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.