Benthic feeding in basal mysticetes, part 1: paleopathology of a Miocene "cetothere"

The last couple years have been relatively good for cetacean paleontology; we saw the description of the protocetid Maiacetus (which I still have to cover...) about a year ago, the rediscription of "Balaenoptera" gastaldii, now recognized to be a fossil gray whale, the fantastic analysis done by T.A. Demere et al. regarding the presence of baleen in toothed mysticetes, Larry Barnes' Albireo monograph, the odontocete cranial lexicon by Jim Mead and Ewan Fordyce, the taphonomic study of the Sharktooth Hill Bonebed by Nick Pyenson and colleagues, Frank Whitmore and L. Barnes' Herpetocetus monograph, Steeman's (2009) paper on Uranocetus, Brian Beatty and Alton Dooley's paper on paleopathology in the Carmel Church Diorocetus, and most recently Erich Fitzgerald's paper on Mammalodon, among many others which I've probably failed to remember.

For the purposes of the next couple posts, I'll be focusing on basal mysticete feeding, and will be discussing Beatty and Dooley (2009), Fitzgerald (2010), and Demere et al. (2008).

The pathologic left dentary of Diorocetus from the Carmel Church Quarry in Virginia, From Beatty and Dooley (2009). The pathologic fracture is directly below the 'c' in 10 cm.

For those of you who pay close attention to Alton Dooley's blog "Updates From the Vertebrate Paleontology Lab", Dooley does quite a bit of fieldwork at the Carmel Church Quarry, an exposure of the middle Miocene Calvert Formation. The Calvert Formation in Maryland and Virginia is famous among amateur paleontologists and fossil collectors for the stunning abundance of easily collected fossil shark teeth. The Calvert Formation is also famous for its incredible cetacean fossil assemblage - primarily chronicled by Remington Kellogg, the father of marine mammal paleontology (although there have been a number of papers recently on Calvert Fm. and Chesapeake Group cetaceans). One of the recent discoveries at Carmel Church is a beautiful skeleton of the archaic mysticete Diorocetus. This skeleton includes a complete skull (which initially was fragmented to hell, but Dooley and the VMNH have managed to put all of the pieces back together, and it looks pretty damn nice), dentaries, anterior vertebral column, and nearly complete set of ribs.

Fracture and pathology in the left dentary, from Beatty and Dooley (2009).

The left dentary was found to have an odd fracture in it; the two parts didn't match up very well, and it did not appear to be a post-depositional fracture, like most of the fractured material at Carmel Church (it is not clear if the jumbling and fracturing of bones is biostratinomic or diagenetic - e.g. peri- or post- burial). Additionally, a callus of bone was identified around this fracture, and can be seen well in x-rays (above). Additional pathologies were noted in the anterior tips of the premaxillae, and the left squamosal, which was significantly less dense and more porous than the right (potentially due to decreased stress during post-injury feeding?). Most interesting is the fact that although the callus formed, the fracture never healed, suggesting repetitive use that kept the bone from healing, i.e., the anterior and posterior portions of the dentary remained as separate elements until death, allowing some motion at the fracture site.

What could cause this sort of a fracture? The authors indicate the most common cause of these sorts of injuries in extant mysticetes are collisions with ships and boats - which obviously did not exist in the middle Miocene. Other possibilities include predation, agonistic (violent) intraspecific behavior, and a collision or impact with seafloor topography. If this is a case of predation, then our friend survived, given the amount of healing (i.e. callus formation). Agonistic behavior among mysticetes is poorly documented, and are largely restricted to injuries on the order of cuts and scrapes. Otherwise, the authors conclude, lies the chance that this injury was caused by an impact with the seafloor, or submarine outcrop (i.e. much of the California coastline I'm used to has rocky points and sea stacks and a topographically complex seafloor with many submarine exposures of rock). Apparently, injuries of this sort are the most commonly observed trauma on dead gray whales, which are benthic suction feeders.

Before I continue, I'll add a quick note about mysticete feeding. Among modern mysticetes, there are three observed modes of feeding: Lunge/engulfment feeding, suction feeding, and skim/ram feeding. Lunge or engulfment feeding is mostly utilized by balaenopterid whales (e.g. Blue, Fin, Sei, Minke, and Humpback whales), and is characterized by the whale opening its mouth and engulfing clusters/'schools' of nektonic organisms (i.e. krill, fish, etc.). The mouth is closed, and water is actively 'pushed' out of the baleen plates (I can't remember if both the tongue and throat are used for this action, or one or the other). Skim feeding is employed by balaenids (and the sole existing neobalaenid, Caperea, the pygmy right whale), and consists of the whale slightly opening its mouth while swimming forward; nekton prey-rich water enters the oral cavity, and during forward movement, water flows passively out of the oral cavity through the baleen, which traps the poor critters inside the mouth; this feeding is often at or near the surface. Benthic feeding, on the other hand, is only observed in the gray whale (Eschrictius robustus), which will filters through muddy substrate; fine sediment is entrained in suspension, and can escape with water through the baleen, trapping benthic organisms (i.e. amphipods) in the oral cavity. The major problem is that the most basal known fossil mysticetes retained teeth, and did not yet have baleen. More on that later, though.

Cross sections of mysticete ribs; A-B is the new Diorocetus specimen; C - undescribed basal edentulous mysticete, Oligocene, Oregon; D-E-toothed mysticete Aetiocetus cotylaveus; F & I - balaenopterids (latter is Eobalaenoptera); G-H - cetotheriid (sensu stricto) Metopocetus; K - Diorocetus hiatus; L- Balaena ricei. All of these have osteoclerotic ribs, with the exception of Eobalaenoptera and Balaena ricei, which are part of the mysticete crown group.

Another interesting feature Beatty and Dooley (2009) noted was the osteosclerotic condition of the ribs in Diorocetus. In contrast, extant cetaceans have postcranial bones that are osteoporotic (yes, like menopausal women). For the purposes of this discussion, there are two types of bone: cancellous, and cortical (spongy and dense, respectively; there are many other types, which I won't go into here; read papers by de Ricqles and Horner for more info on paleohistology). Cortical bone (or the cortex) is the strong, outer portion, while cancellous bone is the very spongy middle part. Osteosclerosis refers to increasing bone density by adding cortical bone toward the center of the bone, making the cancellous inner portion thinner. Pachyostotic bone is where cortex is increased outward, giving the bone an 'inflated' look - sirenians have pachyostotic (and osteosclerotic) bones. Osteoporosis simply refers to bone that is very porous, and generally lense dense - this is simply a condition; in cetaceans it is 'normal', but in adult women it is a bad condition which can lead to fractures. Osteosclerosis, on the other hand, can act as a sort of 'bio-ballast' adaptation for maintaining (or simply attaining) neutral bouyancy - most terrestrial vertebrates are positively bouyant, especially in seawater. Champsosaurs, I just learned in Jack Horner's class, have retained super-dense embryonic bone into the adult stage as a ballast adaptation.

Beatty and Dooley (2009) observe that Diorocetus hiatus is one of the last mysticetes to retain osteosclerotic bone, and that it may be related to bouyancy problems associated with benthic feeding. Indeed, osteosclerotic bone is a plesiomorphic feature among not only mysticetes, but is also characteristic of pelagic archaeocetes as well (I am not referring to the clade Pelagiceti, by the way). So, it is certainly possible that this is an adaptation for benthic feeding. However, it is also possible that this is a case of phylogenetic inertia, similar to the retention of an enlarged mandibular foramen in mysticetes.

The nature of the likely cause of the mandibular injury may also suggest benthic feeding as well (unless this was a freak accident; i.e. a lunge feeding whale impacting the seafloor). While the repetitive feeding behavior that kept the fracture from healing may have been caused by benthic feeding, *if* Diorocetus had been a lunge feeder, the incredible stresses experienced by mysticete dentaries during this action would certainly keep the fracture from healing. In any event, taken as a whole, the benthic feeding idea is very intriguing, and raises some very interesting questions regarding the primitive mode of feeding by baleen-bearing mysticetes. I understand that the authors have received criticism for some of the more speculative ideas in the paper, you'll find none from me; this study brings up some very interesting ideas, and I'll be covering more on the topic of benthic feeding on my next post, regarding the enigmatic toothed mysticete Mammalodon.

Also see:
Alton Dooley's blog post about the article, and Brian Beatty's post as well.


Beatty, B.L. and A.C. Dooley. 2009. Injuries in a mysticete skeleton from the Miocene of Virginia, with a discussion of bouyancy and the primitive feeding mode in the Chaeomysticeti. Jeffersoniana 20:1-28.

Bioturbation and ash beds in the Purisima Formation

This is really just a collection of annotated photos I took over winter break, and are sedimentological and ichnological in nature. These are all photos taken of Purisima Formation exposures in San Mateo county. During the winter, more intense storm activity cleans off the coastal cliffs and makes examining trace fossils, sedimentary structures, and bed geometry an easier task. In some cases, the most beautiful trace fossils and sedimentary structures are associated with ash beds. Above is part of a very thin ash bed (8-30cm thick - the ligher colored sediment) that has almost been destroyed by bioturbators (by the way, bioturbation is the disruption of primary sedimentary fabric by burrowing organisms/infauna). In fact, for most of its exposure it has been pierced by burrows (where the ash has been displaced into the burrow fill) that it looks like a dotted line. Above shows a U-shaped burrow; I can't remember what taxon this is - because some of them (i.e. Diplocraterion?) are defined based on spreiten (laminae within the burrow) inside the 'U'.

Here yu can see how little of the original bed is left; much of the ash has been introduced as burrow fill, and mixed and diluted with regular sediment (fine-very fine silty sandstone in this case), hence the blotches looking slightly less 'pure' than the primary ash.

A couple hundred feet away this bed thickens and isn't completely chewed up by bioturbation, enough so that you can see original sedimentary fabric within. In this case, it is a mix of swaley cross stratification (a small-scale version of hummocky cross stratification) and climbing ripples. Both of these sedimentary structures indicate uni- or bi-directional flow with a relatively high rate of sedimentation, i.e. sediment is just dumping out of suspension. This can happen during hyperpycnal flow - often occuring as a dense plume of sediment rich water introduced into the ocean from a river mouth, say after a big storm.

This ash bed, on the other hand, is huge. There's a reason I don't have a scale bar; this is about a 5-10 meter thick ash bed. This has a completely different set of weird features - some pretty incredible soft sediment deformation. These look like giant scale ball and pillow or loading structures.
This cliff right here is about 200 feet high, and we're looking at about 1/3 of it or so. These S.S.D. features continue for the entire outcrop length of this bed. The thinner ash bed featured above is visible in the very bottom of this photograph. The intense loading features here could, of course, be caused by a relatively rapid influx of a LOT of ash to the seafloor, which could lead to liquefaction of more typical sediment at the former (i.e. pre eruption) sediment-water interface (i.e. sea bottom), and leading to the big pillow-like lobes of ash, and the long upward pointing 'fingers' of sand.

Uranocetus and hearing in mysticetes

Hey Folks, Sorry about the delay; I realize its been over a month since I last posted anything. Winter break was not exactly relaxing, and the parts that neared relaxation were spent doing fieldwork (which definitely yielded some interesting material). In other news, my first technical paper has been tentatively accepted for publication by the UCMP-published journal PaleoBios; I'm approximately 99% done with revisions at this point, so you'll hear more about it after it's in press.

Recently two mysticete related papers have been published - Erich Fitzgerald's monograph on the truly bizarre Mammalodon colliveri, which I'll cover later, and M.E. Steeman's (2009) thought provoking paper naming the new "cetothere" Uranocetus from the Miocene of Denmark and its implications for mysticete hearing.

The cranium of Uranocetus, from Steeman (2009).

First off, "cetotheres" are a wastebasket group of generalized archaic baleen whales that don't fit nicely in modern families, although Bouetel and Muizon (2006) have redefined the Cetotheriidae sensu stricto as a small group with some very strange cranial features, including my personal favorite, Herpetocetus. Most other cetotheres (Cetotheriidae sensu lato) were placed into newly named families (Pelocetidae, Aglaocetidae, and Diorocetidae) which were sister taxa to the Balaenopteridae all included in her concept of the Balaenopteroidea (but not in the concept of the Balaenopteroidea advocated by Demere et al. 2005, which is Eschrictiidae + Balaenopteridae). Bottom line is Uranocetus is some kind of stem baleen-bearing mysticete, no matter whose phylogeny you use. The dentary of Uranocetus (from Steeman, 2009).

Interestingly, while it is placed rather close to Balaenopteridae, it still retains a large mandibular foramen, a plesiomorphic feature for mysticetes. The mandibular foramen is very small in extant mysticetes, but extremely large in odontocetes, so much that the posterior portion of the dentary is a thin bony shell (the "pan bone") that houses the mandibular fat pad. The lateral margin of the dentary is extremely thin, so that high frequency sounds can pass through without significant volume loss (Nummela et al. 2007, Steeman 2009). High and mid frequency sounds pass through this, and are then channeled up through the mandibular fat pad and up to the tympanic plate; in odontocetes, this is more or less a functional analog of the external ear pinna. And, by the way, all these strange auditory features are adaptations for allowing directional hearing underwater; otherwise terrestrial mammals hear via bone conduction hearing (sound travels faster in water, and the mammalian body is roughly as dense as the surrounding aqueous medium), and sounds more or less arrive at each ear too quickly to discern the direction. Cetaceans have separated their ear bones (petrosal, tympanic, and ossicles) from the temporal bone and surrounded them by sinuses to isolate these complexes from the skull to hear directionally. While this was initially thought to be an adaptation for hearing high frequency sounds and thus an adaptation for echolocation (a capability restricted to the odontoceti, and associated with high frequency sounds), recent research has identified the pan bone/enlarged mandibular foramen (i.e. bony correlates of the mandibular fat pad) in many archaeocetes, including Ambulocetus, remingtonocetids, protocetids, and basilosaurids (Nummela et al. 2007) as well as many archaic toothed- and toothless mysticetes, such as Aetiocetus weltoni, Mammalodon, Eomysticetus, and even Herpetocetus. This led Nummela et al. (2007) to reason that, since neither archaeocetes or mysticetes have any anatomical features associated with echolocation, that this feature is probably instead related to underwater hearing in general, and not just echolocation.

Dentaries of various archaic mysticetes and an archaeocete, from Fitzgerald (2009).

The fact that most basal mysticetes have an enlarged mandibular foramen suggests that this is a feature inherited from basilosaurid ancestors. Interestingly, modern mysticetes are adapted for hearing low frequency sounds, which pass through dense bone without significant volume loss. While Uranocetus has a large mandibular foramen, the lateral wall is too thick to be useful for hearing anything aside from low frequency sounds (which Uranocetus is adapted to hear based on its cochlear structure; Steeman 2009). The exact same thing is seen in Herpetocetus, which is also adapted for low frequency hearing, but has a large foramen with a thick lateral wall. This suggests that at least in these later diverging taxa, that the large mandibular foramen was a vestigial feature perpetuated by phylogenetic inertia.

Lateral aspect of a (not so typical) mysticete (Eshrichtius robustus, the Gray Whale) skull and dentary in articulation, from Johnston et al. (2009).

Steeman (2009) reasoned that the mandibular foramen decreased in size to strengthen the dentary due to the intense forces involved during feeding. Above shows a gray whale skull and mandible in articulation, just to give you an idea of how strange the mysticete feeding apparatus is (exclusive of baleen). In any event, I've been thinking about this quite a bit recently, and got to add a (very short) synopsis of this in my manuscript revisions, but you'll hear about that soon enough.

References-
Deméré, T.A. and A. Berta (2008). Cranial anatomy of the toothed mysticete Aetiocetus weltoni and its implications for aetiocetid phylogeny. Zoological Journal of Linnean Society, 154(2): 308-352. PDF

Deméré, T.A., A. Berta, and M.R. McGowen. 2005. The taxonomic and evolutionary history of fossil and modern balaenopteroid mysticetes. Journal of Mammalian Evolution 12:99-143.

Fitzgerald, E.M.G. 2009. The morphology and systematics of Mammalodon colliveri (Cetacea:Mysticeti), a toothed mysticete from the Oligocene of Australia. Zoological Journal of the Linnean Society 110p.

Johnston, C., T. Deméré, A. Berta, J. St. Leger and J. Yonas. 2009. Observations on the musculoskeletal anatomy of the head of a neonate gray whale (Eschrichtius robustus). Marine Mammal Science PDF

Nummela, S., J.G.M. Thewissen, S. Bajpai, T. Hussain, and K. Kumar. 2007. Sound transmision in archaic and modern whales: anatomical adaptations for underwater hearing. Anatomical Record 290:716-733.

Steeman, M.E. 2009. A new baleen whale from the late Miocene of Denmark and early mysticete hearing. Palaeontology 52 :1169-1190.