The Flamingo’s Smile

by Stephen Jay Gould

  If Alvarez’s asteroid was the external prod to cohesion, this book has an internal theme as well. It is no particular secret that I have spent the last few years fighting cancer. My disease was diagnosed just a week after the last volume went to the printers. This book becomes, therefore, a kind of roman à clef (complete, I hope) to a personal odyssey. Essay 19, “The Hottentot Venus,” was the first piece I wrote as a member of this largest involuntary club—and its last line was my touché. When arranged in their order of appearance in Natural History, these essays may trace an emotional journey (though I do not choose to pursue the analysis). I will only say that some essays are spare in their exegetical style of commentary on single historical texts (for I couldn’t reach the libraries for my usual ramblings, and several nights with a beautiful old book were such a solace), while others are downright baroque in their patchwork of detail (my simple joy in being able once again).

  I dare not even try to express my thanks to those who supported me through all this; the words do not exist in any language. But to those who know me only through these essays, and who took time to tell me that they cared, my special gratitude; it mattered in the most palpable way. I dwelled on many things—that I simply had to see my children grow up, that it would be perverse to come this close to the millennium and then blow it. I hope that it won’t sound corny if I thank nature too—in the context of the plodding regularity of these essays. Who can surpass me in the good fortune they supply; every month is a new adventure—in learning and expression. I could only say with the most fierce resolution: “Not yet Lord, not yet.” I could not dent the richness in a hundred lifetimes, but I simply must have a look at a few more of those pretty pebbles.

  1 | Zoonomia (and Exceptions)

  1 | The Flamingo’s Smile

  BUFFALO BILL played his designated role in reducing the American bison from an estimated population of 60 million to near extinction. In 1867, under a contract to provide food for railroad crews, he and his men killed 4,280 animals in just eight months. His slaughter may have been indiscriminate, but the resulting beef was not wasted. Other despoilers of our natural heritage killed bison with even greater abandon, removed the tongue only (considered a great delicacy in some quarters), and left the rest of the carcass to rot.

  Tongues have figured before in the sad annals of human rapacity. The first examples date from those infamous episodes of gastronomical gluttony—the orgies of Roman emperors. Mr. Stanley, Gilbert’s “modern major general,” could “quote in elegiacs all the crimes of Heliogabalus” (before demonstrating his mathematical skills, in order to cadge a rhyme, by mastering “peculiarities parabolous” in the study of conic sections). Among his other crimes, the licentious teen-aged emperor presided at banquets featuring plates heaped with flamingo tongues. Suetonius tells us that the emperor Vitcllius served a gigantic concoction called the Shield of Minerva and made of parrot-fish livers, peacock and pheasant brains, lamprey guts and flamingo tongues, all “fetched in large ships of war, as far as from the Carpathian sea and the Spanish straights.”

  Lampreys and parrot fishes (though not without beauty) have rarely evoked great sympathy. But flamingos, those elegant birds of brilliant red (as their name proclaims), have inspired passionate support from the poets of ancient Rome to the efforts of modern conservationists. In one of his most poignant couplets, Martial castigated the gluttony of his emperors (circa 80 A.D.) by speculating about different scenarios, had the flamingo’s tongue been gifted with song like the nightingale’s, rather than simple good taste:

  Dat mihi penna rubens nomen; sed lingua gulosis

  Nostra sapit: quid, si garrula lingua foret?

  (My red wing gives me my name, but epicures regard my tongue as tasty. But what if my tongue could sing?)

  Most birds have skinny pointed tongues, scarcely fit for an emperor, even in large quantities. The flamingo, much to its later and unanticipated sorrow, evolved a large, soft, fleshy tongue. Why?

  Flamingos have developed a surpassingly rare mode of feeding, unique among birds and evolved by very few other vertebrates. Their bills are lined with numerous, complex rows of horny lamellae—filters that work like the whalebone plates of giant baleen whales. Flamingos are commonly misportrayed as denizens of lush tropical islands—something amusing to watch while you sip your rum and coke on the casino veranda. In fact, they dwell in one of the world’s harshest habitats—shallow hypersaline lakes. Few creatures can tolerate the unusual environments of these saline deserts. Those that thrive can, in the absence of competitors, build their populations to enormous numbers. Hypersaline lakes therefore provide predators with ideal conditions for evolving a strategy of filter feeding—few types of potential prey, available in large numbers and at essentially uniform size. Phoenicopterus ruber, the greater flamingo (and most familiar species of our zoos and conservation areas in the Bahamas and Bonaire), filters prey in the predominant range of an inch or so—small mollusks, crustacea, and insect larvae, for example. But Phoeniconaias minor, the lesser flamingo, has filters so dense and efficient that they segregate cells of blue-green algae and diatoms with diameters of 0.02 to 0.1 mm.

  Flamingos pass water through their bill filters in two ways (as documented by Penelope M. Jenkin in her classic article of 1957): either by swinging their heads back and forth, permitting the water to flow passively through, or by the usual and more efficient system that inspired the Roman gluttons—an active pump maintained by a large and powerful tongue. The tongue fills a large channel in the lower beak. It moves rapidly back and forth, up to four times a second, drawing water through the filters on the backwards pull and expelling it on the forward drive. The tongue’s surface also sports numerous denticles that scrape the collected food from the filters (just as whales collect krill from their baleen plates).

  The extensive literature on feeding in flamingos has highlighted the unique filters—and often neglected another, intimately related, feature equally remarkable and long appreciated by the great naturalists. Flamingos feed with their heads upside down. They stand in shallow water and swing their heads down to the level of their feet, subtly adjusting the head’s position by lengthening or shortening the s-curve of the neck. This motion naturally turns the head upside down, and the bills therefore reverse their conventional roles in feeding. The anatomical upper bill of the flamingo lies beneath and serves, functionally, as a lower jaw. The anatomical lower bill stands uppermost, in the position assumed by upper bills in nearly all other birds.

  With this curious reversal, we finally reach the theme of this essay: Has this unusual behavior led to any changes of form and, if so, what and how? Darwin’s theory, as a statement about adaptation to immediate environments (not general progress or global direction), predicts that form should follow function to establish good fit for peculiar life styles. In short, we might suspect that the flamingo’s upper bill, working functionally as a lower jaw, would evolve to approximate, or even mimic, the usual form of a bird’s lower jaw (and vice versa for the anatomical lower, and functionally upper, beak). Has such a change occurred?

  The enigmatic smile of a swan—or is it?

  Nature harbors a large suite of oddities so special that we scarcely know what to predict. But, in this case, we encounter a precise reversal of anatomy and usual function—leading to a definite expectation: upside-down animals should reorient the form of their bodies to a new function when current behavior and conventional anatomy conflict.

  We may begin by sparing the usual pontification (but only for a while) and looking at a picture. If this picture excites a vague feeling of familiarity slightly awry, your perceptions are acute, but ride with me for a while.

  We seem to see a long-necked swan with a broad smile. But look carefully, for details betray this impossible beast. Its mouth opens above the eyes; its feathers run the wrong way; and where are its legs? I now show you the celebrated original in its proper orientation (and with the legs restored)—the flamingo from J.J. Audubon’s Birds
of America, and a sure entry on anyone’s hit parade of most famous pictures in natural history.

  This dramatic perceptual switch from happy swan to haughty flamingo recalls any standard item in the psychological arsenal of optical illusion—particularly the young well-dressed lady looking away who becomes the old hag in profile. In fact, any accurately executed picture of a flamingo produces the same jolting effect when viewed upside down (I have checked all historically important portraits)—and for an obvious reason. The jaws have evolved to fit their reversed function. The flamingo’s upper jaw does look like a typical bird’s lower bill, and we therefore see the upside-down flamingo not as an absurdity, but as an only slightly odd swan-like bird.

  The morphological alterations extend far beyond the changes in external form that produce such a striking perceptual shift from upright flamingo to inverted “swan.” But note first the peculiar curve of the beak itself. The flamingo’s bill projects out from its face, but then makes a sharp angular turn, producing the pronounced hump that looks like a trough (and works like one) when inverted for feeding. Some Near Eastern peoples call flamingos “camels of the sea,” not because the inclined bill recalls the hump on a camel’s back, but because it mimics the bend of the nose that imparts an inappropriate (but unshakable) impression of haughtiness to both animals (see my essay on the history of Mickey Mouse and the messages accidentally conveyed by facial features of animals—essay 9 in The Panda’s Thumb). Turned upside down, the hump becomes a grin as a smiling “swan” replaces the haughty flamingo.

  The famous flamingo, FROM J.J. AUDUBON’S Birds of America.

  The bills are elaborately adapted to their reversed roles, not simply bent in the middle for proper reorientation. First, relative sizes have been rearranged to complement the shapes. The upper bill is small and shallow, the lower deep and massive. (In most birds, the smaller lower bill moves up and down against the larger upper beak.) Second, the flamingo’s lower bill (functionally upper in feeding) has evolved unusual rigidity. The bones of each half (or ramus, in technical parlance) are tightly fused, and the rami themselves are then bonded extensively to each other. The lower bill is massive and well braced. The tongue runs fore and aft in a deep trough cut into the lower jaw. (Remember that filter feeding serves as a coordinating theme for all these changes—the upside-down feeding posture, the attendant alteration in size and shape of the bills, and the fat tongue that once almost sealed the flamingo’s fate.) Third, in most species of flamingo, the smaller upper jaw slots into a receiving space on the larger lower jaw, a reversal of the usual convention—lower jaw moving up and fitting into a larger upper bill.

  These complex, coordinated changes make a persuasive case, but they leave a missing piece, recognized as the key to flamingo peculiarities ever since Menippus recorded the first preserved speculation nearly 300 years before Martial’s plea: are movements also reversed to match the inversion of form?

  In most birds (and mammals, including us), the upper jaw fuses to the skull; chewing, biting, and shouting move the mobile lower jaw against this stable brace. If reversed feeding has converted the flamingo’s upper jaw into a working lower jaw in size and shape, then we must predict that, contrary to all anatomical custom, this upper beak moves up and down against a rigid lower jaw. The flamingo, in short, should feed by raising and lowering its upper jaw.

  With great credit to the clear thinking of our finest naturalists, I noted with pleasure in my readings that this central question has been continually posed as paramount for more than 2,000 years—by scientists of many cultures and through all the vicissitudes of theory and practice that have marked the history of biology. Georges Buffon, the greatest of all synoptic naturalists, began his mid-eighteenth-century essay on flamingos by admitting the fame of their red color, while maintaining that the odd form of their beak posed a problem of even greater interest: “This fiery color is not the only striking character displayed by this bird. Its beak has an extraordinary form, the upper bill flattened and strongly bent at its midpoint, the lower thick and well set, like a large spoon.” In short, and in his own lovely tongue, “une figure d’un beau bizarre et d’une forme distinguée.” Then, tracing the question right back to Menippus, Buffon stated the primum desideratum of flamingo studies—“to know if, in this singular beak, it is (as many naturalists have said) the upper part that moves, while the lower remains fixed and motionless.”

  Nehemiah Grew’s flamingo, 1681. The illustration accompanying the first important proposal that flamingos feed by moving their upper jaw up and down against their lower. Look at this figure upside down as well. FROM N. GREW, MUSAEUM REGALIS SOCIETATIS, 1681. REPRINTED FROM NATURAL HISTORY.

  The first extensive and explicit commentary had been offered in 1681 by Nehemiah Grew, the great English naturalist (known primarily for his early microscopical studies of plants). Cataloguing the collections of the Royal Society—in his Musaeum Regalis Societatis, or a catalogue and description of the natural and artificial rarities belonging to the Royal Society and presented at Gresham Colledge, whereunto is subjoined the comparative anatomy of stomachs and guts—he encountered a lone flamingo (see figure) and stated: “that wherein he is most remarkable, is his bill.” Grew suspected that the oddities of the bill would all be resolved if the upper beak moved against a stationary lower jaw. He stated that the “shape and bigness of the upper beak (which here, contrary to what it is in all other birds that I have seen, is thinner and far less than the nether) speaks it to be more fit for motion and to make the appulse and the nether to receive it.”

  Flamingos in their characteristic feeding pose—upside down. PHOTO BY D. PURCELL.

  The question was not fully resolved until Jenkin published her comprehensive paper in 1957—affirming with hard data the suspicions and good judgment of Menippus, Grew, and Buffon. In fact, flamingos (along with many other birds) have developed a highly mobile ball and socket joint between upper and lower jaws. The beaks therefore have great mobility, and each can move independently. In preening, either the upper or lower jaw may be opened and operated against the other. But, in feeding, the upper jaw usually drops and raises against a stationary lower jaw—just as the great naturalists had always expected.

  The flamingo’s flip-flop is complete and comprehensive—in form and motion. The shapes are overturned by bending, the sizes reversed, the slotting inverted, the buttressing transposed. The action, too, is topsy-turvy. A peculiar reversal in behavior has engendered a complex inversion of form. Evolution as adaptation to particular modes of life—Darwin’s vision—gains strength from an extreme test imposed by life upside down.

  But do flamingos just provide a funny example, or do they symbolize a generality? What about other creatures that live upside down? Consider another animal of shallow West Indian waters, the inverted jellyfish, Cassiopea xamachana (the unorthodox trivial name honors the Native American designation for the island of Jamaica).

  Cassiopea is an unconventional jellyfish in many ways. It grows neither marginal tentacles nor central mouth. Instead, eight fleshy and complexly branched “oral arms” (so called because each contains a separate mouth) emerge from a short and stout central stalk, itself attached to a usual jellyfish umbrella with a difference (see figure—a reproduction of the classical lithograph from Mayer’s 1910 monograph, Medusae of the World). The oral arms are crammed with symbiotic algal cells, a possible adaptive impetus for their elaborate branching (to provide light-capturing surfaces for the photosynthetic symbionts). Each oral arm harbors about forty oral vesicles—hollow sacs connected with the feeding canals and containing bags of nematocysts, or stinging cells, at their tips. The vesicles shoot their nematocysts at prey (mostly small crustaceans) in strings of mucus; the strings with their attached and paralyzed victims are then pulled into the oral mouths. (Yes, I was as amused as some of you by the redundant “oral mouth”—the zoological equivalent of pizza pie or AC current. This clumsy phrase arises as unfelicitous fallout from a prior decision t
o call the appendages “oral arms”—as a shortcut for “mouths of the oral arms.”)

  Cassiopea xamachana. Note concavity of bell’s upper surface and the raised muscular ring. Figure reproduced as presented (in the ecologically wrong right-side-up position). FROM MAYER. 1910. REPRINTED FROM NATURAL HISTORY.

  Cassiopea’s unusual anatomy matches its unconventional orientation and style of life. Ordinary, self-respecting jellyfish swim actively with their umbrellas uppermost and their arms and tentacles below. Cassiopea lies stationary on the bottom of shallow ponds and coastal areas—upside down. The top of its umbrella hugs the sediment and the oral arms wave above, waiting for small crustacea to enter their orbit. Sailors at Fort Jefferson in the Tortugas, where Cassiopea lined the docks, called them “moss cakes.” (Since Cassiopea can give a nasty sting, and since men in blue usually spice their language to match the stimulus, I wonder what the sailors really called them. But Mr. H.F. Perkins, writing in 1908 on the anatomy of Cassiopea, didn’t choose to tell us.)

  The umbrella of Cassiopea recalls the flamingo’s jaw in its adaptation to reversed life. The umbrella’s upper surface is smoothly convex in ordinary jellyfish, as hydrodynamic efficiency dictates. But the upper surface of Cassiopea’s umbrella (its functional lower surface for life upside down) is markedly concave—well suited to serve as a cupping device for gripping and holding the substrate.

  Cassiopea has made a second intriguing change for its unusual reversed life. Most jellyfish move through the water by contracting rings of concentric muscles that circle the outer portion of the umbrella. In Cassiopea, one of these muscle rings has been raised and accentuated, forming a continuous circular band surrounding the inner concavity. This raised rim operates together with the concave surface to form an efficient suction cup that keeps the “head” of this jellyfish in its proper position on the bottom. (Cassiopea can still swim, albeit weakly and inefficiently, in the conventional manner. If dislodged from the bottom, it will turn over and swim for a few pulsations before settling down again on its head.) Some scientists have also suggested that the pulsating contractions of the concentric muscles, ordinarily used in swimming, serve other important functions in Cassiopea’s attached, upside-down position—maintaining connection with the substrate by pushing the animal down and moving water currents with potential prey towards the oral arms. But these reasonable proposals have not been properly tested.