Weird world of fossil worm cocoons

Stephen McLoughlin, Benjamin Bomfleur and Thomas Mörs (Sweden)

Fossil hunters occasionally chance upon small glossy red to amber-coloured, roughly circular objects on bedding planes, when they crack open shales that were deposited in ancient swamps and rivers. These curious fossils range from about a millimetre in diameter up to the size of a fingernail (Fig. 1). When well preserved, they are egg shaped, but, in most cases, they have been flattened to a thin flake in the rock by the weight of the overlying strata. Some specimens appear to have a net-like coating on the surface but, otherwise, they offer few clues as to their identity.

Indeed palaeontologists have reported these objects for over 150 years and have variously interpreted them as the eggs of insects, parts of lichens, the food-catching devices of ancient invertebrates, the membranous coatings of seeds, or the linings of clubmoss sporangia. Many early palaeobiologists simply labelled them as ‘red eggs’ and avoided assigning them to any particular biological group.

These strange objects occur mostly in sediments deposited in continental settings, and they have been reported widely in the residues left over after palaeobotanists have dissolved rock samples in the search for fossil spores, pollen and leaf cuticle. Two conclusions can be gleaned from these occurrences:

1. The mysterious fossils likely belong to a land- or freshwater-based organism; and
2. These objects are composed of a material that is extraordinarily resistant, even to some of the strongest acids used in the laboratory.

The mystery of their origin was finally solved in 1991, when Norwegian palaeontologist Svein Manum and his colleagues recognised that these fossils match the characteristics of the egg-bearing cocoons of modern leeches and their relatives. Our further investigations have revealed that the link to leeches had been identified by the German naturalist, F Gergens, all the way back in 1861, but his report was largely overlooked by later researchers, probably because it was published as a brief communication in the German language. These strange fossils are now known to have a record extending back to the Triassic, but DNA-dating of modern cocoon-producing annelids (earthworms, leeches and their relatives) suggests that this group has an even earlier origin – perhaps in the early Palaeozoic.

New Antarctic discovery

Recently, one of us (TM) recovered a few new specimens of these strange fossils after sieving Eocene (50myr-old) sediments collected on Seymour Island, Antarctica (Fig. 2).

Using a high-powered light microscope, it was clear that several varieties of fossil cocoons were present – some with solid walls and a variable coating of entangled threads (Fig. 3), and another with a rigid mesh-like wall, covering an inner layer of thread-like material (Figs. 4 and 5). We have now formally described these tiny fossils and assigned them to several new species. However, the significance of these fossils does not end with their identification as palaeontological curiosities. They also tell us something about the evolutionary history of worms and their relatives, and they potentially reveal a hidden world of fossil microbes.

To fully appreciate these fossils, one must understand a few things about worm biology. There are three major classes of modern annelids: Echiura (spoon worms), which are entirely marine; Polychaeta (bristle worms), which are mostly marine; and Clitellata (earthworms, leeches and crayfish worms), of which some occur in marine waters, but others have widely colonised freshwater and terrestrial environments.

Only members of Clitellata produce cocoons to protect their eggs. Members of this group are hermaphrodites – they have both pairs of sex organs. During reproduction, they generally exchange sperm between individuals and some species can store the sperm cells in specialised sacs for several months. At the time of egg laying, earthworms, leeches and their relatives secrete a mucus-like material from glands on the clitellum, which are a series of specialised body segments situated in the front half of the body. The clitellum is best seen in earthworms, where it forms a thickened ‘saddle’ (Fig. 6).

The initial mucus-like secretion acts as a scaffold onto which the worm secretes additional threads of more robust material that may build up into several distinct layers to form a cylindrical cocoon around the clitellum. These secretions are initially soft and jelly-like, but, over the course of a few hours to days, they harden into a rigid and extremely durable coating. In the meantime, eggs are deposited into the cocoon, sperm are released for fertilisation, and the cocoon is eventually sealed by a cap (operculum) as the animal withdraws, and then deposited on the substrate. Once the embryos have matured, the eggs hatch and the cocoon’s operculum detaches to release the young worms.

A hidden world of fossil microbes

It is the early stage of cocoon secretion that is important for palaeontology, because it is during this time that micro-organisms from the surrounding environment can become entrapped and entombed in the sticky threads of the cocoon wall, so escaping decay and ultimately becoming part of the fossil record (Fig. 7).

This type of preservation is somewhat like bugs becoming entombed in amber. Manum and his colleagues noted one such unexpected occurrence of a nematode entombed in the wall of a fossil leech cocoon from the Cretaceous of Spitsbergen. More recently, one of us (BB) discovered a microscopic fossil Vorticella (a bell-shaped ciliate protozoan) preserved in the wall of a leech cocoon from the Triassic of Antarctica (Fig. 8).

Given these previous records of entrapped micro-organisms, our recently discovered Eocene cocoons from Seymour Island offered the chance for us to search for additional fossil microbes. Such microbes are best seen on the smooth inner surface of the cocoon. Therefore, we studied the inner surface of a broken cocoon using a scanning electron microscope. Sure enough, embedded within the innermost layer of the cocoon were numerous fossilised spherical and rod-shaped bacteria (Fig. 9).

More curiously, however, we observed numerous elongate structures with long whip-like tails preserved among the bacteria (Fig. 10).

These turned out to be the sperm cells of the cocoon-producer itself that had become trapped in the sticky wall material, before they could fertilise an egg. In many cases, these spermatozoa were broken – probably as a consequence of their efforts to wriggle free of the sticky cocoon lining. When complete, they have a long coiled ‘drill-bit’-shaped front part (the acrosome), followed by a granular region that contains the nucleus. In turn, this is followed by a striate region containing the mitochondria, and then a very long and slender whip-like tail. The finer details revealed similarities to the sperm cells of modern branchiobdellids (crayfish worms) – a group of leech relatives that live in a symbiotic relationship with freshwater crayfish hosts.

If these are indeed the fossil cocoons of crayfish worms, this implies that branchiobdellids had a much greater geographic range in the Eocene compared to their modern relatives, which are restricted to the Northern Hemisphere. However, research on such fossil cocoons is at a very early stage. Once the full extent of diversity and the stratigraphic ranges of these fossils are clarified, they may even have value for correlating and dating sedimentary rocks.

We now have collections of fossil clitellate annelid cocoons from several localities around the world and it will involve some challenging detective work to see if any of these specimens have further identifiable micro-organisms trapped in their walls. Potentially, these cocoons could open up a new gallery of fossil soft-bodied micro-organisms from soil and freshwater environments for which, previously, we have had a very meagre fossil record. Groups – such as tardigrades, rotifers, euglenoids, flatworms and nematodes – are all candidates for becoming entrapped in the sticky walls of newly secreted annelid cocoons. Perhaps, in the future, annelid cocoons will become a valuable resource for understanding the evolution of soft-bodied micro-organisms, as amber is for revealing the fossil record of insects.

Further reading

Bomfleur, B., Kerp, H., Taylor, T.N., Moestrup, Ø., Taylor, E.L. 2012. Triassic leech cocoon from Antarctica contains fossil bell animal. PNAS 109, 20971–20974.

Bomfleur, B., Mors, T., Ferraguti, M., Reguero, M.A. & McLoughlin, S. 2015. Fossilized spermatozoa preserved in a 50-myr-old annelid cocoon from Antarctica. Biology Letters 11, 20150431.

Jansson, I.-M., McLoughlin, S. & Vajda, V. 2008. Early Jurassic annelid cocoons from eastern Australia. Alcheringa 32, 285–296.

Manum, S.B., Bose, M.N. & Sawyer, R.T. 1991. Clitellate cocoons in freshwater deposits since the Triassic. Zoologica Scripta 20, 347–366.

McLoughlin, S., Bomfleur, B., Mörs, T. & Reguero, M. 2016. Fossil clitellate annelid cocoons and their microbiological inclusions from the Eocene of Seymour Island, Antarctica. Palaeontologia Electronica (in press).