead tissues and highly compact bone could therefore constitute an alternative acoustic reflector (Cranford et al., 2008). This model is in agreement with the geometry of compact bone elements in the skull of several extant and extinct ziphiids, even if compact bone is preferentially located in the anterior part of the skull. However, unusual shapes of hyperplasic bones in various extinct ziphiid taxa are in poor agreement with this acoustic model alone. For example, the elevated medial crests of “M.” tumidirostris and Tusciziphius sp. are located anterior to the area of production of the echolocation sounds, and may therefore be considered more as an obstacle than as a reflector for the sounds to be transmitted forwards via soft tissues. Another even more problematic issue is the preferential development of compact bone in adult males of extant ziphiids. Indeed, the few data available hitherto do not allow the distinction of different echolocation or diving abilities between adult males and females/juveniles in a same ziphiid species (Hooker and Baird, 1999, Johnson et al., 2008, Johnson et al., 2004, MacLeod, 2002, Madsen et al., 2005 and Tyack et al., 2006).
As mentioned above, the most obvious physical effect of developing pachyosteosclerotic rostrum bones (irrespective of their external shape and histology) is a local increase in mass. As deep divers, ziphiids might find a benefit in such a ballast, positioned at the anterior extremity of the body, even if it is of minor importance, as compared to the total weight of the animals. This ballast could indeed help them maintaining a vertical position in the water column during descent (dynamic ballast; de Buffrénil et al., 2000). The most obvious criticism to this hypothesis is that the energetic benefit during the descent would be lost during the way back to the surface (MacLeod, 2002). However, preliminary observations on diving ziphiids showed that, at least in some of the few dives recorded for M. densirostris and Z. cavirostris, the locomotion type changes from the descent to the ascent; the studied animals more frequently performed passive and metabolically cheap gliding during the descent, whereas swimming was more active, with more frequent tail strokes during the ascent (Tyack et al., 2006), a behaviour similarly observed in several other groups of diving marine mammals (Williams et al., 2000). Nevertheless, as mentioned above, no significant intraspecific difference could be observed for now between the swimming style and diving depths of adult males, adult females, and juveniles.
With their sexually dimorphic tusks, adult males of many extant ziphiid species are supposed to engage in intraspecific fights. Based on indirect observations (accumulation of unpigmented linear scars on the body, likely made by the tusks), this putative behaviour leads to the hypothesis that thicker and heavier rostrum bones (especially the filling of the mesorostral groove by the vomer) may limit the risks of fractures caused by impacts (Heyning, 1984 and MacLeod, 2002). However, the extremely high mineral content of the hyperdense rostrum of M. densirostris, the only species on which mechanical tests have been applied, results in a very brittle material, certainly unsuited to impact loading (de Buffrénil et al., 2000 and Zioupos et al., 1997). Interestingly, a preliminary analysis of the bone organization in the maxillary crests of H. ampullatus, the only species for which head-butting has been actually observed (Gowans and Rendell, 1999), indicates that, as proposed by Hardy (2005), the crests are made of spongy bone, in strong contrast with the compact bone of many other ziphiid rostra. Such a condition would actually be reminiscent of the spongy aspect of the antlers and other skull elements of head-butting terrestrial ungulates (Currey, 2002). It nevertheless remains that changes in the thickness and shape of the rostrum bones, leading to the dorsal closure or the filling of the mesorostral groove, could have a positive effect on the mechanical strength of this part of the skull, especially in long-snouted species with apical lower tusks (Bianucci et al., 2008 and Lambert et al., 2010a). However, unusual shapes of the rostrum bones, as exemplified by the medial crest in “M.” tumidirostris and Tusciziphius sp., are more difficult to understand in the framework of this hypothesis.
To conclude, the striking diversity of morphological and histological features documented here in the rostrum of extinct and extant ziphiids suggests a complex evolutionary history for these characters within the family, and poorly matches a single, univoqual functional explanation for now. Several behavioural/ecological factors may have played a role in the development of pachyosteosclerotic bone, and the latter could possibly be a relevant solution for more than one selective pressure. A broader sampling for histological analyses, including new extinct species and juveniles, adult females, and adult males of extant species, will certainly provide additional arguments to the discussion, as well as more detailed data about the ecology of extant ziphiids (recognition of different feeding and diving habits for males and females, observation of intraspecific fights…).
Acknowledgements
We wish to thank A. Abourachid, M. Bosselaers, A. Folie, C. Lefèvre, E. Pellé, and E. Steurbaut for the loan or gift of specimens, L. Cazes and J.L. Lemoine for the production of the ground sections, J.M. Lorphelin, P. Somma, F. Boumalk, and L. Jokiel from the Centre d’Imagerie Médicale de Bois-Bernard and W. Coudyser from the Universitair Ziekenhuis Gasthuisberg Leuven for the CT scans, D. Germain for his help with character optimization, D. Geffard-Kuriyama and F. Goussard for their assistance with Mimics, and three anonymous reviewers and the editor M. Laurin for their constructive comments about our manuscript.
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3D reconstructions of the skulls of (a) the delphinid Delphinus delphis MNHN 1934-367 and (b) the ziphiid Mesoplodon bidens MNHN 1975-112 in dorsal view. The densest areas, mostly the porcelanous part of the premaxillae on the rostrum and the left ear bones of M. bidens, are highlighted in yellow and red for D. delphis and M. bidens, respectively. Each reconstruction is accompanied by a virtual transverse section at mid-rostrum length displaying the variation of compactness (white areas represent the most compact bone) and the empty mesorostral groove. Scale bars = 100 mm.
Reconstruction 3D des crânes (a) du delphinidé Delphinus delphis MNHN 1934-367 et (b) du ziphiidé Mesoplodon bidens MNHN 1975-112 en vue dorsale. Les régions les plus denses, principalement la partie « à l’aspect de porcelaine » du prémaxillaire sur le rostre et les os de l’oreille gauche de M. bidens, sont colorées respectivement en jaune pour D. delphis et en rouge pour M. bidens. Chaque reconstruction est accompagnée d’une coupe transversale virtuelle à mi-longueur du rostre, montrant les variations de compacité (les zones blanches représentent l’os le plus compact) et la gouttière mésorostrale vide. Barres d’échelle = 100 mm.
Partial skull of Izikoziphius angustus SAM PQ 3004, Neogene of South Africa, in dorsal view, displaying the complete filling of the mesorostral groove by the vomer. Scale bar = 100 mm.
Vue dorsale d’une partie du crâne de Izikoziphius angustus SAM PQ 3004, Néogène d’Afrique du Sud, montrant le remplissage complet de la gouttière mésorostrale par le vomer. Barre d’échelle = 100 mm.
Skull of a sexually mature female Tasmacetus shepherdi USNM 484878 in anterodorsal view, displaying the thickened vomer on the walls of the mesorostral groove, giving the groove a V-shaped section at the rostrum base. Scale bar = 100 mm.
Crâne de femelle sexuellement mature de Tasmacetus shepherdi USNM 484878 en vue antérodorsale, montrant l’épaississement du vomer sur les flancs de la gouttière mésorostrale, donnant à la gouttière une section en V à la base du rostre. Barre d’échelle = 100 mm.
Partial skull of Berardius arnuxii SAM 39296 in anterior to anterodorsal view, displaying a partial filling of the mesorostral groove by the spongy mesethmoid. The vomer and premaxillae are not significantly thickened. The anterior part of the rostrum is missing, as well as portions of the premaxillae above the groove. Scale bar = 100 mm.
Crâne partiel de Berardius arnuxii SAM 39296 en vue antérieure à antérodorsale, montrant le remplissage partiel de la gouttière mésorostrale par le mésethmoïde spongieux. Le vomer et les prémaxillaires ne sont pas significativement épaissis. La partie antérieure du rostre est manquante, de même que des portions des prémaxillaires au-dessus de la gouttière. Barre d’échelle = 100 mm.
Partial skull of Choneziphius planirostris IRSNB 3774-M.1881, Miocene of the North Sea, in right laterodorsal view, displaying the dorsal closure of the mesorostral groove by the thickened premaxillae. Scale bar = 100 mm.
Vue latérodorsale droite d’une partie du crâne de Choneziphius planirostris IRSNB 3774-M.1881, Miocène de la Mer du Nord, montrant la fermeture dorsale de la gouttière mésorostrale par les prémaxillaires épaissis. Barre d’échelle = 100 mm.
(a) Skull of adult male Hyperoodon ampullatus MNHN 1872-491 in right anterolateral view, displaying the high rostral maxillary crests. (b) detail of the spongy surface of the right crest. Scale bars = 300 mm for a, 10 mm for b.
(a) Crâne de mâle adulte de Hyperoodon ampullatus MNHN 1872-491 en vue antérolatérale droite, montrant les hautes crêtes maxillaires rostrales. (b) détail de la surface spongieuse de la crête droite. Barres d’échelle = 300 mm pour a, 10 mm pour b.
CT scan of the skull of an adult male Mesoplodon layardii MNHN 1984-038. (a) 3D reconstruction in right lateral view. The densest areas, mostly on the rostrum and part of the vertex, are highlighted in red. (b–d) transverse sections displaying the variation of compactness, at the rostrum base (b), three quarters of the rostrum length (c), and mid-rostrum length (d). Scale bar = 100 mm.
CT scan du crâne d’un mâle adulte de Mesoplodon layardii MNHN 1984-038. (a) reconstruction 3D en vue latérale droite. Les zones les plus denses, principalement sur le rostre et une partie du vertex, sont colorées en rouge. (b–d) coupes transversales montrant la variation de compacité, à la base du rostre (b), aux trois quarts de la longueur du rostre (c), et à mi-longueur (d). Barre d’échelle = 100 mm.
CT scan of the skull of adult male Ziphius cavirostris MNHN 1934-253. (a) 3D reconstruction in left anterodorsolateral view. The densest areas, mostly the premaxillae, the vomer, and the left periotic, are highlighted in red. (b–e) transverse sections at mid-rostrum length (b), three quarters of the rostrum length (c), the rostrum base (d), and across the left periotic (e). Scale bar = 100 mm.
CT scan du crâne d’un mâle adulte de Ziphius cavirostris MNHN 1934-253. (a) reconstruction 3D en vue antérodorsolatérale. Les zones les plus denses, principalement les prémaxillaires, le vomer, et le périotique gauche, sont colorées en rouge. (b–e) coupes transversales à mi-longueur du rostre (b), aux trois quarts (c), à la base du rostre (d), et à travers le périotique gauche (e). Barre d’échelle = 100 mm.
Virtual transverse sections in the skull of juvenile Hyperoodon ampullatus MNHN 1881-1149. (a) section across the spongy rostral maxillary crests. (b) section across the posterior part of the cranium highlighting the high compactness of the right ear bones. Scale bar = 100 mm.
Coupes transversales virtuelles dans le crâne d’un Hyperoodon ampullatus juvénile MNHN 1881-1149. (a) coupe à travers les crêtes maxillaires rostrales spongieuses. (b) coupe à travers la partie postérieure du crâne mettant en évidence la compacité élevée des os de l’oreille droite. Barre d’échelle = 100 mm.
(a) Outline of the partial skull of Choneziphius planirostris IRSNB 3774-M.1881 in right lateral view, with the location of the transverse section performed in the rostrum fragment Choneziphius sp. MB CR-15. (b–d) details of the ground section in Choneziphius sp. MB CR-15. (b) numerous secondary osteons, some of them with a subcomplete closure of the vascular canal. Small rectangle = area enlarged in c–d. (c–d) atypical secondary osteons made of parallel-fibered to woven-fibered bone, in natural (c) and polarized (d) light. (e–f) details of a transverse ground section in the rostrum of Mesoplodon densirostris MNHN 1922-143, in polarized light, displaying similar atypical secondary osteons, lacking an alternate birefringence. Scale bars = 100 mm for a, 2 mm for b, 500 μm for c–f.
(a) Contour d’une partie du crâne de Choneziphius planirostris IRSNB 3774-M.1881 en vue latérale droite, montrant la position de la coupe transversale réalisée sur le fragment de rostre Choneziphius sp. MB CR-15. (b–d) détails de la lame mince de Choneziphius sp. MB CR-15. (b) nombreux ostéones secondaires, certains avec une fermeture subcomplète du canal vasculaire. Petit rectangle = zone aggrandie en c-d. (c–d) ostéones secondaires atypiques, constitués d’os à fibres parallèles et à fibres enchevétrées, en lumière naturelle (c) et polarisée (d). (e–f) détails d’une lame mince transversale dans le rostre de Mesoplodon densirostris MNHN 1922-143, en lumière polarisée, montrant le même type d’ostéones secondaires atypiques, sans biréfringence alternée. Barres d’échelle = 100 mm pour a, 2 mm pour b, 500 μm pour c-f.
(a) Outline of the partial skull of aff. “Mesoplodon” longirostris IRSNB 3800 in left lateral view, with the location of the transverse sections performed in the rostrum fragments aff. “M.” longirostris MB CR-10 (S1) and MB CR-9 (S2). (b) ground section in MB CR-10 with part of the sutures between bones visible. (c–g) details of the ground section in MB CR-9. (c) premaxilla-vomer suture area displaying the transition between the barely remodeled vomer (upper left) and the distincly remodeled premaxilla (lower right). (d–e) detail of the fibro-lamellar complex in the vomer with predominantly vertical primary osteons, in natural (d) and polarized (e) light. (f–g) detail of the longitudinally oriented secondary osteons in the premaxilla, in natural (f) and polarized (g) light. Scale bars = 100 mm for a, 10 mm for b, 2 mm for c, 500 μm for d–g.
(a) Contour d’une partie du crâne de aff. «Mesoplodon» longirostris IRSNB 3800 en vue latérale gauche, montrant la position des coupes transversales réalisées dans les fragments de rostre aff. «M.» longirostris MB CR-10 (S1) et MB CR-9 (S2). (b) lame mince dans MB CR-10, avec une partie des sutures entre les os visible. (c–g) détails des lames minces dans MB CR-9. (c) zone de la suture prémaxillaire-vomer montrant la transition entre le vomer à peine remanié (en haut à gauche) et le prémaxillaire distinctement remanié (en bas à droite). (d–e) détail du complexe fibro-lamellaire dans le vomer avec des ostéones primaires en majorité verticaux, en lumière naturelle (d) et polarisée (e). (f–g) détail des ostéones secondaires longitudinaux dans le prémaxillaire, en lumière naturelle (f) et polarisée (g). Barres d’échelle = 100 mm pour a, 10 mm pour b, 2 mm pour c, 500 μm pour d–g.
(a) Outline of the partial skull of Ziphirostrum marginatum IRSNB 3847-M.537 in right lateral view (reversed), with the location of the transverse section performed in the rostrum fragment aff. Ziphirostrum. (b) ground section in the maxilla and premaxilla. (c–d) detail of the maxilla-premaxilla suture area displaying the non-remodeled premaxilla (upper left) and the strongly remodeled maxilla (lower right), in natural (c) and polarized (d) light. (e–f) secondary osteons in the maxilla, in natural (e) and polarized (f) light, displaying the subcomplete closure of the vascular canals and the alternate birefringence typical of lamellar tissue. Scale bars = 100 mm for a, 1 mm for c–d, 500 μm for e–f.
(a) Contour d’une partie du crâne de Ziphirostrum marginatum IRSNB 3847-M.537 en vue latérale droite (inversée), montrant la position de la coupe transversale réalisée dans le fragment de rostre aff. Ziphirostrum. (b) lame mince dans le maxillaire et le prémaxillaire. (c–d) détail de la région de la suture maxillaire-prémaxillaire montrant le prémaxillaire non remanié (en haut à gauche) et le maxillaire fortement remanié (en bas à droite), en lumière naturelle (c) et polarisée (d). (e–f) ostéones secondaires dans le maxillaire, en lumière naturelle (e) et polarisée (f), montrant la fermeture subcomplète des canaux vasculaires et la biréfringence alternée typique du tissu lamellaire. Barres d’échelle = 100 mm pour a, 1 mm pour c–d, 500 μm pour e–f.
(a) Outline of the partial skull of Aporotus recurvirostris IRSNB 3812-M.1887 in right lateral view, with the location of the transverse section performed in the rostrum fragment A. recurvirostris IRSNB 3810-M.2012. (b) ground section in the hyperplasic premaxilla of A. recurvirostris IRSNB 3810-M.2012 displaying conspicuous growth marks (arrows) in the laminar bone. (c) detail of the radiating bone in the upper left area of the section. (d) detail of the laminar (left) and more reticular (right) primary bone. (e) ground section in the remodeled and spongy maxilla of A. recurvirostris IRSNB 3810-M.2012. Scale bars = 100 mm for a, 10 mm for b, 5 mm for e, 1 mm for c–d.
(a) Contour d’une partie du crâne de Aporotus recurvirostris IRSNB 3812-M.1887 en vue latérale droite, montrant la position de la coupe transversale réalisée dans le fragment de rostre A. recurvirostris IRSNB 3810-M.2012. (b) lame mince dans le prémaxillaire hyperplasique de A. recurvirostris IRSNB 3810-M.2012 montrant les marques de croissance (flèches) dans l’os laminaire. (c) détail de l’os radiaire dans la zone supérieure gauche de la coupe. (d) détail de l’os primaire laminaire (à gauche) et réticulaire (à droite). (e) lame mince dans le maxillaire spongieux et remanié de A. recurvirostris IRSNB 3810-M.2012. Barres d’échelle = 100 mm pour a, 10 mm pour b, 5 mm pour e, 1 mm pour c–d.
Growth marks in the premaxilla, on dorsal surface of the rostrum of Choneziphius planirostris IRSNB 3777-M.1882 (a), on transverse fracture surface at the rostrum base of aff. Aporotus dicyrtus IRSNB 3807-M.1889 (b–c), shown in dorsal view (b), in posterior view of the fracture surface (c), and on virtual transverse section at mid-length of the rostrum of Ziphirostrum recurvus IRSNB 3805-M.544 (d). Arrows indicate the most conspicuous growth marks. Scale bars = 50 mm for a-b, 10 mm for d.
Marques de croissance dans le prémaxillaire, en surface dorsale du rostre de Choneziphius planirostris IRSNB 3777-M.1882 (a), sur une surface de fracture transversale à la base du rostre de aff. Aporotus dicyrtus IRSNB 3807-M.1889 (b–c), en vue dorsale (b) et en vue postérieure de la surface de fracture (c), et en coupe transversale virtuelle à mi-longueur du rostre de Ziphirostrum recurvus IRSNB 3805-M.544 (d). Les flèches indiquent les marques de croissance les plus manifestes. Barres d’échelle = 50 mm pour a–b, 10 mm pour d.
Composite phylogenetic tree of the ziphiids based on several cladistic analyses (Bianucci et al., 2007, Bianucci et al., 2010 and Lambert, 2005). †, extinct taxa. Specimens referred to the extinct “Mesoplodon” longirostris probably do not belong to the genus Mesoplodon, even if they are closely related. Optimization of the ancestral state is shown for characters 1–2. Char. 1 (filling of the mesorostral groove) on the left mirror-tree. Light grey, filling by the vomer (0); dark grey, absence of filling (1); black, filling by the mesethmoid (2). Char. 2 (dorsal closure of the groove by the thickened premaxillae) on the right mirror-tree. Light grey, absence (0); black, presence (1). Only the DelTran hypothesis is illustrated for both characters.
Arbre phylogénétique composite des ziphiidés, basé sur plusieurs analyses cladistiques (Bianucci et al., 2007, Bianucci et al., 2010 and Lambert, 2005). †, taxons éteints. Les spécimens attribués au taxon éteint «Mesoplodon» longirostris n’appartiennent vraisemblablement pas au genre Mesoplodon, même s’ils en sont proches. L’optimisation de l’état ancestral est montrée pour les caractères 1–2. Car. 1 (remplissage de la gouttière mésorostrale) sur l’arbre-miroir de gauche. Gris clair, remplissage par le vomer (0) ; gris foncé, absence de remplissage (1) ; noir, remplissage par le mésethmoïde (2). Car. 2 (fermeture dorsale de la gouttière par les prémaxillaires épaissis) sur l’arbre-miroir de droite. Gris clair, absence (0) ; noir, présence (1). Seule l’hypothèse DelTran est illustrée pour les deux caractères.
Data-matrix for the four characters discussed in the text.
Matrice de données pour les quatre caractères discutés dans le texte.
Probability that the distribution of the states of each character studied is random with respect to the phylogeny. This is assessed by determining the number of randomly generated trees (out of 10 000) that imply the same number of steps (or less) than the reference tree. This test was performed by Mesquite. A probability lower than 0.05 indicates a reliable optimization of the given character (number of steps lower in the reference tree than in more than 95% of the random trees).
Probabilité que la distribution des états de caractères soit aléatoire par rapport à la phylogénie. Cette probabilité est déterminée par le nombre d’arbres aléatoires qui impliquent le même nombre de pas (ou moins) que l’arbre de référence. Les 10 000 arbres aléatoires ont été générés à l’aide de Mesquite. Une probabilité inférieure à 0,05 indique une optimisation fiable pour le caractère considéré (nombre de transitions sur l’arbre de référence, plus bas que dans au moins 95 % des arbres aléatoires).
ProbabilityNumber of steps on reference treeChar. 10.05397Char. 20.01043Char. 312Char. 412