One problem remains -- that of scale, and it is here that his spiders seem to embody something unique: they are very much bigger than they ought to be, given the unwritten rules Tolkien seems to have used for creating monsters. Or are they? In this short essay I hope to show, or at least suggest, that Tolkien could have had suitable real-life models for gigantic spiders -- models that inexplicably slipped my mind when writing The Science of Middle-earth. For there once existed spiny, jointed-legged, land-living creatures of sizes comparable with Tolkien's arachnid horrors -- fearsome creatures that could have haunted the lives of our most remote ancestors. What follows, therefore, is something of a corrective.

So, what are these Tolkienian rules for engendering monsters? Leaving aside those creatures that derive directly from pre-existing fantasy or myth (orcs, dragons, trolls), and those that appear to be mainly Tolkien's own invention (ents, balrogs), Tolkien's monsters have analogues in the real world, particularly among extinct creatures markedly larger than their modern relatives. This fits in with the general theme of diminution and loss that runs through Tolkien's work, but is also informed by his evident knowledge of natural history. The Kine of Araw that were the source of Boromir's horn are rare or extinct cattle similar to the aurochs, the gigantic precursor of modern cattle (3); the flying steeds of the Nazgûl are rare or extinct creatures that seem closely akin to pterodactyls; the mûmakil of Harad are creatures comparable in size with some extinct elephants; even the heroic eagles have plausible models in giant but extinct birds of prey. At first sight, Tolkien's spiders do not fit into any of these categories, being neither especially mythical, nor particularly Tolkienian in invention, and yet far too huge, given what we know about living and extinct spiders.

As I wrote in The Science of Middle-earth, the largest living spider is Theraphosa leblondi, a species of bird-eating tarantula from South America that can span a dinner plate at full stretch, but whose body would be no larger than a clenched fist. However, the forests of the Carboniferous Period around 300 million years ago hosted much more formidable arthropods (jointed-limbed creatures), including crow-sized dragonflies, millipedes two metres long, and a spider, called Megarachne, with a body the size of a bagel. Horrific indeed, were you to have met one, but not a match for Shelob: and recent work has demoted even this, suggesting that the fossil of Megarachne is not a spider after all, but possibly a small part of a much larger arthropod -- and thereby hangs a tale, and -- perhaps -- the solution to the missing model of Tolkien's spiders.

Megarachne is now thought by at least one scientist to be a fragment of a different kind of creature called Woodwardopterus (4). This was a member of a group of extinct arthropods called the eurypterids (5), which looked like horrible hybrids of scorpions and giant lobsters. Although sometimes referred to as sea-scorpions, eurypterids were distant relatives of both scorpions and spiders. Although most eurypterids were rather small, even the small ones (at around 20 centimetres long) were large for arthropods, and some of them grew to more than two metres in length, the largest arthropods known to have existed. Could eurypterids have served as models for Tolkien's spiders?

In The Science of Middle-earth I referred briefly to meter-long scorpions but then passed by. Why? The reason was to do with scale, because the sizes of the largest arthropods are limited by the implacable laws of physics. Even the largest insect has a body no larger than a clenched fist, because insect size is limited by the capacity of the way they breathe. Insects take in air through a distributed network of fine tubes that perforate their surfaces. Because an animal's surface area increases at a lesser rate than its volume as it grows (basically, in proportion to the square of its mass, rather than the cube), there is a size when an animal using an all-over breathing mechanism can no longer acquire enough oxygen to satisfy the needs of its tissues. This size is rather small, which is one reason why most insects are tiny. But oxygen was more abundant in the Carboniferous atmosphere than it is today, possibly explaining why many Carboniferous arthropods (especially insects) were larger than their modern relatives.

Other arthropods have got over the surface-area constraint by concentrating their respiratory surfaces into 'book-lungs', folded structures similar in many ways to human lungs, which pack a very large surface area into a very small space. Spiders and scorpions breathe this way, which is why they are often larger than insects. The related dinner-plate-sized horseshoe crabs have gills concentrated into lung-like 'book-gill' structures, and it is possible that eurypterids also had a similar respiratory system. Respiration, then, need be no constraint on the size of an arthropod.

Gravity is more of a problem. In contrast to vertebrates (such as you and me), supported by internal skeletons of bone, arthropods have external skeletons based on a substance called chitin. In order to grow, an arthropod must first shed its external skeleton, after which it inflates its body and waits for the replacement skeleton, forming beneath the old one, to harden. This process suggests an obvious problem for arthropods larger than a certain size: unsupported during the molt, they run the risk of their bodies crushing themselves under their own weight.

But what I forgot when I wrote The Science of Middle-earth was that this applies only to arthropods molting on land. Arthropods molting underwater can exploit the buoyancy of water, allowing them, at least potentially, to grow to very large sizes. This seems to have been true for the monstrous eurypterids.

However, the fact remains that spiders are obligately terrestrial creatures: Shelob and Ungoliant never get their feet wet, let alone go for a swim. This may be true, but the converse does not hold. There is plenty of evidence that eurypterids, even very large ones, ventured up on to land. Writing in a recent issue of the journal Nature, Martin A. Whyte of the University of Sheffield, England, describes the fossilized tracks left by an eurypterid around 1.6 meters in length and a meter wide (6). Although this instance is spectacular, scientists have known for decades that eurypterids ventured on to land, possibly for extended periods. The earliest forests could have been patrolled by enormous arthropods comparable in size to the spiders of Mirkwood, if not perhaps to Shelob or Ungoliant.

Land-crawling eurypterids, therefore, offer a solution to the problem of a real model for Tolkien's spiders: he could have used eurypterids (or, ancient arthropods in general) as models for giant spiders in the same way he used the aurochs for the Kine of Araw, or pterodactyls for the Nazgûl-birds.

But did he? Even though we know from his letters that Tolkien had more than a passing knowledge of paleontology, I know of no direct evidence that he knew about eurypterids in particular, let alone that this knowledge (if it existed) influenced the creation of his fictional giant spiders.

There the case must rest, but for one thing: as I argue in The Science of Middle-earth, the paleontology current in Tolkien's time bore more of a resemblance to narrative and myth-making than it does today. Tolkien was presumably as sensitive to paleontological myths as to those of literature; it just happens that one of the greatest paleontological myth-makers of all time lived and worked during Tolkien's most productive period as a writer; and this myth-maker produced a compelling story about eurypterids and their relation to our own existence.

This mythologist was Alfred Sherwood Romer (1894-1973), an almost exact contemporary of Tolkien, and one of the most influential paleontologists who ever lived. As well as a peerless scholar, Romer was a compelling and powerful writer, and in 1933 published a myth (scientists would call it a 'scenario') explaining why the earliest fishes evolved bone and, in many cases, heavy suits of external armor. His argument was that the earliest fishes were easy prey for merciless, gigantic eurypterids, and had to evolve armor in self-defense. The general loss of armor in these early fishes could only happen, argued Romer, when eurypterids declined in importance.

But the tale did not end there. Eurypterids lived for millions of years after fishes lost their armor, and even after some of these fishes evolved legs instead and ventured on to land, becoming -- after many more adventures -- our own remote reptilian ancestors. Some of the eurypterids, it seems, also ventured on to land. Could they have been pursuing their ancient fishy quarry as part of some aeons-long conflict fought under the stars when the world was young? Were our ancestors fighting their own Long Defeat? Was our own evolution driven by the flight from an ancient arachnoid terror? I do not know if Tolkien had any knowledge of such speculations. Had he done so, I suspect he might have found them irresistible.

-- Olog-hai

1. Humphrey Carpenter, Biography
2. Henry Gee, The Science of Middle-earth, Cold Spring/Souvenir, 2005.
3. http://greenbooks.theonering.net/guest/files/012005.html
4. http://homepage.mac.com/paulselden/PhotoAlbum44.html
5. http://en.wikipedia.org/wiki/Eurypterus
6. Whyte, M. A., A gigantic fossil arthropod trackway, Nature 438, 576 (1 December 2005): doi 10.1038/438576a
7. Romer, A. S. Eurypterid influence on vertebrate history, Science 78, 114--117 (1933).