Ankylorhiza tiedemani, a giant dolphin from the Oligocene of South Carolina, part 2: the ecology, evolution, and swimming adaptations of Ankylorhiza

Don't forget to check out Part 1 here.

Disclaimer: this post includes a lot of irreducible terminology, particularly when it comes to the phylogenetic section – there simply are no useful or meaningful simple synonyms of words like “paraphyletic”. I’ll try to sketch these out, but especially for the phylogenetic terms, I suggest consulting the UCMP online phylogenetics glossary https://ucmp.berkeley.edu/glossary/gloss1phylo.html

Life restoration of Ankylorhiza tiedemani, artwork by yours truly! 

The skull and teeth Ankylorhiza – a killer dolphin?

At first glance, the skull of Ankylorhiza tiedemani bears some gross similarities with Squalodon: it has a somewhat elongate rostrum, procumbent incisors, some triangular posterior cheek teeth (probably molars and/or premolars), large temporal fossae, and long zygomatic processes. But on closer inspection, the similarities seem to end. Ankylorhiza has a more derived dentition than Squalodon: most of the teeth are single rooted and none appear to be completely double rooted: the posteriormost cheek teeth are bilobate or have incompletely split root lobes (the posteriormost teeth are typically the last to become single rooted, both in cetaceans and in pinnipeds), whereas multiple teeth are double rooted in Squalodon. Ankylorhiza tiedemani also generally lacks large accessory cusps, and a couple minute bumps are present on the cutting edges of the last two teeth – and that’s it; in Squalodon, about half the dentition has accessory cusps like a basilosaurid whale. Squalodon, like most crown Odontoceti (modern odontocetes), has a narrow rostrum base and a wide vertex (top of the braincase); in Ankylorhiza, the base of the rostrum is wide, and the vertex is quite narrow – both are features shared with other early odontocetes like Agorophius and the xenorophids, as well as archaeocete whales. Ankylorhiza tiedemani also has quite a bit of parietal exposed at the vertex of the skull: in crown odontocetes, the parietal is completely hidden by the bones of the facial region migrating backwards with the blowhole towards the top of the skull. And that brings us perhaps to one of the most critical differences: the bony naris in Ankylorhiza is very far forward, in front of the orbits and out on the base of the rostrum – approximately the same location as in some xenorophids, and yet posterior to the position in admittedly more plesiomorphic odontocetes like Simocetus and Ashleycetus where it is far out on the rostrum.*

The early evolution of telescoping in odontocetes - maxilla in gray, showing the overriding of the frontal, from Geisler et al. 2014. Ankylorhiza is at a near-identical stage of telescoping as Patriocetus, the third skull from the right.

 *Interestingly, the position of the blowhole does not correspond 1:1 with the phylogenetic placement of xenorophids, Ankylorhiza, and simocetid-grade dolphins: in xenorophids, the blowhole is slightly posterior to the base of the rostrum, despite being the earliest lineage of these three on the cladogram; in the next diverging lineages, the simocetid-grade dolphins, it is far out on the rostrum, and in Ankylorhiza and other “agorophiid” grade dolphins, it is just in front of the orbits. This shouldn’t be terribly surprising as these lineages all more or less appear in the fossil record at the same time and all are contemporaneous, so none are directly ancestral to one another. Instead, these Oligocene odontocetes seem to represent the spokes of a wheel frozen in time just after an explosive radiation of early odontocetes some 35 million years ago – most of which would go extinct, with a few surviving ‘experiments’ and a lot of dead ends. This is also the best explanation for the seemingly haphazard distribution of dental features (e.g. as discussed for Ankylorhiza v. Squalodon above).

So, what was Ankylorhiza eating? Its teeth are relatively large, and bear sharp cutting edges unlike modern dolphin teeth. Further differing, but shared with many extinct marine tetrapod lineages – like the giant pliosaurids, for example – are longitudinal ridges on the enamel (I’ve referred to this in the paper as ‘fluted’ enamel). A recent paper by McCurry et al. (2019) found that these ridges do not seem to correspond to internal tooth structure, enamel thickness, etc. and therefore are likely to be related to the efficiency of puncturing rather than distribution of force/pressure during biting (as has been demonstrated with rugose enamel, for example). The McCurry paper is thought provoking and surprising, indicating that by whatever means, the external shape is important for aquatic feeding regardless of how the tooth is “built” and has re-evolved many times among aquatic tetrapods. It does, however, need to be evaluated in the context of enamel micro/ultrastructure, which to my knowledge has not yet been attempted but would shed considerable light on this topic.

The teeth of CCNHM 103, the best preserved specimen of Ankylorhiza tiedemani. A-B are the upper teeth, C-D are the lower teeth; while the lower dentition is not complete, most positions are preserved. The lower teeth highlight the thick cementum the best: contrast rc1? with rpc4: in the former, the cementum has spalled off from the dentine, and in rpc4, the thickness of the cementum is visible relative to the much thinner dentine 'core' on its own. The cementum is the light tan/buff colored tissue.

Ankylorhiza has two more interesting dental quirks. The first, and most readily interpreted, is that it has thickened cementum on the tooth roots. Cementum is one of the three major dental tissues, along with enamel and dentine – and is the only tissue that can grow externally on the tooth after tooth eruption. Enamel is only developed in the “crypt” and after eruption, dentine is deposited but from the outside in. Cementum, on the other hand, binds the root of the tooth to the bone of the jaw and can be deposited continuously throughout a mammal’s lifespan. In some cetaceans, cementum can be unusually thick – in some sperm whales, half of the radius of a tooth might be cementum. Larger odontocetes tend to have thicker cementum also. There is some experimental evidence that cementum can help teeth in modern mammals sustain higher point loads without fracturing, and thickened cementum in extinct sperm whales has recently been interpreted as improving bite force capabilities and tooth survivability against fractures, which makes sense given that many extinct big-toothed sperm whales were likely macrophagous killer sperm whales (e.g. Zygophyseter, Acrophyseter, Albicetus, Brygmophyseter, Livyatan, etc.). In Ankylorhiza, we similarly interpreted thickened enamel as a sperm-whale like adaptation for increased bite force. Another consideration, however, is body size: it’s also possible that owing to how physiologically expensive it is to produce larger teeth, that tooth size may lag behind skull size, and as the alveoli become larger in later postnatal growth, cementum is used to fill in the gap. This is a concern Brian and I both independently had – a line of investigation for someone else in the future!

Two of the procumbent lower incisors of CCNHM 220, our specimen of Ankylorhiza tiedemani from the lower Oligocene Ashley Formation. In CCNHM 103, the crown is worn down to the gumline - which we interpret as the result of dental ramming.

The last dental feature are the procumbent incisors: this is certainly not unique to Ankylorhiza, as procumbent tusk-like incisors are also present in Squalodon and Phoberodon, and waipatiids, most clearly in Otekaikea huata – though similar teeth are also preserved in the two species of Waipatia. Functional hypotheses for these apical tusks in Squalodon, Phoberodon, and waipatiids have not been proposed in any published article. We noted that the anterior incisors of Ankylorhiza are quite heavily worn in CCNHM 103, and the lower first incisor is worn down to the gumline, with a possible wear facet corresponding to the upper first incisor, which is not completely procumbent – but curves anteroventrally. It’s also possible that this is coincidental and that these teeth did not contact at all, given the shape of the upper jaw. Regardless, extreme wear – the most extreme in the entire dentition – suggests extreme use. We propose that the tusks in Ankylorhiza could have received this extreme wear from being used by ramming prey – this could be an effective way to kill large prey, and is a method that modern delphinids use to dispatch prey (or, in the case of bottlenose dolphins, to commit “porpicide”, seemingly for fun).

A dorsolateral view of the skull of CCNHM 103, showing the enormous temporal fossa for the temporalis muscles. This must have afforded Ankylorhiza a punishing bite force.

In addition to these dental features, the temporal fossae are enormous – each left and right is individually much larger than the endocranial volume for the brain, so perhaps ½ or more of the internal volume of the braincase end of the head is completely occupied by temporalis and masseter muscles to close the jaws. These muscles are quite a bit reduced relative to the condition in basilosaurid whales, of course – but are significantly larger in comparison to xenorophid dolphins and crown odontocetes, indicating that their large size is associated with adaptation to macrophagy in Ankylorhiza. Even further evidence comes from the range of motion at the cranio-vertebral joint: if you take the atlas vertebra (missing in CCNHM 103, but I borrowed one from a different specimen) and moved it to the approximate limits of cranial flexion (dorsal movement of the skull) and extension (ventral movement), the range of movement is nearly identical to that of Orcinus and Pseudorca – which seems correlated with grip and tear feeding, where these large delphinids rip their prey (that is too large to swallow whole) into manageable sized portions by shaking the prey back and forth. Neither modern delphinid has sharp cutting edges or serrations, so this may have been somewhat more efficient in Ankylorhiza.

Altogether, available evidence indicates that Ankylorhiza tiedemani was a macrophagous “killer dolphin” – the first odontocete to evolve into this niche, and the first truly large odontocete to evolve. Ankylorhiza is known from the Ashley Formation, and therefore evolved within only about 4-5 million years of the oldest known odontocetes (Simocetus rayi, ~33 Ma). However, as detailed elsewhere on this blog, odontocetes probably evolved as early as the late Eocene, and there’s probably an additional 5 million years of missing fossil record unaccounted for by fossils permitting the divergence of agorophiid-grade dolphins from basilosaurids. This niche did not disappear of course – it was refilled by Squalodon in the early Miocene – as well as by the macrophagous Scaldicetus-grade sperm whales (Acrophyseter, Brygmophyseter, Livyatan, Zygophyseter) in the middle and late Miocene. These whales at some point died out in the latest Miocene or Pliocene, and this niche was not refilled until some time in the Pleistocene by the modern killer whale.

The skull, vertebrae, and forelimb of Ankylorhiza tiedemani. From Boessenecker et al. 2020.

Ankylorhiza and the evolution of swimming in Neoceti

The feeding ecology is actually not the main thrust of the paper – the main point of the paper is the implication for locomotion and the evolution of swimming. I won’t talk too much about archaeocetes here – there is not too much of a consensus on the swimming style of legged archaeocetes – but to review the situation in basilosaurids, the earliest whales committed to a pelagic lifestyle – there are rectangular vertebrae at the tip of the tail indicating the presence of a caudal fluke, and the tiny vestigial hindlimbs could not have served any role in locomotion. The flippers still have a moveable elbow joint, and the finger bones are elongated and spindly. The scapula is dramatically broader than earlier archaeocetes, generally resembling modern cetaceans. The humerus is very long (longer than the radius/ulna) and little modified from terrestrial mammals – with a long deltopectoral crest. The vertebrae have very smooth changes in proportions, meaning that they are not ‘regionalized’ like in many modern odontocetes. Basilosaurids also have a high vertebral count, with somewhat serpentine bodies – and long thoraces, with large numbers of thoracic vertebrae and ribs. In modern cetaceans, there is a tendency for a reduction in thoracic number and an increase in the number of caudal vertebrae.

Functional anatomy of the postcranial skeleton of Ankylorhiza tiedemani. The top shows the proportions of vertebral centra (bodies) of this skeleton - length, width, and height - and a lot can be inferred from these diagrams, pioneered by coauthor Emily Buchholtz, which I have lovingly nicknamed "Buchholtz diagrams". This plot more or less shows that Ankylorhiza was a better swimmer than a basilosaurid, mysticete, or modern sperm whale, with some vertebral adaptations in parallel with belugas and beaked whales. The second and third are PCA plots, analyzed by Morgan Churchill, which are sort of a "kitchen sink" approach to analyzing measurements of bones. The vertebral plot shows that Ankylorhiza plots with modern odontocetes, close to sperm whales, but slightly closer to archaeocetes. The forelimb plot shows Ankylorhiza clustering with archaeocetes and beaked whales rather than members of the Delphinida. From Boessenecker et al. 2020.

We approached the analysis of postcranial evolution in two ways: we conducted principal components analyses (PCA) of forelimb and vertebral measurements, and also conducted an ancestral character state reconstruction. The PCA is a type of statistical analysis and basically seeks to identify what measurements explain most of the variation in shape within a particular dataset. In this case, we got very different results for the flipper and vertebral column. The vertebral anatomy was similar to modern odontocetes – slightly closer to archaeocete whales, but clustering with odontocetes. The flipper anatomy on the other hand, clustered with basilosaurid whales (and to a lesser extent, the Amazon river dolphin and beaked whales) to the exclusion of most modern odontocetes. Ancestral character state reconstruction takes a single character from a cladistic analysis – for example, if the transverse processes of the lumbar (lower back) vertebrae point sideways or downwards a little bit – and reconstructs where changes probably occurred from one condition to another on a cladistic tree. It’s generally a good idea to exclude these characters from the analysis producing the tree, so that the tree itself is not influenced by the character in question (basically avoiding circular reasoning). We found that over a half dozen anatomical features present in modern cetaceans must have evolved twice – once in baleen whales, and once in echolocating whales. Some of these features that Ankylorhiza, stem odontocetes, and stem mysticetes share with basilosaurids include ventrally deflected transverse processes of the lumbar vertebrae, a long humerus with a long deltopectoral crest (owing to similarly long humerus being present in toothed mysticetes [Mystacodon, Fucaia] and eomysticetids [Eomysticetus, Yamatocetus, Waharoa, Toharahia]), a wide caudal peduncle. The wide caudal peduncle is recorded by equidimensional – rather than narrow – mid-caudal vertebrae. This is an adaptation for efficient up/down movement of the tail – all of the propulsive force is in the flukes, at the end of the tail (a long lever arm) and minimal effort is wasted on moving the tail stock: it slices vertically through the water. Such a peduncle evolved independently in many fish (tuna/mackerel) and many sharks, but the peduncle is instead horizontal given the side to side movement.

Convergent evolution of mysticetes and odontocetes, as reconstructed by our Ancestral Character State Reconstruction (ACSR), with diagrams showing the different flipper skeletons at top. From Boessenecker et al. 2020.

What could have driven such extensive convergence in the postcranial skeleton of odontocetes and mysticetes? This situation does seem a bit different than in pinnipeds, which have remarkably different postcranial features and locomotion. We hypothesize that two major evolutionary “ratchets” appeared in cetaceans: the first was a trade of hindlimbs for tail flukes, highlighted by the evolutionary transformation of protocetids and basilosaurids, and the second was the ‘locking’ of the elbow in the cetacean flipper. With these two adaptations, best interpreted as key innovations in cetacean evolution, there was no going back to any form of quadrupedal paddling, and cetaceans were stuck with fluke-powered swimming. The locking of the elbow meant that, for the most part, the foreflippers would be reduced to hydrofoils for steering rather than being used to generate thrust (like a sea lion or penguin). We think the latter of these features caused a cascade of convergences later on within Neoceti.

Prior to this analysis, these features were assumed – and quite reasonably so – to have evolved in the common ancestor of mysticetes and odontocetes. There’s an interesting ‘perfect storm’ of coincidences that took place to make this sort of knowledge gap and discovery possible:

1)      1) Because the postcranial skeleton of baleen whales and odontocetes share more in common with eachother than either does with archaeocetes, researchers who work on early Neoceti have tended to be “headhunters”.

2)      2) Archaeocete researchers have historically sort of ignored cranial anatomy and spent much more effort on postcranial anatomy. Archaeocete researchers typically (with some minor exceptions) have not worked on Neoceti, and vice versa* – reinforcing point 1 above.

3)      3) Few fossils of early Neoceti, up until now, included either well-preserved forelimbs or vertebral columns, reinforcing point 1 above. Because the scattered remains of early Neoceti didn’t really give us a “transitional blueprint” to postcranial change, neocete specialists didn’t particularly recognize or appreciate differences between stem odontocete and modern odontocete skeletons. Nor did they look for them – reinforcing point 1 above.

no caption needed

*There are a few notable exceptions: Mark Uhen has worked on both groups, and the French/Belgian working group has studied both archaeocetes, odontocetes, and early mysticetes (Lambert, Muizon, Martinez-Caceres, et al.).

So, based on missing data, and descriptive/research practices informed by that missing data, there was a bit of circular reasoning taking place. This situation allowed for the unappreciated significance of Ankylorhiza being preserved with such a complete postcranial skeleton.

Our preferred tree topology - with various relevant clades outlined in color rectangles. From Boessenecker et al. 2020. Ankylorhiza is placed within the red box, a possible monophyletic Agorophiidae.

Who is Ankylorhiza related to?

Ankylorhiza tiedemani was originally placed in the genus Squalodon – but no longer is. Which, begs the question – what is Squalodon, anyway? The short answer is, nobody knows – no modern cladistic analysis has included multiple species of Squalodon, so we’re not quite sure if the genus is monophyletic. Nobody is certain if the family Squalodontidae is monophyletic, and if it is, what other genera belong within it. Many putative squalodontids, including Patriocetus, Phoberodon, Prosqualodon, Neosqualodon, and others – have all shown to be different lineages of stem odontocetes in cladistic analyses. At present, the best we can do, is define Squalodon as large-bodied odontocetes with mostly symmetrical skulls and large triangular molars with accessory 2-4 cusps and rugose enamel and a number of distinctive earbone features – and for the time being, restrict the family to the genus. Squalodon seems to be one of the later diverging stem odontocetes, just outside the crown group, but also appears occasionally within a more broadly defined Platanistoidea – as redefined by Christian de Muizon in the 1980s, including Platanista, squalodelphinids, extinct platanistids, and squalodontids. In recent years, this seems less tenable as the only analyses to recover this relationship do so only at the expense of removing undescribed species from Charleston Museum (originally coded in Geisler and Sanders, 2003) and shorter character lists. When more characters and taxa are included – squalodontids fall out into the stem group as a paraphyletic grade of dolphins between Ankylorhiza and the modern sperm whale, often intermingled with a similarly paraphyletic Waipatiidae (also recovered on some occasions as a clade within Platanistoidea, but frequently also smeared into a paraphyletic grade on the stem).

Comparison of Ankylorhiza with Squalodon, Phoberodon, and the "earthquakes squalodontid" - an Oligocene taxon from NZ that is similar to both Phoberodon and "Prosqualodon" hamiltoni from the early Miocene. From an old SVP talk of mine.

Ankylorhiza may be superficially similar to Squalodon, but shares much more in common with Agorophius pygmaeus and Patriocetus kazakhstanicus, including a wide base of the rostrum and a narrow intertemporal constriction. In our analyses, Ankylorhiza formed a clade with Agorophius (though, surprisingly, not the very similar Patriocetus) – and therefore, in the future, could be the basis for a redefined Agorophiidae. For the record, many whaleontologists wince when they hear the word Agorophiidae – historically it’s been an even bigger wastebasket than Squalodontidae: virtually all stem odontocetes aside from Squalodontid- and waipatiid-grade odontocetes (including the xenorophids!) were placed into a hilariously paraphyletic Agorophiidae.

Patriocetus kazakhstanicus, a very similar but smaller odontocete from the Oligocene of Kazakhstan (from Dubrovo and Sanders, 2000), which differs principally in having more archaic teeth with thinner cementum - large teeth of this morphology are known from Oligocene localities here in South Carolina, and at least one Patriocetus-like dolphin appears to have been the same size as Ankylorhiza but is known only from fragments.

Another surprising result of our analysis was the clustering of three purported squalodontids – Squalodon, Prosqualodon, and Phoberodon – into a clade! However, this was only in one of the two analyses with different weighting schemes. In this analysis, waipatiids “broke apart” and became paraphyletic. Interestingly, in the other analysis, the opposite happened: squalodontids fell apart and the waipatiids became monophyletic. This is likely because the two groups are remarkably similar in morphology and evolutionary grade and 1) may actually be the same clade after all, owing to frequent phylogenetic clustering and 2) in the past have mostly been separated based upon size and some features that may be related to size.

Future Directions

There’s two different suites of future studies I envision. The first are immediate questions to be answered about Ankylorhiza itself. There’s a second species of Ankylorhiza awaiting description! That should be fun to tackle. There are juvenile specimens that can tell us about the growth of Ankylorhiza. There are other specimens of both species that tell us a little bit more about the feeding behavior and ecology of Ankylorhiza – including specimens with serrated teeth, and mandibles. Paleohistology of Ankylorhiza would be a useful endeavor. FEM and reconstruction of the volume of the temporalis could tell us about the bite force capabilities of Ankylorhiza, as can microwear analyses. I am dying to know what the microwear of the incisor tusks looks like!

Other major directions are concerned with broader impacts of our work: is there evidence elsewhere that has been overlooked before? What about the postcranial skeleton of Mirocetus – the second most completely known stem odontocete (yet, arguably, one of the poorest understood). Other studies contrast with ours: Amandine Gillet’s recent paper looked at this differently and concluded that vertebral morphology is quite divergent within Neoceti. Why is this? Maybe each study emphasized different aspects of vertebral anatomy? A clear future direction for research is a renewed effort to find and describe Oligocene odontocete skeletons with postcrania: clearly, not identical to modern cetaceans. What the hell did the flipper of xenorophids look like? We still don’t have one of those. Does anyone else belong in the Agorophiidae? Are the Waipatiidae and Squalodontidae monophyletic or even separate clades? A major overhaul of squalodontid morphology and phylogeny is needed, though recent efforts to redescribe Phoberodon and Prosqualodon are nice initial contributions.

What drove Ankylorhiza to extinction? Within about 5 million years or so, the first macrophagous physeteroids appeared, re-filling the vacant niche. We don’t really have a good handle on what caused apparent turnover between the late Oligocene (e.g. Chandler Bridge Formation assemblage – dominated by “Agorophiidae”, “Waipatiidae”, and Xenorophidae) and the early Miocene (dominated by squalodontids, early platanistoids, and other longirostrine odontocetes – e.g. Belluno Sandstone of Italy).

Lastly, and this is a broad one - this should be a major call for paleocetologists to consider their biases in the study of fossil cetaceans. What parts of the skeletons are you focusing on, perhaps at the expense on other parts? I can tell you, it can be very aggravating as a neocete specialist trying to find anything out about the earbones or basicranium of basilosaurid or protocetid whales, let alone decipherable figures (the landmark monograph on Cynthiacetus peruvianus is a notable exception). Likewise, a neocete worker has a similarly difficult time finding much of anything out about the postcranial anatomy of even well-preserved odontocete and mysticete specimens (this is decidedly worse in the crown of each clade). Each group of researchers have their own set of historical biases, in the absence of which, these findings would have been announced decades ago. Lucky for me, I guess!

Regardless, this won’t be the last you hear of Ankylorhiza – so stay tuned!

Further Reading/References

Boessenecker et al. 2020: https://www.cell.com/current-biology/fulltext/S0960-9822(20)30828-9

Dubrovo and Sanders, 2000: https://www.tandfonline.com/doi/abs/10.1671/0272-4634(2000)020%5B0577%3AANSOPM%5D2.0.CO%3B2

Geisler et al., 2014. https://www.nature.com/articles/nature13086

Gillet et al. 2019: https://royalsocietypublishing.org/doi/full/10.1098/rspb.2019.1771

McCurry et al. 2019: https://academic.oup.com/biolinnean/article/127/2/245/5427318