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 a-fragi.blogspot.com). 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.

Don't forget to see the rest of the series:

Bone-eating zombie worms, part 4: more on bird bones, and Osedax colonizes whale teeth

Bone-eating zombie worms, part 2: the discovery of fossil Osedax traces

Bone-eating zombie worms, part 1: whale falls and taphonomy


References:

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.

Bone-eating zombie worms, part 2: the discovery of fossil Osedax traces

 

A schematic showing a 3d model of an Osedax bone boring. (Source: University of Leeds)

After taking a taphonomy course during my undergraduate program – roughly a year after Osedax was discovered – I had come across several references to bone eating worms. But because only a few papers had been published on fossil whale falls, and whale falls appear to be relatively rare in the fossil record, I didn’t really seriously expect traces of Osedax worms to be found in fossils. Surprisingly, I only had to wait five years. In 2010, a number of papers were published regarding possible Osedax traces – and what modern Osedax borings look like.

To start with – the first fossil record of whale falls was reported not very long after the first modern whale falls were reported. Squires et al. (1991) reported on Oligocene cetaceans  preserved with chemautotrophic mollusks, which were closely related to mollusks already known from cold seeps. Subsequently, a number of other fossil whale fall assemblages were reported (Goedert et al., 1995; Amano and Little, 2005; Pyenson and Haasl, 2007).

In February 2010, some borings were reported from Miocene baleen whale bones from Spain; they were cylindrical, up to 5cm deep and 1-3mm across, with numerous teardrop-shaped lobes internally. These were interpreted by the authors to represent Osedax worm borings (Muniz et al., 2010). Furthermore, the authors were able to name a new ichnospecies – trace fossils are given Linnean binomial names in ichnotaxonomy, a parataxonomic system. They named the trace fossil Trypanites ionasi; other ichnospecies of Trypanites are borings in hard substrates.

 

Traces of Trypanites ionasi, from the Miocene of Spain. From Muniz et al. 2010.

 

Reconstruction of Osedax happily producing Trypanites ionasi traces in bone. From Muniz et al. 2010.

A few months later, in April – Steffen Kiel, Jim Goedert, and colleagues reported on possible Osedax traces in Oligocene cetacean bones from the Olympic Peninsula. More importantly, they also reported on what exactly modern Osedax borings actually look like – data which had not yet been published in the whale fall literature yet. The borings that Kiel et al. (2010) reported on from modern and fossil whale bones had tiny boreholes in the cortical bone surface, and the cortical bone was bioeroded into large coalesced galleries underneath the exterior bone surface. Where the borings coalesced, only the outermost layer of bone was left as a thin veneer. In life, the stalks exit the bone through the tiny boreholes, and the “roots” occupy the bioeroded galleries. The modern and fossil traces were analyzed by CT scans, used to construct 3d models of the borings.

 

Bona fide fossil Osedax traces in Oligocene whale bones from Washington State, from Kiel et al. (2010); compare these with those from Muniz et al. (2010), above.

Oddly enough, these borings don’t really resemble those reported by Muniz et al. (2010) – at all. It is certainly feasible that those reported by Muniz et al. are some other species of Osedax, and we only have a few examples of published modern Osedax traces. However, the fact that Oligocene and modern traces are nearly identical suggests that there is some degree of conservatism in boring shape. So, who really knows what made the traces in the Spanish whale bones. It’s understandable, as the authors of that study didn’t report on what modern Osedax traces look like – a necessary stepping stone for interpreting fossil remains. As an aside, one of the authors of that study – Raul Esperante – is a well known young-earth creationist from Loma Linda Univerisity in southern California who has published a series of articles on whale taphonomy.

 

Finally, examples of Osedax traces from a modern bone: from Higgs et al. (2010).

 

More examples of modern Osedax traces, from Higgs et al. (2011).

More work on modern Osedax traces was published by Higgs et al. (2010). They also used CT scans to construct 3d models of the borings, and reported borings that were roughly similar to that reported by Kiel et al. (2010). Higgs et al. (2010) further found that the borings were mostly restricted to dense cortical bone, generally avoiding lipid-rich cancellous zones. Apparently some isotopic evidence suggests that Osedax synthesizes collagen rather than lipids, although other studies have documented Osedax in Japanese waters that subsist on blubber and spermaceti (Higgs et al. 2010 – references therein).

 

The (awesome) t-shirt Nick Higgs wore to SVP in 2009. The few marine vertebrate taphonomists at SVP - myself included - found this guy pretty damn quick. 

I met Nick Higgs at the 2009 SVP meeting in Bristol, UK – I was chatting with my friend and colleague Laura Vietti (Macalester College/University of Michigan), who is also focused on marine vertebrate taphonomy – and this British guy about our age came up to us, literally wearing a T-shirt he had made which said “bone eating worms” with a picture of Osedax infested whale bone on the back, and text saying “Lets talk: whale taphonomy!” Needless to say, he found Laura and myself really darn quick. Nick has subsequently invited us both to co-write a review paper on marine vertebrate taphonomy, which is an exciting opportunity to say the least.

 

 A beaked whale radius from the Pliocene of Tuscany, Italy, with numerous Osedax traces and pockmarks. From Higgs et al. (2011).

 Osspecus tuscia traces from the Pliocene beaked whale bone. From Higgs et al. (2011).

 

More recently, Nick Higgs and colleagues (2011) published another paper on early Pliocene Osedax borings in a beaked whale radius from Italy. This fossil exhibited a number of different types of borings, which were interpreted as different stages of borings. Some borings in CT-scans were well defined, with small apertures as in Kiel et al. (2010) and Higgs et al. (2010). Other pits had a small bit of bone caved in around the aperture (collapsed stage), while other pits retained no overhanging bone (open-pit stage); the last type has been eroded to the point where it looks like a crater (pockmark stage). Some pits had coalesced, forming combined pits. Higgs et al. (2011) also named a new ichnotaxon for these Osedax borings: Osspecus tuscia.

 

Two modern cetacean bones bored by Osedax. What's the significance of this figure from Higgs et al. (2011)? Stick around for part 4.

Although borings of Osedax have now been documented from the fossil record, what exactly does it mean for taphonomy? And what does it mean about the evolution and earliest record of Osedax? Tune in for parts 3 and 4.

Don't forget to check out the rest of the series:
  
Bone-eating zombie worms, part 4: more on bird bones, and Osedax colonizes whale teeth


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

Bone-eating zombie worms, part 1: whale falls and taphonomy

References:

Amano, K., C.T.S. Little. 2005. Miocene whale-fall community from Hokkaido, northern Japan. Palaeogeography, Palaeoclimatology, Palaeoecology 215:345-356.

Goedert, J.L., Squires, R.L., Barnes, L.G., 1995. Paleoecology of whale-fall habitats from deep-water Oligocene rocks, Olympic Peninsula, Washington state. Palaeogeography, Palaeoclimatology, Palaeoecology 118: 151– 158.

Higgs, N. D., A. G. Glover, T. G. Dahlgren, and C. T. S. Little. 2010. Using computed tomography to document borings by Osedax mucofloris in whale bone. Cahiers de Biologie Marine 51:401-405.

Higgs, N.D., C.T.S. Little, A.G. Glover, T.G. Dahlgren, C. R. Smith, and S. Dominici. 2011. Evidence of Osedax worm borings in Pliocene (~3 Ma) whale bone from the Mediterranean. Historical Biology 24:269-277.

Kiel, S., J. L. Goedert, W. Kahl, and G. W. Rouse. 2010. Fossil traces of the bone-eating worm Osedax in early Oligocene whale bones. Proceedings of the National Academy of
Sciences 107:8656-8659.

Muniz, F., J. M. d. Gibert, and R. Esperante. 2010. First trace-fossil evidence of bone eating worms in whale carcasses. Palaios 25:269-273.

Pyenson, N.D., D.M. Haasl 2007. Miocene whale-fall from California demonstrates that cetacean size did not determine the evolution of modern whale-fall communities. Biology Letters 3:709-711.

Squires, R.L., Goedert, J.L., and Barnes, L.G. 1991. Whale carcasses. Nature 349:574.

Bone-eating zombie worms, part 1: whale falls and taphonomy

 

 

How do we interpret the preservation of fossil marine vertebrates, like this Dorudon atrox skeleton from the Eocene of Egypt? (From Peters et al., 2011)

Unless you've lived in a cave for the last two decades or hate science and the oceans (or all of the above), you've probably heard about whale falls. Whale falls are one of the more fascinating aspects of modern marine biologic research. They were only discovered relatively recently (late 1990's) and research conducted by submersible and ROV has uncovered an amazing fauna that quickly develops around sunken whale carcasses. Biomass is present in relatively small amounts on the seafloor, and much of the food for critters on the abyssal plain rains down from the more densely populated upper part of the water column. When whales die – and sink – most of the time their carcasses will sink down to the seafloor. But whales aren't very common, and although whales die every day – the introduction of a whale carcass to the seafloor, from the vantage point of a seafloor organism – is not an everyday affair. Seafloor ecology is mediated by the introduction of food, and whale carcasses represent the most locally concentrated pulse of food in the deep sea.

 

Whale vertebrae and a hagfish at a whale fall. From www.mbari.org

As a paleontologist, much of the hullabaloo about whale falls is only of cursory interest; many of the ecological details – species diversity at whale falls, similarity to vent and cold seep fauna, interactions between invertebrates – are not really of much practical interest to a vertebrate paleontologist like myself. Certainly these other issues are totally fascinating – but I'm really only going to talk on here about the stuff that interests me as a paleontologist, as you can easily get the perspective of a biologist or ecologist elsewhere on the web.

 

 Photograph of a whale fall hosting a large number of bone-eating worms (Osedax).

So why am I so interested in whale falls? Whale fall research has generated some seriously intriguing information regarding the taphonomy of marine mammals (cetaceans in particular; see Allison et al., 1991). Admittedly, not all vertebrate paleontologists (marine mammal researchers included) are not terribly interested in taphonomy. Taphonomy is the science of fossil preservation, and is often summed up as attempting to discover everything that happened to a fossil from "death until burial" (and sometimes, after burial: diagenesis). This is a serious problem, as any paleontologists who hope to do field-based research need a strong (or even mediocre) background in taphonomy. I find taphonomy to be, on one hand – relatively intuitive, and on the other hand – more intellectually stimulating than bread and butter phylogenetics (this is not a slam against cladistics; I just find taphonomic problems more interesting and challenging). 

A painting of a whale fall assemblage. From www.mbari.org

Taphonomy is also very important if a paleontologist is interested in anything relating to paleoecology: with respect to a fossil, paleoecologic information can generally be preserved intrinsically (functional anatomy, oxygen/carbon isotopes, etc.) or extrinsically (gut residues, coprolites, feeding traces, juvenile/adult or other social associations, etc.). The former category is more or less decoupled from taphonomy, as it generally pertains to information not affected by taphonomic loss. However, once a paleontologist wants to start talking about the nature of a fossil assemblage, and whether it represents a mass death assemblage, a nesting ground, or evidence of feeding behavior, these issues extend outside the bones themselves, so to speak, and into tangential issues affected by processes of preservation. To say anything regarding paleoecology and using extrinsic information, a paleontologist had better do his or her damned homework; there are plenty of examples in the published literature of non-taphonomists saying some pretty silly things.

Because I study fossil marine mammals, whale falls provide a wealth of data regarding what happens to a whale after it dies on the seafloor. So, what does happen? To sum it up, in a way – a multitude of organisms rush in to eat it. Whale fall faunas appear to show a series of successive stages (Smith and Baco 2003):

1) Mobile scavenger stage: large scavengers such as fish, sharks, hagfish, chimaeras, and invertebrates feed (rapidly) on whale soft tissue.

2) Enrichment opportunist stage: organically enriched sediment and exposed bones are colonized by opportunistic polychaetes and crustaceans.

3) Sulphophilic stage: a trophically complex assemblage of nearly 200 species of invertebrates and microorganisms inhabit the skeleton while lipids in the bones undergo anaerobic breakdown and emit sulphides.

A fourth stage – the reef stage – has been hypothesized for late-stage whale falls (Smith, 2006) that are chemically inert, so to speak – and colonized by sessile invertebrates taking advantage of higher elevation (and thus currents) above the seafloor. However, no evidence for this stage currently exists and it is purely hypothetical.

 

A group of Osedax stalks and gills growing in a whale bone. From www.mbari.org

In particular, modern whale falls have benefited taphonomists by providing valuable information regarding rates of scavenging and the timing of skeletonization (exposure of bones in a carcass) as well as rates of bone degradation, burial, and the types of organisms that may leave a physical trace record of their colonization. In 2004, a new type of whale fall specialist was discovered infesting the bones of a baleen whale skeleton off the coast of California: a bone-eating “zombie” polychaete worm, named Osedax (Rouse et al., 2004). It was discovered in massive amounts on bones, with reddish gills mounted on stalks emanating from small holes in the bone. Roots of the worm extend into the bone, and host symbiotic bacteria to synthesize nutrients from the bone. It is currently debated exactly what Osedax feeds upon: lipids in the bone, or collagen. Since 2004, a number of species of Osedax have been discovered, and are now known worldwide from deep marine whale falls. If this parade of weirdness wasn’t enough, the males are dwarfs, never leave the larval stage, and live on/in the females.

 

An individual Osedax worm separated from its bony home. From www.mbari.org

In the next few posts, I’ll cover several issues, including the discovery of Osedax traces in fossil bone (part 2), Osedax colonization/consumption of other types of vertebrates (part 3), and implications for taphonomy and possible “megabias” in the fossil record (part 4).

I highly recommend watching this video: it's not educational, per se, but if you're familiar with whale falls, it is delightfully animated. Whale Fall (afterlife of a whale).

Don't forget to see the rest of the series:

Bone-eating zombie worms, part 4: more on bird bones, and Osedax colonizes whale teeth

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

Bone-eating zombie worms, part 2: the discovery of fossil Osedax traces

References:

Allison, P. A., C. R. Smith, H. Kukert, J. W. Deming, and B. A. Bennett. 1991. Deepwater
taphonomy of vertebrate carcasses: a whale skeleton in the bathyal Santa Catalina
Basin. Paleobiology 17(1):78-89.

Peters, S. E., M. S. M. Antar, I. S. Zalmout, and P. D. Gingerich. 2009. Sequence
stratigraphic control on preservation of late Eocene whales and other vertebrates at Wadi
Al-Hitan, Egypt. Palaios 24:290-302.

Rouse, G. W., S. K. Goffredi, and R. C. Vrijenhoek. 2004. Osedax: Bone-eating marine
worms with dwarf males. Science 305:668-671.

Smith, C. R., and S. R. Baco. 2003. Ecology of whale falls at the deep-sea floor.
Oceanography and Marine Biology: an Annual Review 41:311-354.

Smith, C. R. 2006. Bigger is better: the role of whales as detritus in marine ecosystems.
Pp. 286-302. In J. A. Estes, D. P. DeMaster, D. P. Doak, T. M. Williams, and R. L.
Brownell, eds. Whales, Whaling and Ocean Ecosystems. University of California Press,
Berkeley, CA.