Thursday, January 28, 2010

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.


J. Velez-Juarbe said...

Nice post!

Whitmore and Barnes paper was my intro to cetotheriids, they seem to be an interesting group. Pachyosteosclerosis is the word used when both conditions are found (Domning & Buffrénil, 1991), as in most* sirenians. I didn't knew about champsosaurs. If I remember correctly other incidence of pachyostosis or osteosclerosis also include Placodus, some mosasaurs, and in juvenile plesiosaurs. All likely associated with some form of benthic feeding.
*Some Eocene and Oligocene species were only osteosclerotic.

I’m looking forward to the upcoming installment of this series!

Robert Boessenecker said...

The Whitmore and Barnes paper has its strengths and weaknesses; unfortunately they chose to include "cetotheres" such as Parietobalaena, Cophocetus, etc. which clearly do not form a monophyletic group with true Cetotheriidae sensu stricto. That, and their subfamily divisions were not cladistically tested, and they really (aside from Herpetocetinae) do not add to the discussion, and in fact may subtract from it because it gives the illusion that this group is better understood than it actually is.

Otherwise, thanks - I forgot to mention 'pachyosteosclerotic'. At some point I'm going to discuss that new placodont article on here. I'll get around to talking about Mammalodon later in the week.

Alton Dooley said...

Thanks for the post, Bobby; great summary and explanations.

The Carmel Church Diorocetus specimen is now on exhibit, incidentally. We plan for it to be on display for probably the next year, at least.

A couple of additional notes from our paper:

We had some hints that there may be on ontogenetic component to the degree of osteosclerosis. The sub-adult type of Diorocetus had ribs in about the same range as contemporary adult "cetotheres". So far, I haven't been able to measure juvenile ribs from Eobalaenoptera, Metopocetus, etc., since most of the Carmel Church whales are adults. (However, I may have a juvenile Metopocetus in my lab...)

Oligocene mysticetes like Aetiocetus seem to have ribs just as dense as Diorocetus, so it does seem to be primitive for Mysticeti. However...

While archaeocetes do have pachyosteosclerotic ribs, the condition seems to be limited to the distal ends of the ribs, while the mysticetes we looked at are ostersclerotic throughout their length. Also, while mysticetes have an increased percentage of cortical bone, there doesn't seem to be any thickening of the bone. In other words, the ribs look like completely typical mysticete ribs until broken open (no swollen, banana-like ribs). Interestingly, when we collected them, the first thing we noticed was how heavy they were (I've picked up a lot of ribs at Carmel Church!). Then we saw one broken in half and understood why it was so heavy.

As you say, it seems that, in general, the more crownward we go in Mysticeti the less dense the ribs are. However, even the crown mysticetes are MUCH more dense than any odontocetes we've looked at (we included one in the paper, but I've looked at a few others since). It's so dramatic that I bet you can distinguish odontocete and mysticete ribs based on cortical bone percentage alone. When did osteoporosis appear (derived for Odontoceti, maybe)?

Just some (benthic) food for thought! I look forward to seeing your next post.

Robert Boessenecker said...

Interesting that you mention such a contrast between archaeocetes and basal mysticetes; that definitely makes the benthic feeding hyothesis more convincing. You guys should have made that distinction in the paper! ...Unless I'm being an idiot, and am I'm not remembering it completely...

Anyway - thanks for the additional tidbits - part 2 will be coming soon...

Alton Dooley said...

Page 16:

"This cortical bone thickness occurs throughout the length of the rib, not just in the ventral ends like in archaeocetes (Buffrénil et al., 1990), indicating that this had a ballast function rather than a role in maintaining trim or preventing rolling like it is presumed to have had in basilosaurids."

I think that's the only place we mentioned it, though.

Robert Boessenecker said...

Oh sh*t, my bad! Well... now I know! That would be a really neat study - looking at comparative rib histology across cetacea...

By the way, it's still going to be at least another day until I write about Mammalodon; I'm swamped (and sick) this week.

Alton Dooley said...

"That would be a really neat study - looking at comparative rib histology across cetacea..."

I agree completely!

Hope you feel better.

Brian Lee Beatty said...

I'm sorry I missed so much of this, and Butch's blog lately. I was swamped with work during the holidays, and then with my father's illness. He died on Feb 3, and I just got back from his funeral.

I really appreciate the careful attention to this paper, it was a stimulating thing to work on, something that we had to cut short or it would have become endless and unwieldly.
Thanks again.