Leonardo’s Mountain of Clams and the Diet of Worms

by Stephen Jay Gould

  In an attempt to answer their own question, they performed the obvious experiment—and made an astonishing discovery. The food has become the feeder—this time by overwhelming in number, not equaling in size (the whelks are much smaller than the lobsters). The conventional passive voice of scientific prose does not convey excitement well, but a good story easily transcends such a minor limitation. So, in Barkai and McQuaid’s own words, and without any need for further commentary from me (I would only be tempted to make some arch and utterly inappropriate statement about slave revolts—Spartacus and all that):

  One thousand rock lobsters from Malgas Island were tagged and transferred to Marcus Island . . . The result was immediate. The apparently healthy rock lobsters were quickly overwhelmed by large numbers of whelks. Several hundreds were observed being attacked immediately after release and a week later no live rock lobsters could be found at Marcus Island . . . The rock lobsters escaped temporarily by swimming, but each contact with the substratum resulted in several more whelks attaching themselves until weight of numbers prevented escape. On average each rock lobster was killed within fifteen minutes by more than three hundred Burnupena [whelks] that removed all the flesh in less than an hour.

  Sic semper tyrannis.

  3. FISH AND DINOFLAGELLATES. Fish don’t generally eat dinoflagellates; why should they even deign to notice such microscopic algae, floating in the plankton? But dinoflagellates certainly don’t eat fish; the very notion, given the disparity in sizes, is ludicrous to the point of incomprehensibility.

  Dinoflagellates do, however, kill fish, by indirect mechanisms long known and well studied for their immense practical significance. Under favorable conditions, dinoflagellate populations can soar to 60 million organisms per liter of water. These so-called blooms can discolor and poison the waters—“red tide” is the most familiar example—leading to massive deaths of fish and other marine organisms.

  J. M. Burkholder and a group of her colleagues from North Carolina State University have studied toxic blooms associated with fish kills in estuaries of the southeastern United States. The largest event resulted in the death of nearly one million Atlantic menhaden in the estuary of the Pamlico River. The oddity of this case lies not in the killing of fish per se, a common consequence of dinoflagellate blooms. We have always regarded the deaths of fishes and other marine organisms during red tides as passive and “unintended” results of dinoflagellate toxins, or other consequences of massive algal populations during blooms. No one had supposed that dinoflagellates might actively kill fish as an evolved response for their own explicit advantage, including a potential nutritional benefit for the algal cells. And yet the dinoflagellates do seem to be killing and eating fishes in a manner suggesting active evolution for this most peculiar reversal.

  The dinoflagellate lives in a dormant state, lying on the sea floor within a protective cyst. When live fish approach, the cyst breaks and releases a mobile cell that swims, grows, and secretes a powerful, water-soluble neurotoxin, killing the fish. So far, so what?—though the presence of fish does seem to induce activity by the dinoflagellate (breaking of the cyst), thus suggesting a direct link. Anatomical and behavioral evidence both suggest that dinoflagellates have actively evolved their strategy for feeding on fishes. The swimming cell, breaking out from the cyst, grows a projection, called a peduncle, from its lower surface. The cells seem to move actively toward dead or dying fishes. Flecks of tissue, sloughed off from the fish, then become attached to the peduncle and get digested. The authors describe this reversal at maximum disparity in size among my four cases:

  The lethal agent is an excreted neurotoxin. [It] induces neurotoxic signs by fish including sudden sporadic movement, disorientation, lethargy and apparent suffocation followed by death. The alga has not been observed to attack fish directly. It rapidly increases its swimming velocity to reach flecks of sloughed tissue from dying fish, however, using its peduncle to attach to and digest the tissue debris.

  4. SPONGES AND ARTHROPODS. Among invertebrates, sponges rank as the lowest of the low (the bottom rung of any evolutionary ladder), while arthropods stand highest of the high (just a little lower than the angels, that is, just before vertebrates on a linear list of rising complexity). Sponges have no discrete organs; they feed by filtering out tiny items of food from water pumped through channels in their body. Arthropods grow eyes, limbs, brains, and digestive systems; many live as active carnivores. Most arthropods wouldn’t take much notice of a lowly sponge, but we can scarcely imagine how or why a sponge might subdue and ingest an arthropod.

  However, in a 1995 article, crisply titled “Carnivorous Sponges,” J. Vacelet and N. Boury-Esnault of the Centre d’Oceanologie of Marseille have found a killer sponge (about as bizarre as a fish-eating dinoflagellate—but both exist). Relatives of this sponge, members of the genus Asbestopluma, have only been known from very deep waters (including the all-time record for sponges at more than 25,000 feet), where behavior and food preferences could not be observed. But Vacelet and Boury-Esnault found a new species in a shallow-water Mediterranean cave (less than one hundred feet), where scuba divers can watch directly.

  The deep sea is a nutritional desert, and many organisms from such habitats develop special adaptations for procuring large and rare items (while relatives from shallow waters may pursue a plethora of smaller prey). Asbestopluma has lost both filtering channels through the body and the specialized cells (called choanocytes) that pump the water through. So how does this deep-water sponge feed?

  The new species grows long filaments that extend out from the upper end of the body. A blanket of tiny spicules, or small skeletal projections, covers the surface of the filaments. The authors comment: “The spicule cover . . . gives the filaments a ‘Velcro’-like adhesiveness”—the key to this feeding reversal at maximal anatomical distance for invertebrates. The sponge captures small crustaceans on the filaments—and they can’t escape any more than a fuzz ball can detach itself from the Velcro lining of your coat pocket. The authors continue: “New, thin filaments grew over the prey, which was completely enveloped after one day and digested within a few days.” The sponge, in other words, has become a carnivore.

  Four fascinating stories to give us pause about our preconceptions, particularly our dualistic taxonomies based on the domination of one category over another. The little guys sometimes turn tables and prevail—often enough, perhaps, to call the categories themselves into question.

  I see another message in these reversals—a consequence of the reassessment that must always proceed when established orders crumble, or merely lose their claim to invariance. In our struggle to understand the history of life, we must learn where to place the boundary between contingent and unpredictable events that occur but once and the more repeatable, lawlike phenomena that may pervade life’s history as generalities. (In my own view of life, the domain of contingency looms vastly larger than all Western tradition, and most psychological hope, would allow. Fortuity pervades the origin of any particular species or lineage. Homo sapiens is a contingent twig, not a predictable result of ineluctably rising complexity during evolution—see the end of chapter 15 for Darwin’s view on this issue.)

  The domain of lawlike generality includes broad phenomena not specific to the history of particular lineages. The ecological structure of communities should provide a promising searching ground, for some principles of structural organization must transcend the particular organisms that happen to occupy a given role at any moment. I imagine, for example, that all balanced ecosystems must sustain more biomass as prey than as predators—and I would accept such statements as predictable generalities, despite my affection for contingency. I would also have been willing to embrace the invariance of other rules for sensible repetition—that single-celled creatures don’t kill and eat large multicellular organisms, for example. But these four cases of reversed order give me pause.

  In a famous passage from the Origin of Species, Charles Darwin extolled the
invariance of certain ecological patterns by using observed repetition in independent colonizations to argue against a range of contingently unpredictable outcomes:

  When we look at the plants and bushes clothing an entangled bank, we are tempted to attribute their proportional numbers and kinds to what we call chance. But how false a view is this! Every one has heard that when an American forest is cut down, a very different vegetation springs up; but it has been observed that the trees now growing on the ancient Indian mounds, in the Southern United States, display the same beautiful diversity and proportion of kinds as in the surrounding virgin forests. What a struggle between the several kinds of trees must here have gone on during long centuries, each annually scattering its seeds by the thousand; what war between insect and insect—between insects, snails, and other animals with birds and beasts of prey—all striving to increase, and all feeding on each other or on the trees or their seeds and seedlings, or on the other plants which first clothed the ground and thus checked the growth of the trees! Throw up a handful of feathers, and all must fall to the ground according to definite laws; but how simple is this problem compared to the action and reaction of the innumerable plants and animals which have determined, in the course of centuries, the proportional numbers and kinds of trees now growing on the old Indian ruins!

  But the same patterns do not always recur from adjacent starting points colonized by the same set of species. Even the most apparently predictable patterns of supposedly established orders may fail. Remove the lobsters from waters around one South African island, and a new equilibrium may quickly emerge—one that actively excludes lobsters by converting their former prey into a ganging posse of predators!

  Thus, I sense a challenge in these four cases, a message perhaps deeper than the raw peculiarity of their phenomenology—and the resulting attack upon our dualistic and hierarchical categories. We do not yet know the rules of composition for ecosystems. We do not even know if rules exist in the usual sense. I am tempted, therefore, to close with the famous words that D’Arcy Thompson wrote to signify our ignorance of the microscopic world (Growth and Form, 1942 edition). We are not quite so uninformed about the rules of composition for ecosystems, but what a stark challenge and what an inspiration to go forth: “We have come to the edge of a world of which we have no experience, and where all our preconceptions must be recast.”

  BIBLIOGRAPHY

  Bahn, P. G. and J. Vertut. 1988. Images of the Ice Age. New York: Facts on File.

  Barber, L. 1980. The Heyday of Natural History. Garden City, N.Y.: Doubleday.

  Barkai, A., and C. McQuaid. 1988. “Predator-Prey Role Reversal in a Marine Benthic Ecosystem.” Science 242: 62–64.

  Barnosky, A. 1985. “Taphonomy and Herd Structure of the Extinct Irish Elk Megaloceras giganteus.” Science 228: 340–44.

  Barnosky, A. 1986. “The Great Horned Giants of Ireland: The Irish Elk.” Carnegie Magazine 58: 22–29.

  Boyle, R. 1661. The Sceptical Chymist. London: J. Cadwell.

  Boyle, R. 1688. A Disquisition About the Final Causes of Natural Things. London: H. C. for John Taylor.

  Brace, C. L. 1977. Human Evolution. 2nd ed. New York: Macmillan.

  Brace, C. L. 1991. The Stages of Human Evolution. Englewood Cliffs, N.J.: Prentice Hall.

  Breuil, H. 1906. L’Evolution de la peinture et de la gravure sur murailles dans les cavernes ornées de l’age du renne. Paris: Congres Prehistorique de France.

  Breuil, H. 1952. Les Figures Incisées et Ponctuées de la Grotte de Kiantapo. Belgium: Musée Royal du Congo Belge.

  Brooks, W. K. 1889. “The Lucayan Indians.” Popular Science Monthly 36: 88–98.

  Brooks, W. K. 1889. “On the Lucayan Indians.” Memoirs of the National Academy of Sciences 4: 2, 213–23.

  Brown, L., and D. Amadon. 1968. Eagles, Hawks, and Falcons of the World. New York: McGraw-Hill.

  Buffon, G. 1752. Histoire Naturelle. Paris.

  Burkholder, J. M., E. J. Noga, C. H. Hobbs, and H. B. Glassgow Jr. 1992. “New ‘Phantom’ Dinoflagellate Is the Causative Agent of Major Estuarine Fish Kills.” Nature 358: 407–10.

  Chambers, R. 1853. A Biographical Dictionary of Eminent Scotsmen. Glasgow: Blackie.

  Chauvet, J. 1996. Chauvet Cave: The Discovery of the World’s Oldest Paintings. London: Thames and Hudson.

  Clutton-Brock, T. 1982. “The Functions of Antlers.” Behavior 79: 108–25.

  Coe, M. D. 1992. Breaking the Maya Code. New York: Thames and Hudson.

  Cuvier, G. 1812. Recherches sur les ossemens fossiles. Paris: Deterville.

  Dagg, A., and J. B. Foster. 1976. The Giraffe: Its Biology, Behavior, and Ecology. New York: Van Nostrand Reinhold Co.

  Dana, J. D. 1852–55. Crustacea. Philadelphia: C. Sherman.

  Dana, J. D. 1857. Thoughts on Species. Philadelphia.

  Dana, J. D. 1863. “On Parallel Relations of the Classes of Vertebrates, and on Some Characteristics of the Reptilian Birds.” American Journal of Science 36:315–21.

  Dana, J. D. 1863–76. “The Classification of Animals Based on the Principle of Cephalization.” American Journal of Science, 1863, 36:321–52, 440–41; 1864, 37:10–33, 157–83; 1866, 41: 163–74; 1876, 12: 245–51.

  Dana, J. D. 1872. Corals and Coral Islands. New York: Dodd & Mead.

  Dana, J. D. 1876. Manual of Geology. 2nd ed. New York: Ivision, Blakeman, Taylor and Company.

  Darwin, C. 1842. The Structure and Distribution of Coral Reefs. London.

  Darwin, C. 1851–54. “A Monograph on the Fossil Cirripedes of Great Britain. (Lepadidae, Balanidae, Verrucidae).” London: Palaeontographical Society.

  Darwin, C. 1859. On the Origin of Species. London: John Murray.

  Darwin, C. 1868. The Variation of Animals and Plants Under Domestication. London: John Murray.

  Darwin, C. 1881. The Formation of Vegetable Mould Through the Action of Worms. London: John Murray.

  De Robertis, E. M., and Y. Sasai. 1996. “A Common Plan for Dorsoventral Patterning in Bilateria.” Nature 380: 37–40.

  Delage, Y. 1884. Evolution de la Sacculine (Sacculina Carcini Thomps): Crustace endoparasite de l’ordre nouveau des Kentrogonides. Paris: Centre National de la Recherche Scientifique.

  Dickens, C. 1859–1895. All the Year Round. London: Chapman and Hall.

  Dickens, C. 1865. Our Mutual Friend. Philadelphia: T. B. Peterson & Brothers.

  Dimery, N. J., R. McN. Alexander and K. A. Deyst. 1985. “Mechanics of the Ligamentum Nuchae of Some Artiodactyls.” Journal of Zoology 206: 341–51.

  Du Chaillu, P. B. 1861. Explorations and Adventures in Equatorial Africa. London: John Murray.

  Egerton, J. 1995. Turner: The Fighting Temeraire. London: National Gallery Publications.

  Farago, C. 1996. Leonardo da Vinci: Codex Leicester: A Masterpiece of Science. New York: American Museum of Natural History.

  Figuier, L. 1863. La Terre Avant la Deluge. Paris: Hachette.

  François, V. and E. Bier. 1995. “The Xenopus chordin and the Drosophila short gastrulation Genes Encode Homologous Proteins Functioning in Dorsal-Ventral Axis Formation.” Cell 80: 19–20.

  François, V., M. Solloway, J. W. O’Neill, H. Emery, and E. Bier. 1994. “Dorsal-Ventral Patterning of the Drosophila Embryo Depends on a Putative Negative Growth Factor Encoded by the short gastrulation Gene. Genes and Development 8: 2602–26.

  Gaskell, W. H. 1908. The Origin of Vertebrates. London: Longmans, Green and Co.

  Geoffroy St. Hilaire, E. 1822. “Considérations générales sur la vertèbre.” Paris, Memoires du Museum National D’Histoire Naturelle 9: 89–119.

  Gerace, D. T., ed. 1987. “Columbus and His World.” San Salvador, Bahamian Field Station. Fort Lauderdale: The Station.

  Glenner, H., and J. T. Høeg. 1995. “A New Motile, Multicellular Stage Involved in Host Invasion by Parasitic Barnacles (Rhizocephala).” Nature 377: 147–50.

  Goffart, M. 1971. Function and Form in the Sloth. New York: Pergamon Press.

  Gosse, P. H. 1
856. The Aquarium: An Unveiling of the Wonders of the Deep Sea. 2nd ed. London: J. Van Voorst.

  Gould, S. J. 1965. “Is Uniformitarianism Necessary?” American Journal of Science 263: 223–28.

  Gould, S. J. 1974. “The Origin and Function of ‘Bizarre’ Structures: Antler Size and Skull Size in the ‘Irish Elk.’” Evolution 28: 191–220.

  Gould, S. J. 1977. Ontogeny and Phylogeny. Cambridge, Mass.: Belknap Press of Harvard University Press.

  Gould, S. J. 1986. “Knight Takes Bishop?” Natural History 95:5, 18–33.

  Gould, S. J. 1992. “Red in Tooth and Claw.” Natural History 101:11, 14–23.

  Gould, S. J. 1994. “Lucy on the Earth in Stasis.” Natural History 103:9, 12–20.

  Greenberg, J. 1983. “Poetic Justice in the Arizona Desert.” Science News 124:19, 293.

  Gross, C. G. 1993. “Hippocampus Minor and Man’s Place on Nature: A Case Study in the Social Construction of Neuroanatomy.” Hippocampus 3: 403–13.

  Hibberd, S. 1858. Rustic Adornments, 2nd ed. London: Groombridge and Sons.

  Hitching, F. 1983. The Neck of the Giraffe: Darwin, Evolution, and the New Biology. New York: New American Library.

  Høeg, J. T. 1985. “Cypris Settlement, Kentrogon Formation and Host Invasion in the Parasitic Barnacle Lernaeodiscus porcellanae (Muller) (Crustacea:Cirripedia: Rhizocephala).” Acta Zoologica 66: 1–45.

  Holley, S. A., P. D. Jackson, Y. Sasai, B. Lu, E. M. De Robertis, F. M. Hoffmann, and E. L. Ferguson. 1995. “A Conserved System for Dorsal-Ventral Patterning in Insects and Vertebrates Involving Sog and Chordin.” Nature 376: 249–53.

  Huxley, T. H. 1863. Evidence as to Man’s Place in Nature. New York: D. Appleton.

  Jackman, R., S. Nowicki, D. J. Aneshanslex, and T. Eisner. 1983. “Predatory Capture of Toads by Fly Larvae.” Science 222: 515–16.