Wonderful Life: The Burgess Shale and the Nature of History

by Stephen Jay Gould

  Wiwaxia

  When I asked Simon Conway Morris why he had chosen to work for many years on so complex a beast as Wiwaxia, he replied, with welcome frankness, that Harry and Derek had both done their “blockbusters,” and he wanted to prove that he could also write a “strict monograph in the tradition of the others.” (I regard this statement as overly modest. Simon’s 1977 and 1979 works on priapulids and polychaetes are true and extensive monographs. But each treats several genera, and therefore cannot give the exhaustive treatment to any one species that Whittington provided for Marrella splendens, or Briggs for Canadaspis perfecta.) Perhaps Simon felt unfulfilled in choosing such rare creatures for his first run through the weird wonders that he could write only short, separate papers on five examples. In any case, his monograph on Wiwaxia is a thing of beauty, and the original source of my interest in writing about the Burgess Shale (Gould, 1985b)—for which, Simon, my greatest thanks once again.

  Wiwaxia is a small creature, shaped as a flattened oval (a well-rounded pebble in a stream comes to mind), about an inch long, on average, with a two-inch maximum. The simple body is covered with plates and spines called sclerites—except for the naked ventral surface that rested on the substrate as Wiwaxia crawled across the sea floor. Walcott had shoehorned Wiwaxia into the polychaete worms, mistaking these sclerites for superficially similar structures in a well-known marine worm, whose technical and common names convey such different impressions—Aphrodita, the sea mouse. But Wiwaxia has no body segmentation and no true setae (the hairlike projections of polychaetes)—and therefore lacks both defining traits of the group. Like so many Burgess animals, Wiwaxia is an anatomy unto itself. Wiwaxia is also inordinately difficult to reconstruct, because the sclerites spread over the rock surface in a horribly confused jumble as the fossil compressed on its bedding plane. In figure 3.56, a camera lucida drawing of the most coherent specimen in the most convenient orientation provides a good idea of the problems involved. Simon’s resolution of Wiwaxia is one of the great technical achievements of the Burgess research program.

  The sclerites of Wiwaxia, the key to this reconstruction, grew in two different styles; flattened scales, ornamented with parallel ridges, cover most of the body, while two rows of spines emerge from the top surface, one on each side of the central axis (figures 3.57 and 3.58). The scales display a symmetrical and well-ordered tripartite pattern: (1) a field of overlapping plates, on the top surface, arrayed as six to eight parallel rows (figure 3.57A); (2) two regions on each side (figure 3.57B), with two rows of plates pointing upward and two rows pointing backward; (3) a single bottom row of crescent-shaped sclerites forming a border between the ornamented upper body and the naked belly.

  3.56. (A) Camera lucida drawing of a complete specimen of Wiwaxia. Note the complex intermingling of the compressed sclerites. The labels, which need not concern readers here, identify individual sclerites. For example, R.d.sl. 1 (top right) is a right, dorsal sclerite (sl.) of the first row. L.sp.1 (top left) is the first spine on the left side. (B) Enlargement of one particularly interesting sclerite (located in A at the lower left, next to the label br.). A small brachiopod (br.) affixed itself to the sclerite during the life of this Wiwaxia specimen. Using such evidence, we can reconstruct the life style of this animal. It could not have lived by burrowing under the substrate, for such a habit would have killed the brachiopod.

  The two rows of seven to eleven elongate spines arise from the upper row of sclerites on each side, near the border with the plates of the top surface. The spines project upward and presumably acted as protection against predators, as indicated by their breakage in several specimens (during the animal’s life, not after burial).

  Simon could see little of Wiwaxia’s internal anatomy beyond a straight gut near the ventral surface—further evidence, combined with the naked belly and spines pointing upward, for the animal’s orientation in life. But one internal feature may be crucial both for understanding Wiwaxia and for a general interpretation of the Burgess fauna. About five millimeters from the front end, Conway Morris found two arc-shaped bars, each carrying a row of simple, conical teeth directed toward the rear (figure 3.59). The front bar bears a notch at its center, marking a toothless area between the side regions, each with seven or eight teeth. The rear bar has a more curved but smoother front margin, and teeth all along the back edge. These structures were probably attached to the bottom of the gut. In view of their form and their position near the animal’s front end, their interpretation as feeding devices—“jaws,” if you will—seems secure.

  3.57. Reconstructions of Wiwaxia by Conway Morris (1985). (A) Top view: one of the two rows of spines has been omitted (note the blackened areas of their insertion) so that the sclerites can be seen better. (B) Side view: the front end is at the left.

  In attempting to gather and integrate all the evidence, Conway Morris proceeded as far as possible beyond the basic anatomy of Wiwaxia, probing for hints wherever he could extract some precious information—from growth, from injury, from ecology, from preservation. Small specimens either carry relatively small spines or lack them entirely—thus providing a rare Burgess example of change in form with growth. Two juxtaposed specimens seem to represent an act of molting by one individual, not two animals accidentally superimposed by the Burgess mudslide: the smaller specimen is shrunken and elongate, as if the large body had just crawled out, leaving its old skin behind as “a vacated husk.” Small brachiopod shells, occasionally found attached to a sclerite, indicate that Wiwaxia crawled along the top of the sediment, and did not burrow underneath, where the permanent hitchhikers could not have survived. Patterns of breakage in spines point to the activity of predators and to the possibility of escape. Small spines occasionally found in an otherwise large and uniform row indicate the possibility of regeneration after breakage, or of orderly patterns in replacement (as in the shedding and cycling of teeth in vertebrates without a permanent dentition). The presence of “jaws” suggests a life spent scraping algae or gathering detritus on the substrate.

  3.58. Wiwaxia as it might have crawled on the sea floor. Drawn by Marianne Collins.

  3.59. The jaw apparatus of Wiwaxia (Conway Morris, 1985).

  Put all these bits and pieces together, and Wiwaxia emerges as a complete, working organism—a herbivore or omnivore, living on small items of food collected from the sediment surface as it crawled along the sea floor.

  But if all these guides had enabled Conway Morris to reconstruct Wiwaxia’s mode of life, he could find no similarly persuasive clues to homology, or genealogical relationship with any other group of organisms. With no setae or appendages and no segmentation, Wiwaxia is neither an arthropod nor an annelid. The jaw displays an intriguing similarity to the feeding apparatus of mollusks, called a radula, but nothing else about Wiwaxia even vaguely resembles a clam, snail, octopus, or any other mollusk living or dead.* Wiwaxia is another Burgess oddball, perhaps closer to the Mollusca than to any other modern phylum, if its jaw can be homologized with the molluscan radula—but probably not very close.

  Anomalocaris

  I could not have made up a better story to illustrate the power and extent of the Burgess revision than the actual chronicle of Anomalocaris—a tale of humor, error, struggle, frustration, and more error, culminating in an extraordinary resolution that brought together bits and pieces of three “phyla” in a single reconstructed creature, the largest and fiercest of Cambrian organisms.

  The name Anomalocaris, or “odd shrimp,” predates the discovery of the Burgess Shale, for this is one of the few soft-bodied Burgess creatures endowed with parts solid enough for preservation in ordinary faunas (the spicules of Wiwaxia are another example). The first Anomalocaris were found in 1886 at the famous Ogygopsis trilobite beds, exposed on the next mountain over from the Burgess Shale. In 1892, the great Canadian paleontologist J. F. Whiteaves described Anomalocaris in the Canadian Record of Science as the headless body of a shrimplike arthropod. Walcott accepted the standard view
that this fossil represented the rear end of a crustacean, with the long axis as the trunk and the ventral spines as appendages (figure 3.60). Charles R. Knight followed this tradition in his famous painting of the Burgess fauna (see figure 1.1), where he constructed a composite organism by attaching Anomalocaris to Tuzoia, one of the bivalved arthropod carapaces that lacked associated soft parts and was therefore a good candidate for the cover of Anomalocaris’s unknown head.

  But this official name-bearer of Anomalocaris provides only one piece of our story. Three other structures, all named by Walcott, play central roles in this complex tale.

  3.60. The fragment of a segmented creature originally called Anomalocaris in 1886 (Briggs, 1979). For many years this fossil was considered to represent the trunk and tail of an arthropod. It has now been correctly identified as one of a pair of feeding appendages from the largest of all Cambrian animals.

  3.61. Reconstruction of appendage F by Briggs (1979). Walcott originally described this structure as a feeding limb of Sidneyia. Briggs reinterpreted it as an appendage of a giant arthropod. Recent research shows that appendage F is actually one of a pair of feeding organs from the largest known Cambrian animal.

  1. The head of Sidneyia, the arthropod that Walcott named for his son Sidney and then described first among Burgess creatures (1911a), bears a pair of antennae and no other appendages. Walcott also found a large isolated arthropod feeding limb, later (1979) called “appendage F” (for feeding) by Derek Briggs (figure 3.61). Sidneyia was, in Walcott’s judgment, the only Burgess creature large enough to carry such an appendage; its rapacious character also fitted well with Walcott’s concept of Sidneyia as a fierce carnivore. So Walcott made the marriage without direct evidence, and joined appendage F to the head of Sidneyia. Bruton (1981) later determined that Sidneyia’s head shield does not contain enough space to accommodate such a structure.

  2. Walcott’s second paper (1911b), on the supposed jellyfish and holothurians (sea cucumbers of the echinoderm phylum) from the Burgess Shale, does not rank among his more accurate efforts. He described five genera. Mackenzia is probably a sea anemone and therefore a coelenterate in the same phylum as jellyfish, but Walcott placed this genus in his other group, the holothurians. A second creature turned out to be a priapulid worm (Conway Morris, 1977d). A third, Eldonia, still ranks as a peculiar floating holothurian in the latest reconstruction (Durham, 1974), but I’ll wager a reasonable sum that it will finally end up as another Burgess oddball.

  Walcott named a fourth genus Laggania, and identified this fossil as a holothurian, on the basis of one specimen. He noted a mouth, and thought that it might be surrounded by a ring of plates. Poor preservation had effaced all the distinctive features of holothurians. Walcott admitted: “The body of the animal is so completely flattened that the tube feet are obscured, the outline of the ventral sole lost, and the concentric bands almost obliterated” (1911b, p. 52).

  3. As a fifth and last genus, Walcott named the only Burgess jellyfish Peytoia. He described this peculiar creature as a ring of thirty-two lobes around a central opening. This series of lobes could be divided into four quadrants, with a larger lobe at each of the four corners of the squared-off ring, and seven smaller lobes between the corners in each quadrant. Walcott noted two short points on each lobe, projecting inward toward the central hole. He interpreted these structures as “points of attachment of the parts about the mouth, or possibly oral arms” (1911b, p. 56). Except for radial symmetry, Walcott found no trace of the defining characters of a jellyfish—no tentacles or concentric muscle bands. Peytoia, looking more like a pineapple slice than a medusa, made an awfully odd jellyfish. No true member of the group has a hole in the center. Nonetheless, Walcott’s interpretation prevailed. The best-known modern reconstruction of the Burgess fauna, published in Scientific American several years after Whittington and colleagues began their revisions (Conway Morris and Whittington, 1979), shows Peytoia as a kind of Frisbee cum flying saucer cum pineapple slice, entering the scene from the west (figure 3.62).

  Now who ever dreamed about a connection between the rear end of a shrimp, the feeding appendage of Sidneyia, a squashed sea cucumber, and a jellyfish with a hole in the center? Of course, no one did. The amalgamation of these four objects into Anomalocaris came as an entirely unanticipated shock. Moreover, the successful resolution did not emerge from this unimproved initial chaos. Several intermediate efforts, all basically erroneous but each supplying an important link in a developing story, preceded the successful conclusion.

  Anomalocaris has been the nemesis of recent Burgess research. This creature eventually yielded its secret, but not until both Simon Conway Morris and Derek Briggs had committed their biggest mistakes in coping with its various parts. One cannot hope to do anything significant or original in science unless one accepts the inevitability of substantial error along the way. Three steps, however, did inch matters forward toward a resolution, whatever the longer lateral errors.

  3.62. The best-known reconstruction of the Burgess Shale, drawn for the 1979 Scientific American article by Conway Morris and Whittington. Note priapulid worms in their burrows, and several Burgess oddballs—including Dinomischus (17), Hallucigenia (18), Opabinia (19), and Wiwaxia (24). In a major error, two jellyfish (10) are shown swimming in like pineapple slices from the west. This structure is actually the mouth of Anomalocaris. (From “The Animals of the Burgess Shale,” by Simon Conway Morris and H. B. Whittington. Copyright © 1979 by Scientific American, Inc. All rights reserved.)

  1. In 1978, Conway Morris applied Whittington’s new techniques for distinguishing three-dimensional structure to Laggania, now regarded as a sponge rather than a holothurian. He took a dental microdrill to the counterpart of the unique specimen, and uncovered a pineapple slice of Peytoia, where Walcott had identified the indistinct mouth. Conway Morris stood on the threshold of the proper interpretation, but he guessed wrong. He considered the possibility that the “sponge” called Laggania was not a distinct creature, but a body attached to Peytoia, which would then become the centerpiece of a strange medusoid. But Conway Morris rejected this reconstruction because he regarded almost all Burgess organisms as discretely preserved, rather than disaggregated into parts. He wrote: “The vast majority of Burgess Shale fossils are preserved complete and it may reasonably be concluded that the body of Laggania cambria is not an integral part of Peytoia nathorsti, but an extraneous addition to the medusoid which is interpreted here as a sponge” (1978, p. 130). He argued that the association was simply an accident of deposition from the Burgess mudslide: “The association of the medusoid and sponge is presumably by chance. The phyllopod bed was deposited as a series of turbidites, and it is likely that after transport the two specimens settled together” (1978, p. 130).

  Conway Morris guessed wrong about the reasons for a link between Peytoia and Laggania, but he had uncovered (literally) a key association, joining the first two of four pieces that would form Anomalocaris.

  2. In 1982, Simon tried to grapple with the strangeness of Peytoia (Conway Morris and Robison, 1982). He called Peytoia “one of the most peculiar of Cambrian medusoids” (1982, p. 116), and even used the word “enigmatic” in his title. Simon did not correctly resolve this beast, but he cast doubt upon its affinity with medusoids, and thus kept the channels of questioning wide open. Writing about the central hole, Conway Morris and Robison concluded: “This feature is unknown in either living or fossil cnidarians and may indicate that Peytoia nathorsti is not a cnidarian. Its relationship with any other phylum would seem to be even more obscure” (1982, p. 118).

  3. Anomalocaris itself, Whiteaves’s original rear end of a shrimp, had been allocated to Derek Briggs in the original divvying up of the Burgess Shale. It was, after all, supposed to be the body of an arthropod with a bivalved carapace.

  In 1979, Briggs published a provocative reconstruction of his assignment. He made two outstanding observations that contributed to the resolution of Anomalocaris:

&nb
sp; First, he recognized that Anomalocaris was an appendage with paired spines on its inner borders, not an entire body with appendages on its ventral edges. If Anomalocaris was the trunk of an entire organism, then some of the more than one hundred specimens should show traces of a gut, and at least a few would be found with arthropod joints on their supposed appendages.

  Second, he argued that Anomalocaris and appendage F (Walcott’s feeding limb of Sidneyia) were variants of the same basic structure, and probably belonged together. This conclusion, as we shall see, was not quite correct, but Briggs’s argument did properly unite two more pieces of the Anomalocaris puzzle.

  Beyond these important insights, Briggs’s reconstruction was basically erroneous, though spectacular. He continued to view both Anomalocaris and appendage F as parts of an arthropod, conjecturing that Anomalocaris was a walking leg, and appendage F a feeding structure, of a single giant creature, probably more than three feet long! He called his paper “Anomalocaris, the Largest Known Cambrian Arthropod.”

  But Briggs was scarcely convinced by his own reconstruction. So many mysteries remained. He puzzled over the failure to find any sign, even fragmentary, of the giant body that supposedly held these appendages. Could a structure three feet long be entirely absent from a soft-bodied fauna? Briggs conjectured that such pieces might exist as organic sheets and films, thus far ignored for their lack of distinguishable structures. He wrote: “Large, previously unidentified, relatively featureless fragments of the body cuticle of Anomalocaris canadensis almost certainly await discovery on the scree slopes of Mt. Stephen” (1979, p. 657). Little did Derek realize that the body of Anomalocaris had been known and named since Walcott’s time, but masquerading as the “holothurian” Laggania, later interpreted as a sponge with a jellyfish on top.