• Cetacea;
  • olfactory apparatus Protocetidae;
  • Balaenopteridae;
  • Virginia;
  • ethmoturbinates;
  • Pamunkey River


  1. Top of page
  2. Abstract
  6. Acknowledgements

The structure of the olfactory apparatus is not well known in both archaic and extant whales; the result of poor preservation in most fossils and locational isolation deep within the skulls in both fossil and Recent taxa. Several specimens now shed additional light on the subject. A partial skull of an archaic cetacean is reported from the Pamunkey River, Virginia, USA. The specimen probably derives from the upper middle Eocene (Piney Point Formation) and is tentatively assigned to the Protocetidae. Uncrushed cranial cavities associated with the olfactory apparatus were devoid of sediment. CT scans clearly reveal the dorsal nasal meatus, ethmoturbinates within the olfactory recess, the cribriform plate, the area occupied by the olfactory bulbs, and the olfactory nerve tract. Several sectioned skulls of the minke whale (Balaenoptera acutorostrata) were also examined, and olfactory structures are remarkably similar to those observed in the fossil skull from the Pamunkey River. One important difference between the two is that the fossil specimen has an elongate olfactory nerve tract. The more forward position of the external nares in extant balaenopterids when compared with those of extant odontocetes is interpreted to be the result of the need to retain a functional olfactory apparatus and the forward position of the supraoccipital/cranial vertex. An increase in the distance between the occipital condyles and the vertex in balaenopterids enhances the mechanical advantage of the epaxial musculature that inserts on the occiput, a specialization that likely stabilizes the head of these enormous mammals during lunge feeding. Anat Rec, 2013. © 2012 Wiley Periodicals, Inc.

Most mammals rely heavily upon olfaction to find food, recognize conspecifics, establish and maintain social interactions, find fertile mates, detect potential threats, and orient themselves (Stoddart, 1980a, b; Rowe et al., 2005). The mammalian nose also traps inhaled particles (Kelly et al., 2000), metabolizes airborne xenobiotics (Brain, 1970), helps regulate water balance and heat exchange (Schmidt-Nielsen et al., 1970; Hillenius, 1992; Van Valkenburgh et al., 2004, 2011; Rowe et al., 2005), and removes inhaled chemicals that may be harmful to the more sensitive tissues in the lower tracheobronchial airways and pulmonary parenchyma (Harkema et al., 2006). On the basis of the diversity of nasal-cavity architectures in mammals, it is well known that not all nasal/olfactory functions are equally developed (Negus, 1958; Schreider and Raabe, 1981; Van Valkenburgh et al., 2004; Harkema et al., 2006; Craven et al., 2007). During the course of their evolutionary history from terrestrial artiodactyls to an obligate aquatic lifestyle, cetaceans have modified their olfactory/nasal respiratory apparatus more so than any other mammalian group (Edinger, 1955). One of the most conspicuous changes involved a shift in the relative position, size, and complexity of the scrolls and plates of bone known collectively as turbinals (Owen, 1854; Hillenius, 1992; Klima, 1995).

In artiodactyls, air taken in through the nostrils flows past the maxilloturbinates (Sisson and Grossman, 1953). By contrast, extant cetaceans have eliminated the maxilloturbinates and the unobstructed nasal cavity allows for the rapid exchange of a large volume of air during the brief elevation of the nostrils above the water surface (Reidenberg and Laitman, 2008). Extant odontocetes have no turbinals and have greatly reduced or no olfactory bulbs and olfactory nerve tracts, and consequently little to no sense of smell (Edinger, 1955; Oelschläger, 1992). Mysticetes are increasingly recognized as having an olfactory system that is functional (Flower, 1885; Edinger, 1955; Cave, 1988; Oelschläger and Oelschläger, 2008; Thewissen et al., 2011) but greatly reduced when compared with their terrestrial sister taxa (McGowen et al., 2008; Thewissen et al., 2011; Kishida and Thewissen, 2012). In bowhead whales the relative size of the olfactory bulb and olfactory receptor pseudogene proportions suggest that their sense of smell is better developed than in microsmatic mammals including humans (Thewissen et al., 2011; Kishida and Thewissen, 2012). Extant balaenopterids possess ethmoturbinates, albeit relatively small ones located in an invagination of the nasal cavity (the nasal recess), to which inhaled air is probably channeled unidirectionally along the dorsal nasal meatuses (see below). Reidenberg and Laitman (2008) intimated that inhaled air flowed almost incidentally into the nasal cavity. This may in fact be the case. However, inspired by the findings of Craven et al. (2010), in which they discovered in dogs (Canis familiaris) that during inspiration the dorsal nasal meatus directs odorants to the rear of the olfactory recess where the ethmoturbinates are located, we propose here that the dorsal nasal meatuses in the protocetid and minke whales described below had a similar function and is further evidence for the importance of olfaction in at least some cetaceans.

Stromer (1903), Edinger (1955), Hoch (2000), Uhen (2004), and Bajpai et al. (2011) have described parts of the olfactory anatomy in some archaeocetes despite a combination of postmortem crushing and sedimentary interference in the relatively few specimens available for study. The olfactory anatomy has also been described in some extant mysticetes by Flower (1885), Ries and Langworthy (1937), Breathnach (1955, 1960), and Thewissen et al. (2011). Here, we describe a cetacean partial skull (CMM-V-4536, Figs. 1–5) that was recovered from the bed of the Pamunkey River, Virginia, USA. The specimen probably derives from upper middle Eocene Piney Point Formation and is tentatively assigned to the Protocetidae. Although incomplete, what remains of the skull is wholly uncrushed, preserving both external and internal anatomy superbly well, especially the osteological correlates of the olfactory apparatus and posterior nasal cavity. The preserved cranial cavities were devoid of sediment allowing us to easily identify the dorsal nasal meatuses, the ethmoturbinates, the cribriform plate, the area occupied by the olfactory bulbs, and the olfactory nerve tract in CT images. Similarly sized and shaped structures were identified in several sectioned skulls of the extant minke whale (Balaenoptera acutorostrata, USNM 485829 and USNM 485830). Comparing the olfactory system in the archaic whale (CMM-V-4536) to the minke whale reveals that the modern configuration of reduced turbinals in an invagination of the nasal cavity and voluminous nasal passages probably evolved in the middle Eocene before the divergence of odontocetes and mysticetes.

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Figure 1. A and B: Protocetid partial skull, CMM-V-4536, in dorsal and ventral views, respectively. Recovered from the bed of the Pamunkey River, Virginia, USA. The skull was lightly coated with sublimed ammonium chloride. Scale bar equals 10 cm.

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Figure 2. AC: Protocetid partial skull, CMM-V-4536, in left lateral, anterior, and an anterolateral and slightly ventral view, respectively. The skull was lightly coated with sublimed ammonium chloride. Scale bar equals 10 cm.

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Figure 3. AO: Individual transverse CT scans of CMM-V-4536 in posterior view. P, CMM-V-4536 in dorsal view, adjacent to which are lettered lines indicating where the correspondingly lettered CT image derives. Scale bar equals 10 cm.

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Figure 4. Reconstructed negative space of the ethmoturbinates and related olfactory apparatus in CMM-V-4536 in an anterolateral and slightly dorsal view. Based on CT scans compiled in Mimics®.

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Figure 5. Comparative archaeocete ethmoturbinates (not to the same scale). A: Saghacetus osiris (Staatliches Museum für Naturkunde Stuttgart no. 11786) skull in dorsal view showing endocasts of the right dorsal nasal meatus, ethmoturbinates, olfactory bulb chamber, and olfactory nerve tract beneath missing bones of the skull roof. Reproduced and edited from Stromer (1908) Plate V, Fig. 12. B: Saghacetus osiris (Staatliches Museum für Naturkunde Stuttgart) partial skull in dorsal view preserving mostly endocasts of the dorsal nasal meatus, posterior nasal cavity, ethmoturbinates, and olfactory nerves passing through what would have been the area occupied by the cribriform plate. Reproduced and edited from Stromer (1903) Plate X, Fig. 2. C: CMM-V-4536 in dorsal view, upon which the reconstructed negative space (giving the impression of an endocast) of the ethmoturbinates and related olfactory apparatus was superimposed. Superimposed moiety based on CT scan negative spaces compiled in Mimics®.

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Relatively little is known of early (i.e., Eocene) whale evolution in North America (Hulbert et al., 1998; Uhen, 1998, 1999, 2001, 2008; Geisler et al., 2005; McLeod and Barnes, 2008; Weems et al., 2011). A scattering of a few localities along the Gulf coast and eastern seaboard, from the states of Texas, Louisiana, Mississippi, Alabama, Georgia, and South Carolina (middle Eocene) in the south, to North Carolina and Virginia further north (middle Eocene) preserves the remains of protocetid whales, the oldest-known cetaceans in North America (Uhen, 2012). Weems et al. (2011) described two protocetid vertebrae from Virginia, both of which were collected from the bed of the Pamunkey River. Microfossil analysis of adhering sediments indicates the source of the vertebrae as having come from the middle Eocene Piney Point Formation, the same Formation from which the specimen described herein is thought to derive. Although CMM-V-4536 is far from complete, it adds to our understanding of the anatomical diversity of early whales in North America. It also demonstrates that there are phylogenetically informative characters within the olfactory system hitherto unaccounted for in systematics of archaeocete whales. Following a description of CMM-V-4536, comparisons between its olfactory anatomy and that of the extant minke whale (B. acutorostrata) will be made.


  1. Top of page
  2. Abstract
  6. Acknowledgements

Anatomical nomenclature was taken from Sisson and Grossman (1953), Uhen (2004), Craven et al. (2010), and Thewissen et al. (2011).

Institutional Abbreviations

CMM-V-, Calvert Marine Museum fossil vertebrate collection, Solomons, Maryland, USA; GSM, Georgia Southern Museum, Statesboro, Georgia, USA; H-GSP, Howard University-Geological Survey of Pakistan, Islamabad, Pakistan; USNM, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia, USA.

Table  . 
Systematic Paleontology
Cetacea Brisson, 1762
Protocetidae Stromer, 1908
Genus and species indeterminate
(Figs. 1–5)


CMM-V-4536 was collected by R. Ison from the riverbed of the Pamunkey River, Virginia, USA (near 37° 37′ N; 77° 05′ W). More detailed locality information is available from the authors to qualified individuals upon request.

Formation and Age

The partial skull was not found in situ, nor was there any entombing sediment associated with the specimen. Nevertheless, it is presumed to be locally derived from one of the Paleogene units found along the river (Ward, 1985). At the point where the partial skull was found, the depth of the water ranges from 8 to 12 m. Here, above the water line, there is a low bank where (intermittently) ∼1 m of the Old Church Formation (upper Oligocene) is exposed. Above this is a very thin layer of the Miocene Calvert Formation that could be as old as Bed 3A, lower Miocene (∼18 Ma) (Ward, personal communication). Approximately 2–3 m below river level at the site where CMM-V-4536 was found is a 6- to 9-m-thick exposure of the Piney Point Formation (Ward, personal communication), and below that, the Woodstock Member of the Nanjemoy Formation (Ypresian). No cetacean remains have ever come from the Nanjemoy Formation or its equivalent within that interval of the Eocene from anywhere in North America (Weems et al., 2011). Therefore, on the basis of the thickness of the Piney Point Formation where the specimen was found and because of its primitive morphology, it is thought to derive from this Eocene formation. However, we cannot exclude the Oligocene Old Church Formation as a possible source for the specimen. The only other cetacean remains known from the Piney Point Formation are two protocetid whale vertebrae, which Weems et al. (2011) referred to “Eocetuswardii.

In addition to the reddish-brown color of the fossilized bone, parts of it were additionally stained a much darker hue presumably by tannic acid during the time it was exposed on the bottom of the Pamunkey River. This same very dark color characterizes other vertebrate bone collected along the bottom of the river; in situ quarried specimens are not stained thusly. Unfortunately, the color of a fossil at this locality is not indicative of the formation from which it derives.


  1. Top of page
  2. Abstract
  6. Acknowledgements


The single partial skull (CMM-V-4536, Figs. 1–5) consists of most of the interorbital region and the anterior part of the intertemporal area. The positions of the maxillofrontal and nasofrontal sutures, the reduced size of the nasal turbinates, and the presence of an intertemporal constriction (i.e., a narrow postorbital/temporal region) confirm the identity of this specimen as cetacean. The animal was small though, having a frontal shield breadth of only 225 mm [based on the reasonable assumption that the skull is essentially symmetrical (Figs. 1, 2) and taking the measurement from the one complete side (the left side) and doubling that value]. This measurement is just slightly more than in the smallest recorded skull of a subadult Dorudon atrox (Uhen, 2004, Fig. 135: UM 94814 - 224.0 mm).


Although the nasals are not preserved (Fig. 1), a series of mostly parallel, anteroposteriorly aligned ridge-and-furrow sutures on the dorsal surface of the frontal indicate that the nasals extended back toward the anterior most point of the posterior margin of the supraorbital process of the frontal. The shape of the posterior margin of the sutures is similar to the nasal/frontal suture in Georgiacetus, and is consistent with the entire sutural surface being for the nasals; however, we cannot exclude the possibility that the lateral portion held the maxilla.


Most of CMM-V-4536 consists of the robust frontals. The broad dorsal surface of the frontal shield slopes gently ventrolaterally from the median plane toward the thickened supraorbital process. The orbits are directed laterally or perhaps even slightly ventrolaterally (Figs. 1, 2). In dorsal view, the anterior part of the skull is conspicuously furrowed where it was overlapped by nasals. CT scan images (Fig. 3) reveal how the frontal surrounds much of the ethmoid throughout its preserved length.

Viewed laterally (Fig. 2), and in CT scan sections (Fig. 3), the preorbital region of the frontal is seen to consist of a dorsoventrally thickened mass of bone, but no preorbital ridge exists (Fig. 1). By contrast, the preorbital region in Janjucetus hunderi (Fitzgerald, 2006: Figs. 1B, 2A), Mammalodon colliveri (Fitzgerald, 2010), and some aetiocetids (Barnes et al., 1995) consists of a thin plate of bone. The thickened preorbital process in CMM-V-4536 is seen in basilosaurid archaeocetes and crown mysticetes, which have a dorsoventrally thickened preorbital process with a preorbital ridge. The postorbital process of the frontal is not preserved in CMM-V-4536.

Posteriorly, the frontals narrow abruptly at the intertemporal constriction where they are overlapped by the parietals. In dorsal view, the suture between the frontals at the level of the anterior margin of the temporal fossa takes a jog to the left. Posteriorly, this suture disappears beneath the parietals. Deep parallel-sided furrows outline the still-open sutures between the frontals and overlapping parietals. In a dorsal view (Fig. 1A), the frontoparietal suture (i.e., the coronal suture) is distinctly V-shaped, with the base of the “V” conspicuously to the left of the midline of the skull. Consequently, the sutural line between the frontals and parietals is obviously asymmetrical. A V-shaped frontoparietal suture is also seen in mammalodontids, basilosaurids (Fitzgerald, 2010), and the protocetids Georgiacetus (GSM 350, personal observation) and Carolinacetus (Geisler et al., 2005).

The CT scans of CMM-V-4536 (Fig. 3) reveal that there was no development of a frontal sinus, although the anterior portion of the frontal is broadly excavated where it received the posterior part of the nasal passage or a maxillary sinus. In the protocetid Aegyptocetus tarfa, a similarly positioned intracranial cavity has been referred to as the maxillary sinus (actually subdivided into medial and lateral parts), and in that taxon, the maxilla forms the anterior wall of the cavity and a thin partition that separates it from the nasal passages proper (Bianucci and Gingerich, 2011: Fig. 4). Although no such lamina is preserved in CMM-V-4536, given the preservation of the skull, we would not be surprised if such a structure was lost during its exhumation or transport by the Pamunkey River. Among cetaceans, frontal sinuses have been reported in the basilosaurid Dorudon (Uhen, 2004, Figs. 29D, 31), the protocetid Carolinacetus (Geisler et al., 2005), and the remingtonocetid Remingtonocetus (Bajpai et al., 2011). In each case, the structure reported as a frontal sinus is an intracranial excavation of the frontal bone. However, without more detailed descriptions of how these spaces relate to vascular foramina, the diploe of the frontal bone, and/or the nasal passages, the differences between CMM-V-4536 and these specimens may simply reflect different terminology for similar morphology.

The dorsal surface of the frontal has a scattering of over a dozen minute foramina (only three of which are indicated in Fig. 1A) which we interpreted as having carried frontal diploic veins. Most of the foramina face dorsally or laterally and are within 30 mm of the sutural surface with the nasal. Similarly positioned foramina occur in Georgiacetus (personal observation), although in the holotype of that taxon the foramina are larger, face anteriorly, and lead into distinct anteroposteriorly aligned sulci. Intracranially, the foramina for the frontal diploic veins can be traced into a ragged space that is continuous with the diploe of the frontal bone (Fig. 3I–M). Ventrally, this diploic sinus connects with the canals for the olfactory bulbs. Additional diploic veins connected to this space open into the roof of the orbit (Fig. 1B).


Much of the ethmoid is well preserved in CMM-V-4536. CT scans show the frontal-ethmoid sutures as well as textural differences between the two bones (Fig. 3). Anteriorly, below the deeply furrowed frontal shield, the dorsal margin of the ethmoid encloses a pair of tubular troughs (the dorsal nasal meatuses) separated along their entire preserved length by a median nasal septum. Each dorsal nasal meatus opens ventrally into the much larger posterior narial passage. Posteriorly, each olfactory recess is continuous with the narial passage where the ethmoturbinates find their full expression within the ethmoidal labyrinth/olfactory recess. For the most part, the ethmoturbinates project medially from the lateral side of the ethmoid into the olfactory recess. In total there are seven or eight individual ethmoturbinates on each side, although three are much larger than the others. Distally, these larger turbinates further subdivide (Fig. 4). In general, the ethmoturbinates are quite thick and are slightly curved, not scroll-shaped, as in terrestrial mammals. The only exception is one of the middle ethmoturbinates, which curls ventrally 180 degrees to form a partial coil (Fig. 3H). At the posterior-most end of the olfactory recess—level of the ethmoidal foramen—the turbinates give way to the diminutive cribriform plate (Fig. 3I,J). Immediately above the cribriform plate are the pockets that held the olfactory bulbs (Fig. 4). Posteriorly, they merge into the canal that held the olfactory tracts (Figs. 3M–O, 4).


The anterior-most reach of each parietal extends to the anterodorsal-most margin of the temporal fossae (Figs. 1, 2), level to the back of the frontal shield. This is decidedly unlike the condition in D. atrox in which the coronal (frontoparietal) suture remains further back in the central skull region, but is similar to the North American protocetid Carolinacetus (Geisler et al., 2005). In Georgiacetus, the frontal/parietal suture is more posteriorly positioned but still well anterior to the position seen in Dorudon (personal observation).

CMM-V-4536 exhibits a narrow intertemporal constriction, decidedly narrower than in aetiocetids (Barnes et al., 1995). An absolutely and proportionately narrow intertemporal constriction is primitive for cetaceans. However, a narrow intertemporal constriction is present in some cetothere-grade mysticetes like Pelocetus calvertensis (Kellogg, 1965). A narrow intertemporal constriction does not always an archaic whale make. The width of the constriction should be appraised in conjunction with the length of the intertemporal constriction, the latter of which in mysticetes, in contrast to archaeocetes, is very short. In CMM-V-4536, the narrow intertemporal constriction was proportionately at least as long as in Dorudon (Uhen, 2004).

The preserved portions of the parietals in CMM-V-4536 do not include a sagittal crest, although several shallow longitudinal furrows posterodorsally hint at its original presence.


  1. Top of page
  2. Abstract
  6. Acknowledgements

On the Identity of CMM-V-4536

Although fragmentary, what is preserved of the skull restricts the taxonomic identity of CMM-V-4536. It lacks the key odontocete synapomorphy of an ascending process of the maxilla that is expanded posteriorly and laterally to overlap the dorsal surface of the supraorbital process of the frontal (Miller, 1923; Heyning, 1989; Barnes, 1990; Fordyce, 1994; Messenger and McGuire, 1998; Geisler and Sanders, 2003; Uhen, 2010). Two more likely alternatives remain: archaeocete or mysticete and in many respects, basal mysticetes and some archaeocetes have similar interorbital and intertemporal regions.

There are currently five recognized families of archaeocetes: Pakicetidae, Ambulocetidae, Remingtonocetidae, Protocetidae, and Basilosauridae. One of the major differences among these families is the orientation and spacing between the orbits. Protocetids and basilosaurids share with neocetes transversely wide supraorbital processes, in contrast to the closely spaced and in some cases dorsolaterally facing orbits of pakicetids, ambulocetids, and remingtonocetids. The ratio of the width across the middle of the orbits to the minimum width across the dorsal half of the intertemporal region in CMM-V-4536 is estimated to be about 4.1. This ratio is within the range observed among protocetids (Georgiacetus = 3.6, Gaviacetus = 5.2, latter based on Gingerich et al., 2005, Fig. 9) but higher than that seen in pakicetids (Pakicetus = 1.7, based on cast of H-GSP 96231) or remingtonocetids (Remingtonocetus = 3, based on Bajpai et al., 2011, Fig. 1).

CMM-V-4536 does resemble basilosaurids, although there are some important differences. Like the basilosaurids, Cynthiacetus peruvianus (Martínez-Cáceres and Muizon, 2011, Fig. 3) and to a lesser extent D. atrox (Uhen, 2004, Fig. 26), the antorbital process of CMM-V-4536 is thickened. However, other basilosaurids have a distinctly smaller antorbital process (e.g., Zygorhiza kochii: USNM 11962, cast 510828). The width across the orbits is absolutely and relatively smaller in CMM-V-4536 than in basilosaurids. The ratio of the width across the middle of the orbits to the minimum width of the intertemporal constriction is 4.1 in CMM-V-4536, whereas in Z. kochii it is between 5.6 and 5.8 (USNM 11962, cast 510828) and 5.0 in both D. atrox (Uhen, 2004, Fig. 32) and C. peruvianus (Martínez-Cáceres and Muizon, 2011, Fig. 2). Other differences include a more posteriorly positioned nasal/frontal suture (over posterior half of orbit in CMM-V-4536, over anterior third of orbit on basilosaurids) and a rounded ridge on the posterior edge of the supraorbital process (this ridge is sharp and overhangs more ventral portions in basilosaurids).

CMM-V-4536 most closely resembles protocetids in several respects: the relative width of the supraorbital shield falls within the range observed among protocetids (closest to Georgiacetus vogtlensis and A. tarfa), the posterior edge of the supraorbital process does not form a sharp crest, and the posterior edge of the nasal suture is in a more posterior position. In the last feature, CMM-V-4536 is slightly different in that the posterior edge of the nasal nearly reaches the level of the posterior margin of the supraorbital process, whereas in most protocetids (e.g., Georgiacetus, Gaviacetus, and Protocetus) it is approximately aligned with the midpoint of the orbit. The most noteworthy difference between CMM-V-4536 and protocetids is the presence of a robust antorbital process in the former, similar to some, but not all, basilosaurids (see above).

Unlike all known odontocetes, mysticetes lack an expanded nasal process of the maxilla; thus, it is possible that CMM-V-4536 represents a mysticete. However, comparisons with described taxa reveal several differences. Aetiocetids are different from CMM-4536 in having a low ratio (width across the middle of the orbits to the minimum width of the intertemporal constriction) due in large part to a widening of the intertemporal region in the former (ratio of 2.0 in Aetiocetus cotylalveus, based on USNM 24210, holotype). This difference is also seen in the mysticetes Janjucetus (ratio of 2.1, Fitzgerald, 2006, Fig. 1) and Mammalodon (ratio of 2.5, based on Fitzgerald, 2010, Fig. 6). Mammalodon, Janjucetus, and aetiocetids further differ from CMM-V-4536 in having an orbital margin that is concave in dorsal view and is sharp in lateral view. Mammalodon and Janjucetus, but not Aetiocetus, also have a sharp posterior margin of the supraorbital process, as is seen in some, but not all, basilosaurids (see above).

As the above discussion illustrates, even though CMM-V-4536 is fragmentary, it is distinct from all described cetacean taxa. Overall, its morphology is most similar to that of currently known protocetids; however, we view allocation of our new specimen to this family as tentative because Protocetidae is a paraphyletic group and at least two published phylogenies support a monophyletic Basilosauridae (Fitzgerald, 2010; Martínez-Cáceres and Muizon, 2011). Under that topology, the stem basilosaurid branch and the stem neocete branch are descendants of an adjacent, stem-ward, internal branch that would be considered a protocetid. If there was a substantial delay between the divergence of basilosaurids and neocetes and the accumulation of the synapomorphies that make each clade diagnosable, then it is possible that the earliest members of these lineages would more closely resemble protocetids than their descendants. This potential problem is further compounded by the fact that CMM-V-4536 is fragmentary and consists of a generally conservative region of the skull. Thus, we view it possible that CMM-V-4536 is a protocetid, a stem basilosaurid, a stem neocete, a stem mysticete, or even a stem odontocete. Of these possibilities, we view the first two options as most likely given the age of the Piney Point Formation (middle Eocene) (or possibly the Oligocene Old Church Formation) and the overall morphology of CMM-V-4536. The earliest definitive neocete is Llanocetus denticrantus (Gingerich, 1992; Fordyce, 2003), which is at least 6 million years younger than the youngest strata of the Piney Point Formation. Although basilosaurids are known from the middle Eocene (e.g., Kohler and Fordyce, 1997), they appear to be from the later part of the Bartonian, whereas the Piney Point Formation spans the Lutetian to earliest Bartonian (Weems et al., 2011).

As the osteological features that held the olfactory apparatus and nasal cavity within both fossil and extant cetaceans become better known, a greater number of phylogenetically significant characters relating to its evolution will almost certainly come to light. To that end, Fig. 5 is a comparison of the partially exposed sediment-infilled ethmoturbinate region in two specimens of the Eocene basilosaurid Saghacetus osiris from Zeuglodon Valley, Fayum, Egypt (Stromer, 1903, 1908) and CMM-V-4536. In both specimens of Saghacetus (Fig. 5A,B), the once air/tissue-filled nasal cavity is now sediment infilled—preserved as an endocast. These endocasts clearly show the presence of a dorsal nasal meatus, posterior nasal cavity, ethmoturbinates, olfactory bulb chamber, and olfactory nerve tract in S. osiris. In comparing the relative position of these features to the supraorbital portion of the frontal bone in CMM-V-4536 (Fig. 5C), they are all further forward in Saghacetus. Furthermore, the ethmoturbinates in Saghacetus are proportionately more elongate than in CMM-V-4536. Establishing an evolutionary polarity vis-à-vis the relative position and size of these structures in archaeocetes and stem Neoceti could help resolve the affinity of CMM-V-4536. The olfactory apparatus in CMM-V-5436 compares well with that preserved in Remingtonocetus harudiensis (Bajpai et al., 2011, Fig. 6) if a somewhat different interpretation is given to several of the structures that they identify. In their Fig. 6, we would interpret what they label as “frontal sinus” to be the chamber that held the ethmoturbinates (i.e., the ethmoid labyrinth) (Fig. 3). The “frontal sinus” in R. harudiensis occupies the same position as the ethmoturbinate chamber in CMM-V-5436, immediately anterior to, and rising to a level slightly above the position of the cribriform plate and the olfactory bulb chambers. Anteromedial to the “frontal sinus” (ethmoturbinates here) and medial to the maxillary sinus are what we would interpret as the anteroposteriorly elongate dorsal nasal meatus (not identified in their text or figures), a feature widely distributed in mammals and present in artiodactyls, S. osiris (Fig. 5), CMM-V-4536 (Fig. 5), and B. acutorostrata (Figs. 6–8; see below). If our interpretation is correct, perhaps cranial sinuses were not present in R. harudiensis, having been abandoned earlier on in the evolution of cetaceans. Clearly, the presence/absence and relative position of these structures within the skulls of archaeocetes and stem Neoceti will have to be more firmly established to resolve the issue.

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Figure 6. A: Parasagittal section (to the immediate left of the midline) through the skull of the minke whale (Balaenoptera acutorostrata, USNM 485829) showing a medial view of the left half of its olfactory apparatus. Anterior end of the skull is to the right. The vertical white lines labeled “1” and “2” indicate, respectively, where along the length of the skull the transverse sections “B1” and “B2” shown in Fig. 7 derive. Scale bar equals 10 cm. B: Enlarged view of the area immediately surrounding the cribriform plate. Scale bar equals 10 mm.

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Figure 7. Transverse sections through comparable regions of the olfactory apparatus in the skull of an Eocene protocetid cetacean (CMM-V-4536; A1 and A2) and the minke whale (Balaenoptera acutorostrata, USNM 485830; B1 and B2). Sections shown to the same scale. A1 and A2: CT scan images. B1 and B2: Photos from a physically sectioned skull. B1 and B2 are anterior and posterior views, respectively, of one 8-cm-thick section through the skull. Scale bar equals 10 cm.

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Figure 8. A: Anteroventrolateral view of a transverse section through the skull of the minke whale (Balaenoptera acutorostrata, USNM 485830). This section corresponds to B1 in Fig. 7. It is proposed here, in accordance with Bernoulli's principle (B. schematic insert), that air is evacuated from the ethmoid chamber/olfactory recess at least in part as the result of a pressure differential created as inhaled air moves past the opening marked with an asterisk, that is, the caudal end of the dorsal nasal meatus. B: The u-shaped tube showing the pressure differential is representative of the dorsal nasal meatus-olfactory recess complex in the minke whale. In both A and B, the opening to the right of the asterisk is a point of decreased air pressure as air speed increases through a tube of smaller diameter.

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The Olfactory Apparatus in CMM-V-4536 and B. acutorostrata

Although the partial skull of CMM-V-4536 differs greatly in size and overall shape from that of the extant minke whale, homologous features of their olfactory apparatus are remarkably similar morphologically and readily identifiable (Figs. 6, 7). CMM-V-4536 was compared directly with two sectioned skulls of B. acutorostrata (USNM 485829 and USNM 485830), and all three present the osteological correlates associated with a fully functional olfactory system. USNM 485829 (Fig. 6) was sectioned lengthwise along a parasagittal plane immediately adjacent to its midline. Among many other features, the cut face reveals, from front to back, the large nasal passage, the dorsal nasal meatus, ethmoturbinates, a cribriform plate, and the chamber that held in life the left olfactory bulb. USNM 485830 was variously sectioned transversely. Figure 7B1, an anterior view of one of these sections, reveals the presence of a dorsal nasal meatus on either side of the ossified nasal septum medial to the nasal passages as in CMM-V-4536 (Fig. 7A1).

In the minke whale, inhaled air passes from the large tubular nasal passages through/along the dorsomedially located trough-like opening of the dorsal nasal meatus into the olfactory recess containing the ethmoturbinates, directly comparable to the morphology that is preserved in CMM-V-4536 (Figs. 2–4, 7). A posterior view (Fig. 7B2) of the same skull section shown in Fig. 7B1 reveals a series of turbinates that project dorsomedially and medially into the olfactory recess, just as in CMM-V-4536 (Fig. 7A2). Like CMM-V-4536, the turbinals in B. acutorostrata are thick and uncoiled. One difference is that although there are seven to eight ethmoturbinals in CMM-V-4536, B. acutorostrata has only five or six. The olfactory recess in both CMM-V-4536 and B. acutorostrata is truly a recess, separated by intervening bone from the more ventrally positioned nasal passage (Fig. 7A2,B2).

In both CMM-V-4536 and B. acutorostrata, the cribriform plate lies at an oblique angle (from anterodorsal to posteroventral and facing anteroventrally) separating the ethmoid labyrinth/olfactory recess from the chamber that held the olfactory bulbs (Figs. 3–6). In the aforementioned features of their olfactory apparatus, the two taxa are much more alike in absolute size and morphology than they are in overall size and gross morphology of their skulls (Fig. 7). If the morphology of the olfactory system in B. acutorostrata can trace its origin to a cetacean like CMM-V-4536, then evolution was remarkably conservative in this integrated suite of features when compared with overall cranial morphology.

In terms of their olfactory apparatus, extant mysticetes and CMM-V-4536 do differ in the distance between the olfactory bulbs and the rest of the cranial cavity (Fig. 4). In CMM-V-4536 (Figs. 3, 4), the chambers for the olfactory bulbs lie anterior to the frontoparietal suture, level to the posterior margin of the supraorbital process of the frontal. Telescoping of the mysticete skull, as evidenced in B. acutorostrata (Fig. 6), greatly reduced the length of the olfactory nerve tracts, placing the olfactory bulb chambers only a short distance anterior to the expansive cranial cavity. With the anterodorsal migration of the parietal in B. acutorostrata (Fig. 6), its entire olfactory apparatus lies posterior to the suture between the frontal and parietal on the cranial vertex.

Craven et al. (2010) found that in dogs, olfactory and respiratory airflows are remarkably distinct. During inspiration, odorant-laden air is moved quickly along the dorsal nasal meatus to the olfactory ethmoturbinates, while the rest of the airflow passes ventrally toward the nasopharynx where it exits the nasal cavity (Craven et al., 2010). Once in the ethmoid labyrinth, airflow speed slows providing additional residence time for odorant absorption (Craven, 2008). Furthermore, during expiration, owing to the partial segregation of the ethmoturbinates above the lamina transversa within the nasal cavity, no appreciable airflow enters or exits this olfactory recess (Craven et al., 2010). Consequently, a unidirectional airflow is maintained through the olfactory recess. By contrast, the microsmatic human nasal cavity has no olfactory recess. As the olfactory region is located along the main airflow path through the nose and not within a highly developed olfactory recess, the sensory area is flushed when humans exhale (Craven et al., 2010).

Craven et al. (2010) observed that all macrosmatic species [e.g., marsupials (Negus, 1958), rodents (Schreider and Raabe, 1981), carnivores (Van Valkenburgh et al., 2004; Craven et al., 2007), and ungulates (Negus, 1958)] possess a dorsal meatus bypassing the respiratory airways, leading to an olfactory recess. Remarkably (but perhaps not so owing to the ultimate origin of cetaceans from terrestrial artiodactyls) CMM-V-4536 (Figs. 1–4, 7) and B. acutorostrata (Figs. 6–8) also possess the same gross morphological suite of olfactory features that characterize macrosmatic mammals: (1) separate olfactory and respiratory airflows (Figs. 7, 8); (2) dorsal nasal meatuses; (3) isolated olfactory recess located caudal to the posteroventral opening of the dorsal nasal meatus into the nasal passage/nasopharynx; (4) probable unidirectional airflow through the recess (i.e., exhaled air in its vast majority probably does not enter the olfactory recess); and (5) following inspiration, stagnation within the recess would be ideal for “chromatographic” odorant separation (Mozell, 1964; Schoenfeld and Cleland, 2005) and odorant vapor absorption (Craven, 2008).

In CMM-V-4536 and B. acutorostrata, the olfactory recess is essentially a blind end chamber. However, rapid exchange of the stagnant air within this recess would occur during inhalation from the high-pressure airflow along the dorsal nasal meatus and possibly by a low-pressure differential created, in accordance with Bernoulli's principle, at the posteroventral opening of the dorsal nasal meatus as inhaled air increased in speed down through the nasal passages (Fig. 8).

Why would an Eocene protocetid, CMM-V-4536 (Figs. 1–4, 7), and B. acutorostrata (Figs. 6–8) possess the same gross morphological suite of olfactory features that characterize macrosmatic mammals and by inference a reasonably well-developed sense of smell? At least for the protocetid (CMM-V-4536), a reasonable explanation could be that this is simply the retention/expression of the primitive artiodactyl state, albeit reduced. The degree to which the olfactory system is reduced in this Eocene protocetid cetacean when compared with its terrestrial antecedents could simply be credited to evolutionary loss through lack of use. That extant odontocetes have none of the obvious osteological correlates associated with olfaction might lead one to assume that mysticetes, which are temporally equally far removed from their terrestrial and archaeocete ancestors, would compare closely with odontocetes in this regard. However, the remarkable osteological parallels between extant macrosmatic mammals, CMM-V-4536, and B. acutorostrata suggest just the opposite and highlight one of the many differences between extant odontocetes and mysticetes. Extant mysticetes have an olfactory system that is developed far beyond what would be expected if the sense of olfaction was vestigial both for them and their archaeocete ancestors.

There is now little doubt that mysticetes have a more highly developed olfactory ability than microsmatic mammals like humans (Thewissen et al., 2011). Thewissen et al. (2011) hypothesize that bowheads, Balaena mysticetus use olfaction to detect conspecific mates and/or more likely clouds of the plankton on which they feed. Evidently, krill give off a peculiar odor, partly caused by dimethylsulfide and pyridines (Nevitt, 1999). Minke whales have a much more diverse diet (Perrin et al., 2009), in which case, if they are using olfaction in their pursuit of prey, it is not known what (other) airborne cues they are responding to.

The osteological features associated with olfaction in CMM-V-4536 show that during the Eocene (and certainly no later than the Oligocene, if CMM-V-4536 derives not from the Eocene Piney Point Formation but rather from the upper Oligocene Old Church Formation) an essentially modern balaenopterid olfactory architecture had already evolved. The balaenopterid olfactory apparatus evidently represents a conservative morphology surrounded by other osteological landmarks that changed much more conspicuously (Fig. 7). If an essentially modern balaenopterid olfactory apparatus was achieved so early in cetacean evolution, a careful examination of still older taxa will likely show the changes that must have occurred between terrestrial artiodactyls and the essentially modern olfactory morphology revealed by CMM-V-4536.

Extant odontocetes have no nasal turbinates; that area having been “squeezed” out between the expansion of the cranial cavity and posterior migration of the nasal passages, the former is separated from the latter only by the thin-walled, and generally imperforate, bone of the ethmoid/presphenoid/frontal complex (Ichishima, 2011). That extant odontocetes have no turbinates may explain in part why their external nares are so close to their brain; level with, or posterior to a transverse plane through their orbits, whereas in mysticetes, the external nares are still far removed from their cranial cavity occupying a position anterior to the transverse plane through their orbits (in Fig. 6A, notice the great length and thickness of the frontoparietal complex; essentially a structural “I-beam”; see Fig. 7B1,B2 and below). The more forward position of the external nares in the extant balaenopterid skull relative to that in odontocetes is interpreted here as the result of the evolutionary interplay between the posterior migration of the external nares countered/opposed by the need to retain a fully functional olfactory apparatus and the forward migration of the supraoccipital/cranial vertex. The conspicuous forward thrust of the vertex in balaenopterids (in both absolute distance and proportionally when compared with both archaeocetes and odontocetes) is likely a consequence of their evolutionary preference toward bulk feeding. This mode of prey capture is described elsewhere and the energetics involved therein continues to be the focus of research attention (Pivorunas, 1977, 1979; Lambertsen, 1983; Lambertsen et al., 1995; Goldbogen et al., 2007, 2008, 2010, 2011; Goldbogen, 2010; Pyenson et al., 2012). It is not yet known how much force is needed to close balaenopterid jaws once the pleated throat is engorged with food-laden water, but at the very least, most of that force has to come from jaw adductor musculature, which in turn take their origin on the skull (Beauregard, 1882; Beneden, 1882; Lambertsen et al., 1995). Whatever those adductor contraction forces are, they are transferred to the bones of the skull and in turn through the occipital condyle to the cervical vertebrae. The forward position of the vertex increases the distance from the occipital condyles (the fulcrum) to the top of the vertex, a path along which epaxial muscles have their origin (Fig. 6A), and consequently also increase their mechanical advantage on the skull during contraction. The distance from condyle to vertex represents the “in lever arm” of a mechanical system, coupled with the I-beam configuration of the greatly thickened midline frontoparietal complex (Fig. 6A) capable of providing the mechanical advantage and cranial strength necessary to counter the demands placed on their disproportionately large skulls while lunge feeding. We propose that the balaenopterid olfactory apparatus has survived to the present from its archaeocete antecedents because it was used to detect airborne odorants, and the olfactory system was “protected” in its location within the vertical thickness of the frontoparietal midline I-beam complex, a long-term evolutionary trajectory not taken by odontocetes—echolocating single-prey predators.


  1. Top of page
  2. Abstract
  6. Acknowledgements

The authors express their deepest gratitude to R. Ison for collecting and donating CMM-V-4536 to the Calvert Marine Museum. C. Potter, J. Ososky, N. Pyenson, and D.J. Bohaska are gratefully acknowledged for providing access to the collections of modern and fossil cetaceans in the United States National Museum of Natural History, the Smithsonian Institution. J. Pojeta (USNM) generously allowed them to whiten and photograph CMM-V-4536 in his laboratory. The CT scans were made possible by B. Frohlich (USNM). J. Siewerdsen [The I-STAR Laboratory ( at Johns Hopkins University] provided liberal access to Mimics® in his laboratory and J. Nance (CMM) produced the images used herein that were crafted using that software. The minke whale skulls were sectioned by A. Pivorunas. The authors benefited from discussions with B. Beatty (New York College of Osteopathic Medicine) during the writing of this article. For reviews of this manuscript, they are grateful to M. Uhen, C.S. Gutstein, and one anonymous reviewer for their constructive critiques. They also gratefully acknowledge J. Trejo, the managing editor at The Anatomical Record.


  1. Top of page
  2. Abstract
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