Thursday, September 13, 2012

Bone-eating zombie worms, part 3: Osedax consume more than cetacean bones

Because Osedax were originally identified colonizing cetacean skeletons, they were originally interpreted as being whale-fall specialists. In order to test the hypothesis that Osedax are cetacean carcass specialists, Jones et al. (2008) experimentally deployed cow bones on the seafloor in Monterey Bay. They attached cow bones to a PVC “tree” on the seafloor, so that the bones would not be in contact with the sediment (with the chance of being covered in sediment. Within a year, the bones were colonized by Osedax. As cow skeletons are probably not typically delivered to the deep sea floor – although given the presence of rare land mammals and dinosaurs in marine fossil assemblages, it does happen, albeit rarely – it suggests that Osedax is not really a cetacean specialist, and can colonize the bones of other mammals. Jones et al. (2008) suggested that Osedax not only colonize the skeletons of baleen whales, but also bones of dolphins, porpoises, sea lions, and seals that reached the seafloor. They further suggested that future experiments should include other-non cetacean bones. One could make the observation that large, domesticated artiodactyls are not only closely related to cetaceans, but also have fatty bones; so perhaps it’s not surprising that cow bones make appropriate habitat for bone eating worms.

Modern cow bones implanted on a PVC "tree" on the seafloor, with closeup of Osedax worms emerging from the bone. From Jones et al. (2008).

This paper seemed to stir up some controversy, and generated a sharp response by Glover et al. (2008) who commented on several aspects of the study which may (or may not…) invalidate observations of cow bone colonization. They argue that Osedax probably qualifies as a whale-fall specialist, because whale skeletons comprise the majority of its “diet”. They indicated that no whale fall assemblages had been identified on naturally occurring terrestrial mammal carcasses in the deep sea. They also argued that the placement of cow bones on a metal tree above the seafloor does not represent a naturally occurring condition; they indicate that the small bones of land mammals would probably be buried too quickly to be colonized by Osedax. I’m not necessarily certain this is really evidence that Osedax wasn’t a generalist, but the inferred rarity of terrestrial vertebrate remains on the seafloor is probably reasonable to cite as evidence of Osedax being a whale fall specialist. Curiously, Glover et al. (2008) make the comment that actualistic taphonomy of large land mammals shows that they are unlikely to be transported far by rivers. This is perhaps amusing when one recalls how many fossils we have of land mammals and dinosaurs in marine rocks – examples from my neck of the woods include a skull of the dome-headed chalicothere Tylocephalonyx from the marine Astoria Formation of central Oregon, and the type skeleton of Aletopelta from the late Cretaceous of San Diego County (a.k.a. the “ankylosaur ass”, as affectionately referred to by some SDSU students). Furthermore – in one of Jack Horner’s first papers, he reviewed the dinosaur record from the late Cretaceous Bearpaw Shale of Montana, and found that numerically more nodosaurid skeletons were known at the time from marine rocks than from terrestrial rocks.

Vrijenhoek et al. (2008) responded to the complaints of Glover et al. (2008) and noted the age-old adage that ‘absence of evidence is not evidence of absence’, and is certainly an excellent point in this case: the lack of discoveries of terrestrial mammal ‘falls’ is probably not a good indication of their existence of not: Glover et al. argued that Osedax may not effectively colonize land mammal bones due to their small size, and it is important to note that the same argument can be flipped on its head – small bones are less likely to be discovered on the seafloor by ROV’s or submersibles. Contrary to the assertion of Glover et al. (2008) that land mammals do not frequently travel long distances in rivers (and thus float out into the sea), Vrijenhoek et al. (2008) report on a pelvis and several hind leg bones of a large mammalian herbivore off the coast of New Guinea at a depth of 1500 meters, discovered by submersible. These bones were also colonized by Osedax, interestingly. Not only does this indicate that Osedax will colonize “naturally” occurring land mammal bones, but also that such occurrences are ‘findable’. Vrijenhoek et al. (2008) report that rice was found on the seafloor around the bones, and they interpreted it as discarded waste from a passing ship; furthermore, the pelvis shows a distinct butcher’s sawmark, indicating it did not arrive naturally.

Partial hindlimbs of a terrestrial mammal found on the seafloor, complete with Osedax... and a pile of rice? This appears to represent waste chucked overboard a ship. From Vrijenhoek et al. (2008).

A beautifully sculpted model of the giant Japanese plotopterid, Copeteryx. Sculpted by Hirokazu Tokugawa (from Oligocene bones of a close relative from Washington state- Tonsala - have been found with trace fossils identifiable as Osedax.

In late 2010, Steffen Kiel and colleagues published another article on fossil Osedax borings – this time on early Oligocene bird bones from the Olympic Peninsula. These were bones of the extinct bird Tonsala hildegardae – a flightless, penguin-like plotopterid bird. Plotopterids such as Tonsala, Copteryx, Hokkaidornis, and Plotopterum are gigantic birds that went extinct during the Miocene; they are known from Japan, California, Oregon, Washington, and British Columbia. These giant birds were up to 2 meters in height, and represent the Northern Pacific analogs of giant Paleogene penguins (e.g. Kairuku, Icadyptes, Platydyptes). Bones of Tonsala were found to have numerous small Osedax pinholes, in addition to typical Osedax borings when CT-data were examined. To recap from part 2, these boreholes are where the Osedax stalks and gills extend out from the bone; below, the borings are confluent with bioeroded galleries roofed over by thin walls of outer (cortical) bone left. Not only does this further indicate that Osedax has naturally colonized non-cetaceans through the course of geologic time, but also that Osedax would have had a suitable source of bones prior to the Eocene evolution of cetaceans. This further suggests that a Cretaceous rather than Eocene divergence date of modern Osedax species (these are the two hypothesized divergence dates in the literature, depending upon which calibration is used).

Plotopterid bone with characteristic Osedax "pinholes". Early Oligocene of Olympic Peninsula, Washington State. From Kiel et al. (2011).

 Fossil record of large marine birds during the latest Cretaceous and Paleogene; these birds may have bridged the gap for Osedax between the extinction of large marine reptiles and the emergence of large, oceangoing cetaceans in the middle Eocene. From Kiel et al. (2011).

The next year, Rouse et al. (2011) published a short paper on another experiment in order to further test the whale-specialist hypothesis. Rouse et al. experimentally deployed large fish bones in small wire cages, and observed Osedax colonization after only 5 months. This is far more surprising than cow bones, as fish bones have avascular histology (i.e. dense bone without pore space), which is perhaps as far from the lipid-rich, osteoporotic bones of cetaceans that you can get among vertebrates. This not only lends support to the idea that Osedax may naturally colonize non-cetaceans, but also that non-cetacean bones (such as those from birds and bony fish) would have sustained Osedax during the Paleocene and early Eocene, after marine reptiles went extinct but before large oceangoing cetaceans evolved.

Fish bones experimentally deployed on the seafloor, and hosting Osedax worms, indicating they have a much taxonomically wider palette of bony substrates for colonization and consumption. From Rouse et al. (2011).

All in all, it appears as though modern Osedax probably does occur most commonly on whale skeletons rather than other vertebrates, but that it has colonized the remains of other vertebrate groups through time. Unfortunately, our fossil record of Osedax boreholes is restricted to a handful of bones from the Oligocene and Pliocene; the real test of Osedax evolution will be in the Eocene and Late Cretaceous. On one hand, I somewhat doubt that we will find Cretaceous Osedax borings, if they have not been identified as of yet. On the other hand – the fact that Osedax borings are so small, and have only been in the collective conscience of marine vertebrate paleontologists for only a year or two, they may legitimately be unidentified in currently established fossil collections of late Cretaceous marine reptiles. If we don’t find late Cretaceous Osedax, it might be reasonable to hypothesize that they arose with Eocene cetaceans, as proposed by some biologists.
Glover, A. G., Kemp, K. M., Smith, C. R.; Dahlgren, T. G. 2008 On the role of bone-eating worms in the degradation of marine vertebrate remains. Proc. R. Soc. B.  275:1959–1961.

Jones, W. J., Johnson, S. B., Rouse, G. W. & Vrijenhoek, R. C. 2008 Marine worms (genus Osedax) colonize cow bones. Proc. R. Soc. B 275, 387–391.

Kiel, S., Kahl, W. A. & Goedert, J. L. 2010 Osedax borings in fossil marine bird bones. Naturwissenschaften 55:51–55.

Rouse, G.W., Goffredi, S.K., Johnson, S.B., and R.C. Vrijenhoek. 2011. Not whale-fall specialists, Osedax worms also consume fishbones. Biology Letters 7:736-739.

Vrijenhoek, R.C., P. Collins, and C. Van Dover. 2011. Bone-eating marine worms: habitat specialists or generalists? Proceedings of the Royal Society B. 275:1963-1964.

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