Is Puijila a pinniped?

Back in February 2009, Natalia Rybczynski and colleagues surprised the paleomammalogy community with their Nature paper naming a new genus and species of early pinniped, Puijila darwini. The holotype skeleton is relatively complete, and include fore- and hind-limbs along with much of the vertebral column, both jaws, and a well preserved skull. Puijila was about one meter long, and would have appeared relatively similar to a modern river otter. It had a short snout and a wide head, with large eyes and relatively high-crowned teeth. The teeth of Puijila still retain many of the cusps lost in modern pinnipeds, and also exhibit pits in the roof of the mouth for the lower teeth (embrasure pits). Unlike modern pinnipeds, it had a long tail, and did not have its fore- and hindlimbs modified into flippers. Puijila was discovered in 2007 from the Haughton Formation on Devon Island in Nunavut (formerly Northwest Territories in Canada). The Haughton Formation was deposited in an impact crater – the impact has been dated to 24-21 Ma (earliest Miocene), and fossil mammals from the Haughton Formation corroborate an early Miocene age. The Haughton Formation was deposited in an ancient lake that filled in the impact crater. In fact – if it were not for the impact, there would be no sedimentary rocks of Miocene age preserved that far North – all the young rocks have been eroded away by glaciation.

The skull and jaw of Puijila darwini, from Rybczynski et al. (2009).

The holotype skeleton of Puijila darwini (from http://nature.ca)

Previously, the earliest diverging pinniped (and arguably more derived than Puijila) is Enaliarctos, a fur seal sized pinniped from the latest Oligocene and early Miocene of California and Oregon. Enaliarctos retains carnassials, although many of the other dental features are very simplified and reduced, trending toward the condition in modern pinnipeds. Enaliarctos also exhibits limbs developed into flippers – and is very clearly a pinniped. But the relationships of Puijila – to pinnipeds and other carnivores – are not so clear. Because of the older age of Enaliarctos and its marine occurrence, Puijila is hypothesized to represent a lineage of early pinnipeds that stayed in their freshwater niche while marine pinnipeds like Enaliarctos evolved, remaining otterlike. It suggests that pinnipeds went through an otterlike freshwater stage before invading the ocean. Prior to this, Enaliarctos suggested a direct to saltwater invasion – although due to the absence of intermediates, it was not exactly clear one way or the other.

The skeleton and life restoration of Enaliarctos mealsi, from Berta et al. (1989).

Before we continue – I must also be specific about some clade names. Although Rybczynski et al. (2009) refer to Puijila as a member of the Pinnipedia – which is not really the traditional cladistic nomenclature for basal pinnipeds. Annalisa Berta and colleagues (1989) proposed the clade Pinnipedimorpha, for Enaliarctos and all later diverging pinnipeds. Berta (1994) later proposed the name Pinnipediformes for Pteronarctos and all later diverging pinnipeds. Pinnipedia is nested within Pinnipediformes, and Pinnipediformes within the Pinnipedimorpha. Within this traditionally accepted and utilized framework, Puijila’s obviously more primitive morphology than Enaliarctos indicates it should be referred to as a pinnipedimorph.

Rybczynski et al. (2009) listed six characteristics that unite Puijila with Enaliarctos and other pinnipeds. These are: a posteriorly expanded palate (the palate extends posteriorly past the upper toothrow in pinnipeds), an enlarged infraorbital foramen (occurring within pinnipeds due to larger whiskers and greater innervation of the snout), a shelf-like protocone on the upper fourth premolar (occurring in basal pinnipeds and some related arctoids), an upper second molar that is reduced and positioned medially to the upper first molar (reduction of the molariform teeth to conical teeth is a major dental transition within the pinnipedimorpha), a posterodorsally expanded scapula (a feature of pinnipeds, which often have very broad scapulae, an adaptation for swimming), and an expanded deltopectoral crest of the humerus (another feature in pinnipeds related to swimming).

Some of these features may be of only limited use in hypothesizing a close relationship between Puijila and pinnipeds. First, an enlarged infraorbital foramen (the small hole below the eye socket in a skull) also occurs in many mustelids, such as badgers (Taxidea), weasels (Mustela), and most (if not all) otters (e.g. Lontra, Enhydra); in badgers and weasels, this is due to a more innervated and sensitive snout, an adaptation for digging in burrows. This characteristic may not be useful in identifying early pinniped relatives, as otters (another hypothesized pinniped sister taxon) exhibit this feature – presumably evolving for the same purpose. The two postcranial features – an enlarged deltopectoral crest and a posterodorsally expanded scapula – may not be coded correctly in Puijila. To be quite honest, based on the available photographs – these features do not appear too different between Puijila and a river otter (Lontra), and don’t really exhibit the derived condition, which is much more extremely developed in Enaliarctos and other fossil and modern pinnipeds). This leaves only three reliable characters behind.

Skeletons of Enaliarctos (A), Puijila (C), and Lontra (D).

One of these features – a posteriorly expanded hard palate – also appears in the aberrant arctoid Kolponomos, as well as Pachycynodon and Allocyon (Tedford et al., 1994). This feature appears to be more widely distributed than previously admitted, although it is worth mentioning that it is probably an adaptation towards aquatic feeding. The two dental characteristics are probably more reliable, although it is odd to note that these two dental characteristics are also found in Kolponomos. Kolponomos will feature more in part two of this post, as it is both a fascinating creature which I have not yet properly covered on this blog, and it is also extremely topical to the subject of Puijila.

A wonderful reconstruction of Kolponomos by Ken Kirkland, published in Neptune's Ark by David Rains Wallance.

There are a whole host of pinniped characteristics that Puijila does not have, or features that were not described in enough detail to independently evaluate. Cranial and dental features that characterize pinnipeds (either at the level of the Pinnipedimorpha, Pinnipediformes, or Pinnipedia) include a reduced upper first molar, reduced cingulum on the upper first molar, an absent or reduced metaconid, loss of the embrasure pit between the upper fourth premolar and first molar, closely spaced mastoid and paroccipital processes, a reduced nasolabialis fossa, reduced cingulum on the upper third incisor, and a reduced trigonid cusp on the lower molars. None of these derived conditions appear to be present in Puijila. A number of postcranial features which characterize pinnipeds (either at the level of the Pinnipedimorpha, Pinnipediformes, or Pinnipedia, as above) include a short and robust humerus, enlarged tuberosities of the humerus, a flattened radius and ulna that are longer than the humerus, emphasis of certain digits in the hand and foot (i.e. largest digit in the hand being the first or “thumb”, and the lateral and medialmost digits of the foot being largest and the smallest being the middle digit), a short, flattened femur with an enlarged greater trochanter and medially inclined condyles, a reduced tail, and a short ilium (bone in the pelvis). Curiously, none of these features are present in Puijila – although nearly all of them (perhaps all – I can’t remember off the top of my head) occur in Enaliarctos.

In summary, there are very few features that actually unite Puijila and pinnipeds. The cladistic analysis of Rybczynski et al. (2009) was relatively limited, both in terms of the number of fossil and modern species used, and also with regard to the number of morphological characters used in the analysis. An earlier study – considered to be the landmark phylogenetic analysis of pinnipeds, Berta and Wyss (1994) – utilized 143 characters, while Rybczynski et al. (2009) only used 42. Granted, the earlier study focused on relationships within pinnipeds – and many of those characters may or may not apply to Puijila and other similar arctoids.

Because of the above, I am skeptical that Puijila has a close relationship with pinnipeds – and although I’m not convinced, I am equally receptive to the idea pending further analyses. There is much we’ve been waiting for – a detailed description of its anatomy and large, detailed figures of its skeleton were not included in the original study, which is understandable given the short length of Nature papers (however, it was not included as supplementary info either). There is certainly more work to be done, and there are rumors of a more detailed phylogenetic analysis in the works; such a study should include a comprehensive description of the skull and skeleton of Puijila accompanied by exhaustive figures (formerly difficult, but several modern journals have made this a far less difficult prospect), sample a broader variety of caniform carnivorans as well as more fossil and modern pinnipeds (fossil pinnipeds with postcranial skeletons such as Allodesmus, Thalassoleon, Leptophoca, Acrophoca, Piscophoca, Imagotaria, Neotherium, and Proneotherium) as well as the “beach bear” Kolponomos (which was not included in the original analysis or discussed by Rybczynski et al. 2009). Puijila certainly could belong to some group of otterlike “protopinnipeds” as hypothesized, but given the few characters uniting them, it very well could be some sort of mustelid or other aquatic carnivore.

Further reading

Official Puijila website (Canadian Museum of Nature)

Puijila, a very basal 'pinnipedimorph' (this blog)

Commentary by Ed Yong (Not exactly Rocket Science)

Commentary by Brian Switek (Laelaps)

Literature cited

Berta, A., C.E. Ray and A.R. Wyss. 1989. Skeleton of the oldest known pinniped, Enaliarctos mealsi. Science 244:60-62

Berta, A. 1991. New Enaliarctos* (Pinnipedimorpha) from the Miocene of Oregon and the role of "Enaliarctids" in Pinniped Phylogeny. Smithsonian Contributions to Paleobiology 69.

A. Berta. 1994. New specimens of the pinnipediform Pteronarctos from the Miocene of Oregon. Smithsonian Contributions to Paleobiology 78:1-30

Rybczynski, N., Dawson, M.R., Tedford, R.H. (2009). "A semi-aquatic Arctic mammalian carnivore from the Miocene epoch and origin of Pinnipedia". Nature 458 (7241): 1021–24

R. H. Tedford, L. G. Barnes, and C. E. Ray (1994). "The early Miocene littoral ursoid carnivoran Kolponomos: Systematics and mode of life". Proceedings of the San Diego Society of Natural History 29:11-32.

Pinniped ancestry: the "Oligocene Seal" from South Carolina

One of the most fascinating aspects of the study of marine mammals are the origins of the land to sea transition in various groups. Often marine mammals are so adapted for marine existence, that it is difficult to identify what group (fossil or modern) they descended from. Such has been the case with the origin of whales, for example. While I'm certainly interested in cetaceans, there has been a ton written about them, and I'm currently more intrigued by pinnipeds.

While modern cetaceans don't necessarily look like their artiodactyl relatives, pinnipeds generally retain enough features that allows them to be readily identified as carnivoran mammals, straight down to the dog-like bark of California sea lions. Certainly, this should make identifying the terrestrial progenitors of pinnipeds an easier task. Or does it?

The prevailing opinion throughout much of the 20th century was that the Pinnipedia are diphyletic; the sea lions and walruses formed the "Otarioidea", who descended from the Ursidae, and the true seals (the Phocidae) descended from mustelid (or musteloid) ancestors. In 1973, Ed Mitchell and Richard Tedford described Enaliarctos mealsi from the Early Miocene Pyramid Hill member of the Jewett Sand in Kern County, California. Enaliarctos still bore an ursid-like shearing dentition, which is absent in all modern pinnipeds (which have generally homodont postcanine teeth). Enaliarctos was purported to be the common ancestor of the Otarioidea.

Later work (which at some point will be detailed on here) by Andre Wyss (UC Santa Barbara) and Annalisa Berta (San Diego State University), proposed a drastically different phylogeny of the pinnipeds, which suggested that pinnipeds were instead monophyletic, and that walruses (Odobenidae) were more closely related to the true seals (Phocidae), forming a new group, the Phocomorpha. Dozens of molecular phlyogenetic analyses have unequivocally supported pinniped monophyly, chucking the old diphyletic view out the window. The major tenets of the new studies are the following: 1) all pinnipeds descended from a common ancestor; 2) Enaliarctos is basal to the Otariidae, Odobenidae, and Phocoidea; 3) the Otarioidea is paraphyletic, as odobenids and desmatophocids are more closely related to the phocids; and 4) pinnipeds were derived from an ursid (bear) like ancestor sometime during the Late Oligocene, probably in the Northeast Pacific, where the oldest pinniped fossils are known.

Putative seal femora from the Late Oligocene of South Carolina, from
Koretsky and Sanders (2002).

In 2002, Irina Koretsky and Al Sanders reported on some partial femora from the Late Oligocene of South Carolina. According to Koretsky and Sanders, these femora are most similar to those of extant phocids, and list several features they share in common. However, they argued that the Late Oligocene age of these, as well as the occurrence of these in deposits of the Atlantic Coastal Plain, indicate that true seals were already present in the Atlantic Ocean when the very primitive Enaliarctos was just appearing in the Pacific Ocean. Thus, the monophyletic origin of pinnipeds was not supported by this fossil, and it appeared that true seals evolved in the Atlantic separately from the Otarioidea, which are (during the Oligocene and the Miocene) restricted to the North Pacific.

There are, of course, some issues with this study and its inherent implications, irrespective of the incomplete nature of the fossils. For starters, the fossil record is notoriously crappy; in fact, the Early Oligocene marine record is the poorest of all with regards to marine mammal fossils. Very few cetaceans are known from the Early Oligocene worldwide, for example, primarily due to the scarcity of marine rocks for this time, due to low sea levels caused by the Eocene-Oligocene climate crash. Pinniped fossils just "show up" after sea levels rise and deposit more marine sediments during the late Oligocene, in both the Pacific (Enaliarctos) and Atlantic (Phocid femora). So - it is entirely possible for even more primitive pinnipeds to be found in earlier sediments (or, as "lazarus taxa" in Late Oligocene rocks).

The completeness of these fossils requires additional scrutiny. Some of Koretsky's other work focuses on the major elements of the fore- and hind-limb of true seals (and lower jaws) but generally placing low importance on cranial material (Koretsky and Ray, 2008). Koretsky and Sanders (2002), however, did not compare these specimens with femora of Enaliarctos, or basal odobenids such as Proneotherium and Neotherium (or an unnamed basal odobenid described by Naoki Kohno early on, ~1990). Additionally, now that the putative stem-pinniped Puijila darwini has been described, it's femora should be compared with these specimens as well. These could very well turn out to belong to something more like Enaliarctos or Puijila that we don't yet have a record of in the Atlantic. However these fossils are interpreted, their Late Oligocene occurrence (if the provenance is accurate) is intriguing, and further field investigation of Late Oligocene sedimentary rocks of the Atlantic Coastal Plain (and elsewhere!) should be considered.

References:

Koretsky, I.A. and A.E. Sanders, 2002. Paleontology of the Late Oligocene Ashley and Chandler Bridge Formations of South Carolina, 1: Paleogene pinniped remains; the oldest known Seal. Smithsonian Contributions to Paleobiology 93: 179-183.

Koretsky, I.A., and Ray, C.E. 2008. Phocidae of the Pliocene of Eastern USA. In: C.E. Ray, D. Bohaska, I.A. Koretsky, L.W. Ward, and L.G. Barnes (eds.), Geology and Paleontology of the Lee Creek Mine, North Carolina, IV. Virginia Museum of Natural History Special Publication 14: 81-140.

Benthic feeding in basal mysticetes, part 2: Mammalodon, the freak

Sorry about the "short" delay; the last week or so has been pretty rough, between my Paleobiology course, getting sick, and administering/grading my first exam. But, all of that's over now, so I've been able to allot some time to this again.

My last post concerned paleopathology and histology of the "cetothere" Diorocetus hiatus, published by Brian Beatty and Alton Dooley last summer in Jeffersoniana. In it they posited that Diorocetus may have been a benthic feeder based on peculiar pathologies as well as an interesting pattern of rib osteosclerosis.

Comparison of the size of Mammalodon and a blue whale. From http://museumvictoria.com.au

There's been some buzz in the science blogosphere recently about the truly bizarre Australian toothed mysticete Mammalodon, the subject of a new monograph by colleague Erich Fitzgerald. I'll admit I've been anticipating this paper since Erich's talk at SVP in 2008 (the same session as my first ever SVP talk, you know, the one where no one could see any of my text). Some other blogs have covered Mammalodon already, but mostly just some of the stuff you already hear in the news; ya, it was a mysticete with teeth (all toothed mysticetes look pretty weird), and it likely a benthic suction feeder, so what? There's far more interesting 'meat' in the paper, if you will, that someone who wasn't a mysticete worker and therefore didn't have time or interest to read 110 pages might not pick up on. Okay, I didn't read the description, but I've read the in depth discussion.

The skull and dentary of Mammalodon. From http://museumvictoria.com.au

Mammalodon colliveri was originally described in 1939 from the Oligocene Jan Juc Formation of Australia, although it was not identified as a toothed mysticete until the 1980's when Ewan Fordyce (U. Otago, New Zealand) undertook additional preparation of the fossil. In 1966, Doug Emlong (an extremely prolific and gifted amateur collector) described a peculiar toothed cetacean he discovered in the Oligocene of Oregon: Aetiocetus cotylalveus. Emlong thought it was an archaeocete, but Leigh Van Valen soon after recognized several mysticete features. Toothed mysticetes may seem odd at first, but when you think about it - 1) teeth are primitive for cetaceans and indeed mammals, and 2) they had to eat with something before baleen evolved. Mammalodon shares many similarities with Janjucetus, including a short rostrum, short triangular supraoccipital, and large orbits; however, Mammalodon is distinct in having laterally oriented teeth, and a relatively flat rostrum.

Comparison of Mammalodon (left) and Janjucetus (right). From Fitzgerald (2010).

Mammalodon has some strange features - a short, flat snout, large, upward facing orbits, large foramina on the maxilla, upper teeth that project laterally, and peculiar wear facets on the lower dentition that look like they were filed down at the same time (so to speak) - i.e. they share wear facets oriented on one single plane. Some authors have interpreted the denticulate teeth of basal mysticetes like Llanocetus and Mammalodon to have had a role in filter feeding, much like the teeth of the extant crabeater seal (Lobodon carcinophagus). Fitzgerald (2010) rejected this interpretation, as he did earlier (2006) for the tooth morphology of Janjucetus. Based on the probable presence of hyaline cartilage in the jaw joint of Mammalodon (as opposed to fibrocartilage in lunge feeding balaenopterids), Fitzgerald also rules out lunge filter feeding. Bony correlates of baleen, nutrient foramina, are absent on the palate of Mammalodon, suggesting that it did not possess baleen (such as later diverging aetiocetids - I'll talk more about those next time). Taken in full, few features of Mammalodon suggest filter feeding, rather than raptorial/pierce feeding (aka, biting stuff). Aside from this, some of the features unique to Mammalodon such as the very short rostrum, large maxillary and mandibular foramina, and extreme tooth wear suggest an alternative behavior. Typically, large foramina indicate improved blood flow and innervation to a region; for example the tactile whiskers of pinnipeds are correlated with a greatly enlarged infraorbital foramen (a pinniped synapomorphy), relative to "fissipeds". In this case, the short rostrum, probable highly innervated oral region, and wear most likely due to substrate interaction, all point towards benthic suction feeding. Additionally, the up-and-forward facing orbits would have conferred some degree of binocular vision, similar to the walrus and the bizarrer walrus convergent odontocete, Odobenocetops.

Various archaeocetes (top row), mammalodontids (second row) and aetiocetids (bottom two rows). From Fitzgerald (2010).

Most interestingly are the implications of the phylogenetic hypothesis of this study on the evolution of feeding in the mysticetes, relative to other recent hypotheses. Raptorial feeding is primitive for cetacea as a whole, including basal mysticetes. Interestingly, Llanocetus, Janjucetus, and Mammalodon all form a southern toothed mysticete clade, and Fitzgerald (2010) lumped Janjucetus and Mammalodon into the family Mammalodontidae, scrapping the family Janjucetidae he proposed earlier (2006). Llanocetus exhibits no adaptations for suction feeding, although Janjucetus does, suggesting that suction feeding is derived for this clade, but not a typical feature of basal mysticetes in general. Thus, this suggests that whatever feeding mode the mammalodontids employed was likely not representative of early mysticetes, contra Fitzgerald (2006).

Feeding evolution in baleen whales. From Fitzgerald (2010).

What the hell is Llanocetus, anyway? Llanocetus is perhaps the most interesting and strange described/undescribed cetacean out there. Well, what does that mean? Llanocetus was collected from the late Eocene La Meseta Formation of Antarctica. Yes, the Eocene of Antarctica, my friends. Why is that particularly awesome? The Eocene is dominated by archaeocetes, and elsewhere on earth during the late Eocene fantastic critters like Basilosaurus and Dorudon were kicking ass and taking names. And Llanocetus is the earliest known mysticete, let alone record of the Neoceti. The original description of Llanocetus denticrenatus by Ed Mitchell (1989) includes a maxillary fragment, mandible fragment, and an endocast - overall, marginally crappy. Later on, Ewan Fordyce revisted the site and collected what he initially thought was an archaeocete, and it even included (apparently) vestigial hindlimb elements (plural), similar to the condition in basilosaurid archaeocetes (which are not too phylogenetically divorced from Llanocetus, after all). This turned out not only to be a toothed mysticete, but the remainder of the holotype skeleton. My guess is that whoever originally collected the holotype scraps was freezing their ass off and said "to hell with it" and left. However, even though a cast of the skull is now on display at the USNM, the rest of the holotype is not yet described, and the dotted outline provided by Fitzgerald (2010) is the most informative figure ever published of this rather interesting beast. Anyway, I'll be pretty excited whenever the description gets published (much of the above information was presented by Fitzgerald, 2010, in his discussion of taxa used for the cladistic analysis).

The next post will (hopefully) be less-rambling, and will detail the transition from teeth to baleen in archaic mysticetes.

References:

Fitzgerald, E.M.G. 2006. A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales. Proceedings of the Royal Society B: Biological Sciences
273: 2955–2963.

Fitzgerald, E.M.G. 2010. The morphology and systematics of Mammalodon colliveri (Cetacea:Mysticeti), a toothed mysticete from the Oligocene of Australia. Zoological Journal of the Linnean Society. 110p.

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.

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.

Puijila, a very basal 'pinnipedimorph'

Its been a very busy week for me, and since I finished my proposal tonight, I thought I'd spend some time on a long-ish post. Its been an exciting day. Aside from the obvious (i.e. the topic of this post), today saw the release of the most epic PALAIOS issue ever:

Peters et al. 2009. Sequence stratigraphic control on preservation of Late Eocene whales and other vertebrates at Wadi Al-Hitan, Egypt. PALAIOS 24:290-302.
Ehret et al. 2009. Caught in the act: trophic interactions between a 4-million-year-old white shark (Carcharodon) and a mysticete whale from Peru. PALAIOS 24:329-333.
Nielsen, 2009. Pliocene balanuliths from Northern Chile: The first report of fossil balanuliths. PALAIOS 24:334-335.

The first of these is basically 100% relevant to my master's thesis; the second wasn't too exciting, and the third - well, I'm keeping that on the D-L for now.

Without further adeu, I am very pleased to present Puijila darwini, a very early 'pinniped'. I was extremely excited to read this paper, as was my colleague Morgan Churchill, whose enthusiasm was much shared via facebook. The two of us are some of the only paleontology students in the U.S. studying fossil pinnipeds (ironically both from landlocked states; the last sea in this area was the Cretaceous-Paleocene Cannonball Seaway).

As you can see, this is a pretty cute little critter. It has short-ish fore- and hind-limbs, a complete arctoid dentition (i.e. the postcanine dentition is not simplified as in later-diverging pinnipeds), a wide otter-like skull, large infraorbital foramina, robust forelimb bones (the humerus in particular) which have large muscle attachment areas, flattened phalanges, and an elongate tail.

Before I delve further, a little taxonomy/phylogeny. Pinnipedia (as you surely know) includes the modern walrus, sea lions, fur seals, and true seals. Following the phylogeny of Berta and Wyss (1994), most modern and fossil 'pinnipeds' comprise the clade Pinnipedia. The Pinnipediformes is a slightly more inclusive clade that includes the basal taxon Pteronarctos. The Pinnipedimorpha is an even more inclusive clade that includes the Pinnipediformes + Enaliarctos. Recently, Wang et al. (2005) included the basal (semiaquatic at the very most) arctoid Amphicticeps within the pinnipedia - obviously a much more inclusive use of the clade than Berta and Wyss.

The oldest known pinnipedimorphs are Enaliarctos tedfordi and Enaliarctos barnesi from the Oligocene (Chattian, 29-23 Ma) Yaquina Formation of Oregon (Demere et al., 2003). These appear several MYA before Puijila, already fully marine, and with significantly more marine/aquatic adaptations (larger infraorbital foramina, more enlarged forelimb bones, shorter hindlimbs, clearer progression toward homodonty, reduced tail, enlarged 1st metacarpal and 1st and 5th metatarsals, etc.). Because of this, Rybcyznksi et al. (2009) regard Puijila as a relict taxon.

Two very intriguing implications of this study arise from the location and geologic context of this critter. For starters, this fossil is from Nunavut - specifically, Devon Island, well above the arctic circle. The authors state that this may indicate an arctic ocean origin for pinnipeds. This is fine, except for Enaliarctos occurring in the North Pacific in a far more advanced 'form' several million years before. Demere et al. (2003) predicted the center of origin for pinnipedimorphs to be the North Pacific. It is certainly possible that this is perhaps a function of collecting bias, and that other Oligocene marine units worldwide need to be prospected and more greatly scrutinized (i.e. New Zealand, Australia, Argentina, India (?), and Japan). In any event, the Demere et al. hypothesis is certainly still possible, and likely more parsimonious as 1) the later occurrence of Puijila in the arctic may be a function of dispersal from the North Pacific and 2) there are other similar taxa (i.e. Potamotherium, Amphicticeps) from Europe and central Asia.

The second implication is that Puijila is from lacustrine deposits, and thus was likely semiaquatic. The pre-Enaliarctos pinniped record was effectively nonexistent, and gave no hint at the transition from land-to-sea. The cetacean and sirenian fossil records, however, have a clear transition from 'amphibious' taxa (Pakicetus), semiaquatic taxa inhabiting freshwater (i.e. the "crocowolf" Ambulocetus), semiaquatic marine taxa (protocetids such as Maiacetus and Georgiacetus) and fully (permanently) marine taxa (basilosaurids such as Basilosaurus and Dorudon). However, Enaliarctos is clearly marine in terms of its adaptations and associated depositional environment. In the case of Puijila, however, the associated sediments are lacustrine, and the adaptations are very 'otterlike'.

Additionally, the phylogenetic position of Potamotherium as a pinniped in this analysis is very interesting, as this taxon has traditionally been interpreted as some kind of musteloid, and in the past used as evidence for a true seal-mustelid link (which is a load of B.S., and I'll post about that in the future). Short version: I really, really liked this paper. I first heard about this critter at SVP, although someone told me instead that it was a very early otariid (fur seal/sea lion).

Addendum: I forgot to mention this in my original post, but Tedford et al. (1994) conducted a phylogenetic analysis of the arctoidea when they described new material of the 'beach bear' Kolponomos (a topic for a post of its own, because it is far weirder than Puijila could ever hope to be). Kolponomos is an ursid-like critter, with forward pointing eyes, and very wide/large sea otter-like teeth presumably for crushing mollusks, and postulated to inhabit the intertidal zone. It is known thus far only from shallow marine rocks. Kolponomos is from the late Oligocene and early Miocene of the Olympic Peninsula, and I know at least from the Clallam Formation. In any event, at the time Kolponomos plotted out as the sister taxon to pinnipedia, another intriguing hypothesis. I think future analyses, especially ones investigating pinniped ancestry within the arctoidea, should also include Kolponomos. If Kolponomos is in this group of pinniped-like arctoids as well, it would certainly paint a more convoluted picture (i.e. both freshwater semiaquatic and coastal semiaquatic 'proto-pinnipeds'. Anyway, I really need to get to campus to print off Wang et al. (2005), do some touch ups on my master's proposal, and finish my presentation on Purisima Formation odontoceti.