It was both surprising and exciting to excavate for the first time.… The new reconstruction shows a very different animal from Walcott’s and other restorations, … far more trilobite like than had been thought. Indeed, I conclude Naraoia was a trilobite that lacked a thorax, and place it in a separate order of that class (1977, p. 411).
This change may seem small, a shift from one well-known group to another, and therefore an event of little conceptual interest in the midst of so much Burgess turmoil and discovery. Not so. The classification of Naraoia is a satisfying final piece of a puzzle, proving that the basic Burgess pattern—anatomical disparity beyond the range of later times—applies at all levels. Simon’s weird wonders had established the pattern at the highest level of phyla, the basic ground plans of animal life. Whittington’s monographs had told the same story at the next lower level of disparity within phyla—group after group of orphaned arthropods spoke of Burgess anatomy far beyond the range of any later time, despite a vast increase in arthropod species, including a modern insect fauna of nearly a million described species. Now Harry had demonstrated the same pattern again at the lowest level of disparity within major groups of a phylum. He had discovered an apparent contradiction in terms—a soft-bodied trilobite with a carapace of two valves. (In 1985 he would describe a second soft-bodied trilobite, Tegopelte gigas, one of the largest Burgess animals at nearly a foot in length, so Naraoia is no lone oddity among trilobites.) The Burgess pattern seems to display a “fractal” character of invariance over taxonomic scales: crank up the telescope, or peer down the microscope, and you see the same picture—more Burgess disparity, followed by decimation and diversification within fewer surviving groups.
The monograph on Naraoia marked a conceptual watershed for Whittington. He finally sank the class Trilobitoidea officially, as an artificial wastebasket with no evolutionary validity. He had finally freed himself to view the Burgess arthropods as a series of unique designs, beyond the range of later groups.
The Class Trilobitoidea Størmer, 1959 was proposed as a convenient category in which to place various supposedly trilobite-like arthropods, mainly from the Burgess Shale, and regarded as of equal rank to the Class Trilobita. Studies recently published and in progress are providing abundant new information, particularly on appendages.… The Class Trilobitoidea can no longer be regarded as a useful concept, and a new basis for assessment of relationships is emerging (1977, p. 440).
Harry’s next monograph, on Aysheaia, begins with his most explicit recognition of the new view: “The animals in this community include an astonishing variety of arthropods as well as bizarre forms, such as those described by Whittington and Conway Morris which, like Aysheaia, are not readily placed in Recent higher taxa” (1978, pp. 166–67). Aysheaia was perhaps the most famous and most widely discussed of Burgess organisms—for an interesting reason rooted in the two p’s, “primitive” and “precursor.” Walcott (1911c) had described Aysheaia as an annelid worm, but colleagues soon pointed out with excitement that the creature could hardly be distinguished, at least superficially, from a small group of modern invertebrates called the Onychophora and represented primarily by a genus with the lovely name Peripatus. The Onychophora possess a mixture of characters recalling both annelids and arthropods; many biologists therefore regard this group as one of the rare connecting forms (“nonmissing links,” if you will) between two phyla. But modern Onychophora are terrestrial, while the actual transition from annelid to arthropod, or the derivation of both from a common ancestor must have occurred in the sea. In addition, modern Onychophora have undergone more than 550 million years of evolution since the supposed linkage of annelid and arthropod, and could not be viewed as direct models of the transition. A marine onychophoran from the Cambrian would be a creature of supreme evolutionary importance—and Aysheaia, generally so interpreted (Hutchinson, 1931), became a hero of the Burgess. The great ecologist G. Evelyn Hutchinson, who had done important work on the taxonomy of Peripatus in South Africa, and who, looking back on a rich career from his ninth decade, still places his study of Aysheaia among his most significant (interview of April 1988), wrote:
In Aysheaia we have a form living under entirely different ecological conditions from those of the modern species, and at a very remote time, yet having an external appearance, which in life must have been extraordinarily similar to that of the living representatives of the group (1931, p. 18).
Aysheaia has an annulated, cylindrical trunk, with ten pairs of annulated limbs attached at the sides near the lower surface, and pointing down, presumably for use in locomotion (figures 3.41 and 3.42). The anterior end is not separated as a distinct head. It bears a single pair of appendages, much like the others in form and annulation but attached higher on the sides and pointing laterally. The terminal mouth (smack in the middle of the front surface) is surrounded by six or seven papillae. The head appendages bear three spinelike branches at their tip, and three additional spines along the anterior margin. The body limbs end in a blunt tip carrying a group of up to seven tiny, curved claws. Larger spines emerge from the limbs themselves. These spines are absent on the first pair, point forward on pairs 2–8, and backward on 9–10.
3.41. Aysheaia, probably an onychophoran. Drawn by Marianne Collins.
Whittington combined this anatomical information with other data to reconstruct an interesting and unusual life style for Aysheaia. On or near six of the nineteen Aysheaia specimens he found remains of sponges—an association hardly ever encountered with other Burgess animals. Whittington conjectured that Aysheaia might have fed on sponges and lived among them for protection as well (figure 3.43). The tiny terminal claws of the limbs would not have worked on mud, but might have helped in climbing upon sponges and holding on. The anterior appendages could not have swept food directly into the mouth, but they might have lacerated sponges with their spines, permitting the animal to lap up nutritious juices and soft tissues. The backward-facing claws and spines of the posterior body limbs might have functioned as anchors to keep the animal in place at odd angles.
3.42. Reconstruction of Aysheaia by Whittington (1978). (A) Top view. (B) Side view: the ring of tentacles surrounding the terminal mouth is visible at the top; the dorsal surface is at the right.
3.43. Reconstruction by Whittington (1978), showing Aysheaia living and feeding on sponges.
But was Aysheaia an onychophoran? Whittington admitted some impressive similarities in the anterior appendages, the short, uniramous body limbs with terminal claws, and the annulations on body and limbs. But he also cited some differences, including lack of jaws (possessed by modern onychophorans) and the termination of the body at the last pair of limbs (the body extends farther back in modern onychophorans).
In Whittington’s judgment, these differences raised sufficient doubts to debar Aysheaia from the Onychophora and to recognize this genus, albeit tentatively, as a unique and independent group. Citing the lessons of other genera, he wrote: “Thus Aysheaia, like other Burgess Shale animals as Opabinia, Hallucigenia, and Dinomischus, does not fit readily into any extant higher taxon” (1978, p. 195).
I regard these words as momentous, and (symbolically, at least) as the completion of the Burgess transformation. I say this, ironically, because I think that for once, Harry was probably wrong about Aysheaia. I believe that, on the balance of evidence, Aysheaia should be retained among the Onychophora. The similarities are impressive and anatomically deep, the differences superficial and not of great evolutionary import. Of Harry’s two major differences, jaws may simply have evolved later. Structures can be added in evolution provided that ancestral anatomies do not preclude their development. Just such an event occurred in at least one prominent Burgess group. Burgess polychaetes have no jaws, but jaws evolved by Ordovician times and have persisted ever since. As for the extension of the body beyond the last pair of limbs, this strikes me as an easy evolutionary change, well within the capacity of a broad group like the Onychophora. The American paleontologi
st Richard Robison, who developed a much longer list of distinctions between Aysheaia and modern onychophorans, agrees nonetheless that Aysheaia belongs in the group, and writes of Whittington’s second major difference:
In terrestrial onychophorans, projection of the body behind the posterior pair of lobopods [limbs] seems to represent nothing more than minor modification to improve sanitation by slight displacement of the anus. Such body design is less important to animals living in water, where currents aid separation of toxic waste from the body. Thus, posterior shape of the body may be more indicative of habitat than phylogenetic affinity (1985, p. 227).
Why then did Whittington separate Aysheaia from the Onychophora and assert its taxonomic uniqueness? Since this conclusion came from a man who, for years, had been resisting the temptation to separate Burgess organisms from well-known groups, and who had made such divisions only when forced by weight of evidence, we would naturally assume that he had been compelled to this uncomfortable conclusion by new data direct from Aysheaia. But read the 1978 monograph carefully. Whittington did not upset any of Hutchinson’s basic statements about Aysheaia. Harry had listed and discussed the same differences; he had essentially affirmed, in much greater and more elegant detail to be sure, Hutchinson’s excellent work. But Hutchinson had classified Aysheaia as an onychophoran—on the very same data that Whittington later used to reach the opposite conclusion.
What then had prompted Whittington’s reversal, if not the anatomy of Aysheaia? We have a reasonably well-controlled psychological experiment here. The data had not changed, so the reversal of opinion can only record a revised presupposition about the most likely status of Burgess organisms. Obviously, Whittington had come to accept, and even to prefer, the idea of taxonomic uniqueness for animals of the Burgess Shale. His conversion was complete.
Many fascinating genera still awaited description; the halfway point had not even been reached. But Whittington’s 1978 monograph on Aysheaia marks the codification of a new view of life. What a dizzying few years between 1975 and 1978—from the disturbing discovery that Opabinia is neither an arthropod, nor anything else ever known before, through the cascade of Simon’s weird wonders, to the full acceptance of taxonomic uniqueness as a preferred hypothesis. Three short years and a new world!
ACT 5. The Maturation of a Research Program: Life after Aysheaia, 1979-Doomsday (There Are No Final Answers)
The seven short years from Marrella (1971) to Aysheaia (1978) had produced an extraordinary shift of perspective—from a project designed to redescribe some arthropods classified in familiar groups, to a new conception of the Burgess Shale and the history of life.
The pathway had not been smooth and direct, clearly marked by the weight of evidence and logic of argument. Intellectual transformations never proceed so simply. The flow of interpretation had meandered and backtracked, mired itself for a time in a variety of abandoned hypotheses (on the primitive status of Burgess oddballs, for example), but finally moved on to explosive disparity.
By 1978, the new conception had settled, as symbolized by Whittington’s interpretation of Aysheaia. The period thereafter, and continuing today—Act 5 of my drama—possesses a new calm, in shared confidence about the general status of the Burgess fauna. Yet this final act is no anticlimax in its unaltered conceptual scheme. For confidence has a great practical virtue—you can go forward on specifics without continual worry about basic principles. Hence, Act 5 has witnessed an extraordinary productivity in the resolution of Burgess organisms. Old mysteries have fallen like ranks of tin soldiers—not quite so easily as child’s play (to continue the simile), but with much greater efficiency now that a firm framework guides a coherent effort. The reconstructions of the last decade include some of the strangest and most exciting of Burgess creatures. I can hardly wait to read Act 6.
THE ONGOING SAGA OF BURGESS ARTHROPODS
Orphans and Specialists
At the end of 1978, the scorecard for soft-bodied arthropods spoke strongly for uniqueness and disparity. Four genera—Marrella, Yohoia, Burgessia, and Branchiocaris—had been orphaned within the arthropods. Only Canadaspis (and perhaps Perspicaris) belonged to a modern group; Naraoia had been reclassified as a trilobite, but as a surpassingly odd member of the group, and the prototype of a new order. Opabinia had been tossed out of the arthropods altogether, and Aysheaia lay in limbo. A good beginning, but not yet imbued with the convincing weight of numbers. As I argued above, the “big” questions of natural history are answered as relative frequencies. More data were required—something approaching a complete compendium of Burgess arthropods. Act 5 has now fulfilled this need, and the revisionary pattern has held, in spades.
In 1981, Derek Briggs continued his dispersion of the bivalved arthropods into a series of orphaned groups (with Canadaspis holding increasingly lonely vigil as a true crustacean). Briggs used all twenty-nine specimens to decide the fate of Odaraia, the largest bivalved arthropod in the Burgess Shale (up to six inches long). At the front of its head, and extending beyond the carapace, Odaraia bears the largest eyes of any Burgess arthropod (figure 3.44). Yet Briggs could find only one other structure on the head—a single pair of short ventral appendages behind the mouth. (This arrangement, with no antennae and only one post-oral pair of appendages, is unique, and would be sufficient in itself to mark Odaraia as an orphan among arthropods. But the head is not well preserved under the strong carapace of Odaraia, and Briggs was not confident that he had been able to resolve all structures.) The trunk, enclosed by the large carapace for more than two-thirds of its length, contained up to forty-five limb-bearing segments. The limbs, except perhaps for the first two pairs, are typically biramous.
3.44. Reconstruction of the arthropod Odaraia by Briggs (1981a). (A) Top view, showing the bivalved carapace as transparent so that the soft anatomy may be revealed beneath. Note the projection of the eyes in front of the carapace, and the arrangement of the three-pronged tail behind. (B) Side view.
3.45. Odaraia, swimming on its back. The numerous biramous appendages can be seen through the transparent tubular carapace. Note also the large eyes in front, the curious three-pronged tail behind, and the single pair of feeding appendages behind the mouth. Drawn by Marianne Collins.
Odaraia also exhibits two unique and peculiar specializations. This animal bears a three-pronged tail (figure 3.45), with two lateral flukes and one dorsal projection—a bizarre structure that evokes images of sharks or whales, rather than lobsters. Nothing similar exists in any other arthropod. Second, the bivalved carapace is not flattened, but essentially tubular. Moreover, Briggs argued that the relatively short appendages did not extend beyond the tube—and furthermore, that the two valves forming the tube probably couldn’t gape widely enough to let the appendages protrude from any ventral opening. Clearly, Odaraia did not walk on the sea floor. Briggs wrote: “The combination of an essentially tubular carapace and a telson bearing these large flukes is unique among the arthropods” (1981a, p. 542).
Briggs performed a functional study and united these two peculiarities to infer a mode of life for Odaraia. He argued that Odaraia swam on its back, using its three-pronged tail for stabilization and steering, and its carapace as a filtering chamber for capturing food. Water could be taken in at one end; the appendages would extract food particles and pass the depleted stream out the other end of the carapace.
Briggs had proven once again that the watchword for Burgess arthropods was “uniquely specialized,” not “primitively simple.” In September 1988, Derek wrote to me, in an assessment of his 1981 monograph: “Odaraia turned out to be not only taxonomically unusual but, more importantly in my view, functionally unique among the arthropods.”
Also in 1981, David Bruton published his monograph on Sidneyia, already discussed on pages 87–96. The resolution of Sidneyia set an important milestone in the study of Burgess arthropods for two reasons. First, Sidneyia had long acted as a focus or symbol for the fauna. Walcott regarded this genus as the largest of B
urgess arthropods (we now know that the soft-bodied trilobite Tegopelte and one or two of the bivalved arthropods were bigger). Moreover, he mistakenly assumed that a spine-studded appendage, found separately, fitted onto the head of Sidneyia (for he knew nothing else big enough to carry such an appendage). With this addition Sidneyia was not only large, but also fierce. Since our culture values these traits, Sidneyia attracted attention. (A psychologist friend of mine explains our society’s fascination with dinosaurs by a simple list—“big, fierce, and extinct.” Sidneyia, in Walcott’s reconstruction, is all three). In Bruton’s revision, Sidneyia is still a predator, but the pair of limbs belongs to Anomalocaris. Sidneyia carries no feeding structures on its head.
Second, Sidneyia was the first form to be redescribed in the final, potentially coherent group of Burgess arthropods—the so-called “merostomoids.” Hope had surely faltered for placing any major Burgess assemblage in a modern group, but the “merostomoids” represented a last gasp and opportunity for traditionalism. Merostomes are a group of marine arthropods including modern horseshoe crabs and fossil eurypterids. They are united with spiders, scorpions, and mites into one of the four great arthropod groups, the Chelicerata. The basic merostome body plan—more clearly shown by eurypterids, than by horseshoe crabs—includes a strong head shield, a trunk of several broad segments equal in width to the head, and a narrower tail, often forming a spike. Several Burgess genera, including Sidneyia, share this basic form.