Leonardo’s Mountain of Clams and the Diet of Worms

by Stephen Jay Gould

  Take all this—nauplius; cyprid; kentrogon; injected passage into the host’s body, sometimes by a single cell; migration to a permanent site; reproduction of the rooted interna; and emergence of the externa. Stack up these stages against our own lives, even through all the Sturm und Drang of our teenage years, and which life cycle would you label as more “complex”?

  2. MANIPULATING AND COMMANDEERING THE HOST. The adult parasite may look like a rooted blob, but just as the most unprepossessing humans often hide immense power beneath their ordinary appearance (as many a Hollywood “toughie” has discovered to his great hurt and sorrow), beware of equating ugly wartiness with benign simplicity. The adult rhizocephalan parasite has more tricks up its nonexistent sleeve than externa appearance would suggest.

  Consider the following problem in logic as an indication of the physiological and behavioral sophistication that adult parasites must possess. We know that crabs fight back when the cyprid larvae try to settle, for potential hosts use their cleaning and grooming behaviors to remove the settling cyprids—and the great majority of potential parasites are thereby destroyed. In fact, the rapid transformation of exploring cyprid to cementing kentrogon (accomplished within ten minutes in some species), the low and hunkering shape of the kentrogon, and its firm cementation to the host in many species have all been interpreted—quite correctly in my view—as active adaptations by the parasite to vigorous counterattacks by potential hosts.

  But when the virgin externa pokes through the abdomen and lies flush against the crab’s underside, all “fight” has evaporated from the host. The crab still possesses an active cleaning response, but makes no attempt to remove the externa. Why not? What has happened to the crab? In a remarkable paper published in 1981 in the Journal of Crustacean Biology, authors Larry E. Ritchie and Jens T. Høeg answer these questions in studying the root-head species Lernaeodiscus porcellanae:

  The parasite returns to the surface as the externa. What keeps the host from recognizing it as foreign or “parasite” and destroying it, since the cleaning behavior is still available? When an externa appears on the surface of the host, it must either be in a position or of a form that cannot be removed by the host, or it must be perceived as “self” and not harmed in any way.

  Since the externa could presumably be reached and removed, the second and more interesting alternative probably applies. In other words, the parasite has somehow evolved to turn off the host’s defenses, presumably by disarming the crab’s immune response with some chemical trickery that fools the host into accepting the parasite as part of itself. The authors continue:

  The evolution of host control, probably through some form of hormonal action, represents the ultimate counterdefensive adaptation of the Rhizocephala, for it nullifies the host’s defense system . . . Once host control is achieved, the host is in the absolute service of the parasite.

  The phrase “absolute service” may sound extreme, but a compendium of parasitic devices for usurpation, takeover, and domination of the host can only elicit an eerie feeling of almost macabre respect for the unparalleled thoroughness (and cleverness) of parasitic management!

  First of all, the adult parasite castrates the host, not by directly eating the gonadal tissue (as in most cases of “parasitic castration,” a common phenomenon in this grisly world), but by some unknown mechanism probably involving penetration of the interna’s roots around and into the crab’s nervous system. In Sacculina (but not in most other rhizocephalans), the parasite also cuts off the host’s molting cycle, and the crab never again sheds its outer shell (an obvious benefit to the externa, which can easily be dislodged by molting).

  Lernaeodiscus porcellanae turns control of the host into a fine art. After castration by the parasite, male crabs develop female characteristics in both anatomy and behavior, while females become even more feminized. The emerging externa then takes the same form and position as the crab’s own egg mass (in normally developing uncastrated females)—attached to the underside of the abdomen. The crabs—both male and female (for both sexes are feminized by the parasite)—then treat the externa as their own brood. In other words, the parasite usurps all the complex care normally invested in the crab’s own progeny. Crabs ventilate the externa by waving their abdomens; they actively (and carefully) groom the externa with their cleaning limbs. Moreover, Ritchie and Høeg proved that this behavior may be indispensable for the externa’s survival—for when they removed the cleaning limbs from a parasitized crab, “the externa soon became fouled and necrotic.” Finally, the “simple” root-head even fools the crab into treating the release of parasite larvae from the externa as the discharge of her own fertilized eggs! Ritchie and Høeg write:

  When it is time for the parasite to release its larvae, the host assists by performing customary spawning behavior. Normally cryptic, [the crab] climbs out from under the rock, elevates the body on tiptoes, and then lowers and raises the abdomen in a waving action. Simultaneously, the parasite expels its nauplii into the current generated by the host.

  In short, rhizocephalans are the cuckoos of the marine invertebrate world—laying their eggs in another species’s “nest,” mimicking the host’s own eggs (similarity of the externa to the crab’s egg mass), and then eliciting parental care from the host. But rhizocephalans are even more thorough, for they always castrate their host, while only some cuckoos kill the legitimate nestlings of their foster parents.

  In short, the root-head turns the crab into a Darwinian cipher, a feeding machine working entirely in the parasite’s service. The castrated crab can make no contribution to its own evolutionary history; its “Darwinian fitness” has become flat zero. All feeding and growth now work in the evolutionary interest of the root-head, which continues to reproduce at a prodigious rate, entirely at the crab’s expense—as the interna’s roots drain the crab’s nutrition. But ever so carefully, for the parasite must maintain the crab in constant and perfect servitude—not draining the host enough to kill this golden goose, but not letting the crab do anything for its own Darwinian benefit, either.

  Root-heads can maintain this delicate balance for a long time. Ritchie and Høeg kept infested crabs for two years in the laboratory—with the parasites showing no ill effects and reproducing all the time. Moreover, the root-head can produce prodigious numbers of larvae—all supported by the crab’s feeding. In a 1984 article on Sacculina carcini, Jørgen Lützen found that a single externa, during a breeding season lasting from mid-July to October, can produce up to six batches of eggs, with an average of 200,000 per clutch—for a total of more than a million eggs per season. Complex indeed—and devilishly effective. If I were a conscious rhizocephalan, I would adopt this motto: Don’t call me a simple sac with roots.

  3. WHAT ABOUT MALES? (OR, FURTHER COMPLEXITY IN THE ROOT-HEAD LIFE CYCLE). These first two categories of complexity only consider the female root-head. Delage and all early students of rhizocephalans regarded the externa as a hermaphrodite, with both male and female organs. But the externa forms part of the adult female only. Male rhizocephalans were not well documented until the 1960s, when a group of Japanese zoologists finally worked out the full sexual system of rhizocephalans, and recognized the true nature of males.

  The male life cycle differs in a striking way from the development of females—another testimony to rhizocephalan complexity when we consider full biology rather than adult anatomy alone. The beginning stages of nauplius and cyprid differ little between the sexes. But whereas the female cyprid settles on a crab to begin the stage of internal penetration, the male cyprid alights instead on the female externa. In Sacculina and close relatives, the virgin externa contains no opening. But this initial externa soon molts to a second stage containing an orifice known as the “mantle aperture.” This opening leads into two passageways known as “cell receptacles.”

  Successful male cyprids settle on the externa’s aperture. A unique male stage, called the trichogon, then forms within the cyprid. The trichogon, clearly the h
omolog of the female kentrogon, but much simpler in form, has no muscles, appendages, nervous tissue, or sense organs. The trichogon looks like a small mass of undifferentiated cells surrounded by a cuticle covered with small spines (the name means “hairy larva”). The trichogon passes through the antennule of the cyprid, into the aperture of the externa, and down the passageway of the cell receptacle. (Two trichogons may successfully enter the externa, one in each receptacle.) The trichogon then sloughs the spiny cuticle and lodges as a small group of cells at the end of the passageway. (Other rhizocephalans form no trichogon; the male cell mass must then be injected through the cyprid antennule right into the body of the externa.) These tiny male cell masses become sources for the production of sperm.

  These facts may not warm the hearts of superannuated macho blusterers among humans, but male root-heads end up as tiny dwarfs, injected into the body of a vastly larger female, and finally coming to rest as a small mass of loosely connected cells deep inside the externa. Biologists refer to such males as hyperparasites—for they are parasitic upon a parasite. The female parasitizes a crab, but the tiny male depends entirely upon the female for nourishment. The male cells, permanently enclosed deep within the body of a relatively enormous and protective female (an odd kind of Freudian fantasy even for human males, I suppose), then spend their days producing sperm in synchrony with egg production by the externa.

  In summary, the intricate and different life cycles of both male and female root-heads, and the great behavioral sophistication shown by the female in reconfiguring a host crab as a support system, all underscore the myopia of our conventional wisdom in regarding rhizocephalans as degenerate parasites because the adult anatomy of internal roots and external sac seems so simple.

  This reassessment of root-heads forces me to revise my initial take on the lessons of parasites for correcting the bias of equating evolution with progress—for I can no longer hold that parasitic degeneration argues for a slight preponderance of simplification over complexification among evolutionary trends. But this correction leads to an even better argument against predictable progress—one that also takes us back to the roots of our intellectual heritage in Darwin’s ideas.

  In his famous 1880 essay Degeneration: A Chapter in Darwinism, E. Ray Lankester correctly identified belief in progress as the principal inference falsely drawn from Darwin’s theory of natural selection. Lankester wrote:

  Naturalists have hitherto assumed that the process of natural selection and survival of the fittest has invariably acted so as either to improve and elaborate the structure of all the organisms subject to it, or else has left them unchanged, exactly fitted to their conditions, maintained as it were in a state of balance. It has been held that there have been some six or seven great lines of descent . . . and that along each of these lines there has been always and continuously a progress—a change in the direction of greater elaboration.

  Lankester then cited supposed cases of degeneration, including root-heads as a primary example, to prove that natural selection does not guarantee such progress. “Degeneration,” he wrote, “may be defined as a gradual change of structure in which the organism becomes adapted to less varied and less complex conditions oflife.” Lankester, in other words, remains true to Darwin’s deeper principle that natural selection leads only to local adaptation, not to global progress. He correctly states that simplified conditions of life might lead, by natural selection, to less complex anatomies—and that these simplified descendants would be just as well adapted to their habitats as more complex ancestors to previously more elaborate modes of life. But Lankester erred in regarding root-heads as degenerate, forms properly responding to simplified conditions. An enlarged view of the entire root-head life cycle reveals great complexity and corresponding adaptation through several intricate phases of growth. The simple adult sac of the female externa tells only a tiny part of a fully elaborate tale.

  Rhizocephalans, instead, provide a superb example of Darwin’s genuine principle—the production of appropriate local adaptation by natural selection. Rhizocephalans are phenomenally well suited to their complex conditions of life. But in evolving their unique specializations, rhizocephalans did not become better (or worse) than any close relative. Are root-heads better than barnacles because they live in crabs rather than on rocks? Are they worse than barnacles because the adult female looks like a bag, rather than a set of gills enclosed in a complex shell? Is a crab better than a barnacle? Do we prefer seahorses over marlins, bats over aardvarks? Such questions are foolish and diversionary.

  Natural selection can only adapt each creature to its own local conditions—and such a mechanism therefore cannot serve as a rationale for our oldest and most pernicious prejudice of progress. Rhizocephalans derail the bias of progress not because they are degenerate, but because they are so well adapted and uniquely specialized to their own intricate series of lifetime environments—and how can we possibly rank all the disparate uniquenesses of the animal kingdom as cosmically better or worse? May this aid provided to our poor benighted intellects—not only their undoubted success in commandeering crabs for Darwinian advantage—represent the triumph of the root-heads.

  20

  CAN WE TRULY KNOW SLOTH AND RAPACITY?

  THE CLASSIC GENERALIZED STATEMENT OF A COMMON PROBLEM IN INTELLECTUAL and practical life may be found in Tennyson’s lament that his dearest (and deceased) friend Arthur Hallam seemed so close in loving memory, yet so unreachable in actuality:

  He seems so near, and yet so far.

  The classic particularized statement of the same problem describes Coleridge’s Ancient Mariner, adrift in an utterly unusable but completely enveloping bounty:

  Water, water, every where,

  Nor any drop to drink.

  The common experience of being so close that you can almost touch, yet so utterly distant by any available way of knowing, provides a decidedly mixed blessing—as both a primary frustration of daily life and a major prod to scientific advance. My favorite example has a largely happy ending still vigorously in progress; consider how much of medicine’s sorry history of so little advance over so many centuries (until very recently) arose primarily from a diagnostic problem involving only an inch or two. The trouble requiring visualization lies just below the opaque covering of our skin. Untold millions (probably billions) of premature, and often painful, deaths have occurred because no one could see a developing tumor or an internal source of infection. The old surgeons could do little more than cut it off or (on occasion) take it out—where “it” refers to something quite large (a limb, for example), removed in toto because a small and local lesion could not be pinpointed. Imagine, then, the triumphant benevolence of a host of inventions from X rays to CT scans to MRIs. The ability to see an inch or two inside has revolutionized our lives and greatly improved our prospects.

  Natural historians have dedicated themselves to the noble and fascinating task of trying to understand, in the deepest way accessible to us, the amazing variety of life on our planet. The best possible procedure immediately runs into Tennyson’s limit of proximity with impossibility. I go eyeball to eyeball with some other creature—and I yearn to know the essential quality of its markedly different vitality. I cry to God the Gatekeeper of scientific knowability: Give me one minute—just one minute—inside the skin of this creature. Hook me for just sixty seconds to the perceptual and conceptual apparatus of this other being—and then I will know what natural historians have sought through the ages.

  But this god stays as silent as Baal, who would not answer the loud and fervent pleas of his 450 prophets, even when Elijah mocked them for the impotence of their deity. I can only look from the outside (or cut into the inside, but flesh and genes do not reveal organic totality). I am stuck with a panoply of ineluctably indirect methods—some very sophisticated to be sure. I can anatomize, experiment, and infer. I can record reams of data about behaviors and responses. But if I could be a beetle or a bacillus for that one precious mi
nute—and live to tell the tale in perfect memory—then I might truly fulfill Darwin’s dictum penned into an early notebook containing the first flowering of his evolutionary ideas during the late 1830s: “He who understands baboon would do more towards metaphysics than Locke.”

  Instead, we can only peer in from the outside, look our subject straight in the face, and wonder, ever wonder. Still, considering how far our methods must lie from the unreachable optimality of dwelling within, we have managed pretty well in a world without metempsychosis. Our indirect methods have taught us a mountain of things about horses, but if you wished to learn even more, wouldn’t you rather be Whirlaway in the stretch, than interview Eddie Arcaro afterwards?

  I came face to face (many times) with this old paradox during a recent trip to Costa Rica, a nation justly celebrated for its maximal attention among poor and tropical lands to the health and preservation of remaining natural environments—a position not only ethically correct, but also potentially profitable both to a nation itself, and to all of us. Two Costa Rican animals cast a particularly enigmatic stare at me, and elicited the old frustrating thought that if I could only get inside their different world for a minute, I might understand. Small mammals and insects strike us as frenetic; some reptiles and amphibians seem overcome with torpor. But we are not overwhelmed with the difference, if only because all these creatures vary their routines and paces: a squirrel can sit rigidly still, while an “immobile” frog catches insects on a lightning tongue.