American Scientist

What is a fossil? This word can mean many things, but it usually refers to the mineralized skeleton of some extinct organism—a trilobite or dinosaur, for example—which resists degradation and thus survives the eons largely intact. The fossil record of such hard parts, however, captures only a minority of invertebrates, because up to two-thirds of these species are soft-bodied—they have no shells at all.

Fortunately, circumstances occasionally conspire to preserve evidence of these creatures. Here we relate such an example, one that reveals an amazing amount of detail about animals that lived during the Silurian Period.

For those who are not geologists, the time scale involved in this story may not be familiar, so first we must review some Earth history. The first major diversification of animal life took place during what paleontologists and evolutionary biologists refer to as the Cambrian Explosion. At the time, all animal life was restricted to the ocean. During much of the Cambrian Period (542–490 million years ago), most animals lacked the ability to burrow deeply into sediment. So after subsea mudflows entombed bottom-dwelling animals, their carcasses were protected from burrowing scavengers, leaving behind a fairly rich fossil record.

Deeper burrowers appeared in abundance during the succeeding period, the Ordovician, at which point buried carcasses became more vulnerable to scavenging. This is one reason why more soft-bodied animals are preserved in deposits of Cambrian age than in those from more recent times, which typically contain only fossilized hard parts.

It is for this reason that our discovery is particularly important. More than a decade ago, we found a diverse, well-preserved assemblage of largely soft-bodied fossils from the Silurian Period, which followed the Ordovician. Because they are from a typical marine setting, these remarkable fossils provide important insights into the early evolution of life in the ocean.

Silurian Time Capsules

We found these fossils in the rocks of Herefordshire, a county that lies on the historic borderland between England and Wales. In the late 18th and early 19th centuries, this area was the stomping ground for many geological pioneers, including one who has been jokingly dubbed the "King of Siluria," Sir Roderick Impey Murchison. In 1839, he wrote a monumental treatise, titled The Silurian System, in which he coined the name for this geological period. He named it after the Silures, an ancient tribe that inhabited this part of Britain during Roman times.

Herefordshire owes much to its underlying geology. It boasts a beautiful, tranquil landscape of gently rolling hills, small-scale escarpments and open river valleys, which have attracted artists and men of letters down the ages. Some modern-day geologists have gravitated to the place, too.

One, Robert J. King, a noted mineralogist and retired curator at the Department of Geology of the University of Leicester, visited Herefordshire while vacationing in the area in the summer of 1990. Intrigued by the geology, he returned later that year to collect rock samples. On splitting open a hard, near-spherical concretion that had rolled to the quarry floor at one site, he caught sight of some sparkling mineralization that seemed to preserve a fossil.

King collected nine concretions, four of which revealed fossils when he cracked them open, and in December 1990 he donated these specimens to the collections at Leicester. In the fall of 1994, King's successor as curator, Roy G. Clements, asked one of us (David Siveter) to look at one of these finds. It showed something quite unexpected under the microscope—an arthropod with limbs preserved. That discovery prompted the involvement of another one of us (Derek Siveter), David's twin brother and fellow paleontologist, who is a specialist in both arthropods and Silurian geology.

Derek photographed the material at the University of Oxford, and together with his brother and King visited Herefordshire in December 1994 to find the source of these concretions. The following April, Derek contacted another one of us (Briggs), a specialist in exceptionally preserved fossils. Unlike most of the examples that Briggs had studied, the Herefordshire fossils he was shown were not visually spectacular in hand specimens, and the mineral that gives them their sparkle, common calcite, would normally not invite a second glance. This rather uninteresting appearance is undoubtedly the main reason why this wonderful fossil cache lay hidden from so many generations of geologists.

The Herefordshire fossils were deposited 425 million years ago within a marine basin that extended across what is now central England into Wales. This basin first formed some 120 million years earlier, at the beginning of the Cambrian Period. The fossils are preserved in a soft, cream-colored volcanic ash that mixed with some of the normal marine sediment.

This ash deposit is known from just the one locality, where it is exposed over a distance of about 30 meters. Measuring more than a meter thick in places, it is unusual compared with other ash deposits in this region. The hard concretions that carry the fossils vary in size from that of a cherry to something as big as a grapefruit. They seem to have formed randomly throughout the deposit. Even now, the ashy sediment around them is largely unconsolidated and can be dug by hand without great difficulty.

The volcanic ash that engulfed the animals was deposited on top of a thin layer of mud covering thick limestones, the remnants of a reef that was effectively dead and had probably sunk well beneath the waves. Indeed, the animals that became fossilized here likely lived 100 to 200 meters down, below the depth to which light penetrates. We know this because we found no vestiges of photosynthetic algae, which are common in contemporaneous rocks laid down at shallower points on the seafloor to the east.

It is not clear whether a volcanic eruption entombed these Silurian animals directly, Pompeii-style. Perhaps they were buried many years after the explosion, covered in ash that had been transported along the seabed by a fast-moving bottom current. In any event, what is clear is that some very special circumstances allowed for their remarkable preservation.

The first was the immediate precipitation of clay minerals around the dead organisms, which decayed over time, leaving empty spaces behind. The mineral calcite (a form of calcium carbonate) then filled these natural molds, faithfully replicating the shape of the animals. Even spines and other structures just a few microns across were preserved in this way.

At about the same time, the hard round concretions began to form, being cemented by calcite. Thanks to the early hardening of these Silurian time capsules in this way, the fossils were not squashed as the ash layer slowly compacted. We can be sure of this because the fossils appear undeformed and because the concretions are spherical rather than pancake shaped.

Freshly exposed concretions are hard with a blue- to gray-colored core. The Herefordshire concretions are unusual in that they do not correspond in size to the fossils they contain. And the fossils are commonly not at the center—so the nucleus of the concretions must have been something other than the fossil itself. Just what it was remains a mystery, however, because no trace remains.

We have carried out fieldwork at this site for several days most summers since 1996. On most of these occasions, we hired excavators who used earth-moving equipment to strip off the overlying shale and expose the volcanic deposit fully. They scooped the ash up in the bucket of their backhoe and tipped it out slowly, at which point we collected the hard, round concretions by hand from the piles of dumped sediment. We carefully mined the deposit in this way, amassing more then 4,000 samples, which are held in the Oxford University Museum of Natural History.

In our announcement of the discovery to the scientific community (a 1996 article in Nature), we highlighted the rarity of soft-bodied fossils from the 100-million-year interval following the Cambrian. We provided brief descriptions of a small arthropod and of a number of other animals that we then thought were worms. We noted the unusual setting—calcite-filled voids in concretions in a volcanic ash laid down in the sea—and suggested that deposits like this could provide an important new source of data on the history of life. But at that point we were relying on random cross sections to view the ancient creatures preserved in these rocks. Little did we know at the time how much more there was to learn.

Liberating the Fossils

At the start, we studied these concretions by splitting them open with a hydraulic vise, cracking them in two and then further dividing the pieces in half until a fossil appeared—or until we reduced the sample to a pile of tiny fragments. About half of the concretions we examined in this way proved to contain fossils. But it was hard to glean much about the animals' complex shapes from these randomly split sections.

We did the best we could and attempted to discern the properties of the most common species, the tiny arthropod Offacolus kingi, by studying it in several hundred randomly split concretions. But despite our best efforts, the picture we obtained of this animal was woefully incomplete. We were unable, for example, to work out how its head appendages fit together. This approach was even less satisfactory for rarer species (which is to say, everything else)—just imagine trying to figure out what something like a shrimp looks like from just a few randomly oriented slices through it. So it became clear to us that we needed to find a way to extract the fossils from these rocks.

The calcite casts proved too small and delicate to be dug out physically, and they couldn't be dissolved out chemically because they are so similar in composition to the rest of the concretion. They were not visible in x-ray photographs or in the other scanning methods we tried because they have the same density as the rock that contains them. So we resorted to physical tomography, which is just a fancy term for serial grinding. That is, we ground away at the fossil in very fine increments, up to 50 per millimeter, and recorded each exposed surface as a digital image.

Paleontologists have used serial sectioning since the beginning of the last century. But working in the late 1990s, we were able to take advantage of modern computing techniques to produce high-fidelity visualizations of the data. That's not to say that the software for doing this was something we could buy off the shelf. One of us (Sutton) had to write a considerable amount of code from scratch. All this programming allowed a computer to distinguish automatically between the fossil and the lighter-colored rock enclosing it. We then edited these digital images to correct them where our eyes told us that such retouching was necessary. These two steps were the virtual analogues of what paleontologists normally do: digging bones out of rock and cleaning them.

It took a long time, but it was worth the effort. All our image gathering and editing produced spectacular results. Using Sutton's software, we can manipulate our virtual fossils on the computer screen, using stereo glasses to add depth. Or we can render them as rotating animations. What's more, the software allows different structures to be hidden at will, allowing us to perform virtual dissections of these long-dead creatures.

Revisiting our preliminary reconstruction of Offacolus, which was based on random sections, we were able to substitute direct observation for educated guesswork, allowing us to correct many minor errors. And we finally figured out the nature of the head appendages: There are seven pairs, five of them with two branches each. This better understanding allowed us to place Offacolus more accurately on life's evolutionary tree. This animal turns out to be a primitive member of the chelicerates, the major group that includes scorpions, mites, ticks and horseshoe "crabs."

Although our method of studying these fossils is time consuming and destructive, it has yielded a wealth of data unobtainable in any other way. Through these observations, the Herefordshire fossils have begun to give up their secrets, revealing a diverse and astonishingly well-preserved fauna.

The Worm that Wasn't

It is difficult for us to predict what one of these animals looks like based on random fractures through a few concretions, so we tend to refer to them by informal names until we can work out their shapes in detail. One of the first species we tackled in this way was Acaenoplax hayae, which we called just "spiny worm."

After much work, we determined that the under-surface of this animal was smooth but had a number of flexible lobes, arranged in a pattern of overlapping chevrons, which probably helped it to gain purchase on the sediment. The body was wrinkled and carried an array of sharp spines behind the head that must have served for defense. The largest spines projected from fleshy ridges on its back, which also had seven plate-like shells along its length, most of which were also spiny. At the rear, two shells enclosed a respiratory cavity from which fleshy gills protruded.

It was hard to know what to make of such a strange creature. The presence of seven shells, together with an obvious space where an eighth seems to have been lost in evolution, suggested to us that Acaenoplax is related to the living chitons, which are eight-shelled polyplacophoran mollusks. Other investigators have interpreted almost identical shells (preserved without any evidence of soft parts) from Silurian rocks in Gotland, Sweden, as belonging to this group. Our reconstruction made it clear, however, that Acaenoplax was no chiton: it lacked a foot, a feature that is characteristic of this group.

The body plan of Acaenoplax is closer to aplacophorans, simple wormlike mollusks that lack a foot and have a rear respiratory cavity. However, no aplacophoran is known with shells. Acaenoplax appears to be a kind of molluscan 'missing link'—neither a polyplacophoran nor an aplacophoran, although more closely related to the latter.

This conclusion implies that today's aplacophorans are secondarily simplified, having lost the shells present in their Acaenoplax-like ancestors. So, contrary to orthodox thinking, the earliest mollusks were not simple wormlike forms. Acaenoplax revamped our understanding of how the mollusks fit into the evolutionary tree of life.

Even though we had grown accustomed to calling it spiny worm, in the end it became clear that Acaenoplax was a mollusk rather than a real worm. Kenostrychus clementsi, however, the second most common species in the Herefordshire fauna, is a polychaete or bristle worm, an early representative of the most diverse worm group in the modern oceans.

Kenostrychus is neither the oldest nor the most unusual fossil polychaete, but it is by far the best preserved of any age. Although it appears normal in most respects, its gills take the form of coiled tentacles attached to an unusual part of its trunk appendages. This configuration has implications for the early evolution of polychaete respiratory structures. Kenostrychus provides an example of how even relatively routine animals of this antiquity, when preserved with sufficient fidelity, can also inform our understanding of evolution.

A Diversity of Crustaceans

Ostracodes (sometimes called "seed shrimps") are crustacean relatives of barnacles and water fleas. These tiny aquatic arthropods are typically only a few millimeters long as adults. Most species live on or close to the bottom.

Ostracodes are by far the most common group of arthropods in the fossil record, known from thousands of species and countless empty shells. They are also abundant today. They have been very successful in adapting to a wide range of marine, brackish and freshwater environments, from the deep ocean to garden ponds.

Although ostracodes have been studied extensively for more than 150 years, the earliest forms were known to paleontologists only from their shells. And without being able to study how their limbs were configured, these investigators struggled to understand the creatures' affinities—could the tiny fossils simply be another group of arthropods masquerading in an ostracode-like shell? With the discovery of fossil ostracodes from Herefordshire, this question was answered at a stroke.

Inside the protective, hinged shell of the first ostracode we investigated, we discovered the head and trunk with their specialized appendages for feeding and locomotion, and a pair of lateral eyes. The gut of this creature is also preserved, together with gills for breathing and evidence of its circulatory system. This anatomy proved remarkably similar to that in some living forms, indicating that these creatures were indeed ostracodes and that little evolutionary change has taken place over 425 million years. The male copulatory organ is even preserved in this Silurian fossil, providing the earliest unequivocal testimony for gender in animals.

Colymbosathon ecplecticos—meaning "swimmer with a large penis"—of course attracted extensive media coverage when we announced its discovery in 2003. The International Herald Tribune noted, "He's 425 million years old and clearly virile." MSNBC declared that the "Oldest known male fossil bares all." And although the New York Times thoughtfully informed its readership that "It's a boy," the UK's Guardian reported on this story under the headline, "Well Hung Scientists' Big Find." It goes to show what heady intellectual considerations drive most of the world's science reporting.

A second exceptionally well-preserved ostracode not only turned out to be a female, but one containing eggs and possible juveniles. We called it Nymphatelina gravida—"pregnant young woman of the sea"—because this fossil provides an unequivocal and unique view of maternal care in a fossil invertebrate and demonstrates that an egg-brooding reproductive strategy was passed down from the Silurian to the present day.

The evidence of the soft parts shows that both these remarkable Herefordshire ostracodes belong to a living group called the myodocopes. Surprisingly, however, the shell of the female in particular resembles that of a different group of fossil ostracodes, the palaeocopes, which are known only from their preserved hard parts. This observation demonstrates that the shell alone may be a poor clue to the true nature of the animal within!

The Herefordshire deposit also preserves a number of other crustaceans, including barnacles, which are remarkable in that they metamorphose from a small free-swimming larva (the cyprid) to a stalked "goose" barnacle or to the more familiar balanomorphs, which are often seen attached to rocks in the intertidal zone. The adult barnacle develops a mineralized shell of several parts, which tend to separate when the animal dies and may be preserved as individual fossils. The tiny larva is much less likely to become fossilized. Indeed, we discovered the first fossil cyprid known, Rhamphoverritor reduncus, in the Herefordshire deposit.

The most familiar living crustaceans, at least to the restaurant goer, are the malacostracans, the group that includes the shrimps, lobsters and crabs. Crabs have a good fossil record because of the thick calcified covering on their backs, which is called the carapace. In simpler malacostracans, however, such as the phyllocarids, even the carapace was soft and prone to decay; hence their fossil record, which holds the key to the origin and early evolution of the group, is poor.

Fortunately we discovered the earliest completely preserved phyllocarid, which we named Cinerocaris magnifica ("splendid shrimp from the ashes"), among the Herefordshire fossils. It has two pairs of antennae and prominent eyes projecting forward from the head, which also bears a suite of feeding appendages. The body is divided into a thorax and abdomen, the latter being muscular (and no doubt good to eat!) and ending in the tail fork typical of this group.

Not all the crustaceans in the Herefordshire deposit are clearly recognizable as belonging to still-living groups. Tanazios dokeron, for example, has the two pairs of antennae and mandible characteristic of crustaceans, but its rear head appendages were not specialized for feeding—they appear very similar to those of the trunk. The head shield of Tanazios is a strange horned structure, and the long trunk is made up of more than 60 short segments, each with a similar pair of unusual appendages shaped a bit like a catcher's mitt. A pair of antenna-like appendages projects from the tail. Given these characteristics, we concluded that Tanazios was an early offshoot of the crustacean lineage.

Other Creatures Great and Small

Our Herefordshire finds shed light on a variety of animals besides crustaceans, including the pycnogonids, or sea "spiders," which are a group of marine invertebrates that are widespread in the oceans today, with almost 1,200 living species. But their delicate form has resulted in an extremely sparse fossil record of just a few tens of specimens belonging to perhaps nine species.

We discovered the most completely preserved fossil sea spider in the Herefordshire deposit, older by about 35 million years than the previous record holder, at least for an adult animal. (Tiny specimens from the Cambrian of Sweden have been interpreted as sea-spider larvae, but this identification is disputed.)

The relationship of sea spiders to other arthropods has been a subject of debate for two centuries. There are two main views on the position of sea spiders on the tree of life: Either they belong with the chelicerates, or they represent a group separate from all other arthropods. Well-developed pincers on the large first appendage of the Silurian sea spider we discovered, Haliestes dasos, support the former view, and a comparison with other fossil and living species shows that the features typical of today's sea spiders had arisen by Silurian times.

Our studies also improved the understanding of the Marrellomorpha, a poorly known group of fossil arthropods that contains five genera and species. Marrellomorphs are important because they branched off the arthropod lineage earlier than did the trilobites, chelicerates and crustaceans and their various relatives. Our discovery of Xylokorys chledophilia from Herefordshire, provides the most complete three-dimensionally preserved marrellomorph, and the first from the Silurian.

The Herefordshire fauna includes other ancient animals that, unlike Xylokorys or Haliestes, were already known to science—but only from their fossilized skeletal remains. Our finds have added information on their soft tissues.

The Herefordshire specimens of the sea-star Bdellacoma, for example, preserve not only the mineralized plates of the skeleton, but also soft tissues including tube feet and papulae (respiratory organs). We have also described a gastropod mollusk that uniquely preserves internal structures such as a coiled gut, previously unknown in a fossil.

Another example is provided by the brachiopods or "lamp shells," a type of shellfish unrelated to the mollusks. Brachiopod shells are among the most common fossils, and many paleontologists have spent their entire careers studying them, examining countless thousands of specimens—not one of which contained any internal soft tissues. We have so far reconstructed just one brachiopod specimen from Herefordshire, and the amount of information it provides is so great that it almost mocks the normal fossil record of brachiopods, which consists only of shells.

The fossil we studied contains three tiny post-larval brachiopods, representing at least two different species, which are attached to a larger brachiopod, Bethia serraticulma, a third species. All three species preserve the fleshy pedicle (attachment stalk), and one also preserves sensory hairs. The largest brachiopod fossil shows internal structures including the mantle that secretes the shell, and the filaments used for filter feeding.

In spite of its spectacular state of preservation, however, Bethia has proved difficult to place, ironically because the soft tissues obscure parts of the shell that are critical for classification. Bethia, nonetheless, carries an important message: Paleontologists who use living forms as models for fossil animals can easily be misled, particularly for organisms like brachiopods, which are much less diverse today than they were in ancient times.

More to Come?

Our research on the Herefordshire deposit continues. Many more fossils remain to be described: sponges, worms, a diversity of arthropods (including a trilobite with preserved appendages), more brachiopods, mollusks and echinoderms, and, perhaps most exciting, a number of enigmatic forms that we cannot yet identify.

We are continuing to explore ways to present our findings, too. For example, we have fabricated physical models of these fossils using what engineers refer to as rapid-prototyping techniques. One system entails the use of a "3D printer," which can construct a replica of the fossil based on the computer reconstruction by fusing powdered plastic resin with a laser beam. In the future, we hope to use this technique to produce museum dioramas showing this Silurian seafloor community.

Although the Herefordshire fossils are unique, it seems unlikely that they will remain so. Somewhere in another ash deposit, other concretions must harbor similarly extraordinary fossils, perhaps of a different age, perhaps containing other vital clues to the history of life. Anyone with curiosity enough to split open a lump of rock might stumble on such a treasure trove. Please let us know if you do!