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.
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.