A Fish Story

Natural History, Oct, 2001 by Adam Summers

The spiny puffer's means of defense is hard to swallow.

When alarmed, some toads and snakes puff themselves impressively. Hedgehogs, porcupines, and some Old World salamanders sport protective spines. But only the spiny puffer (Diodon holocanthus) combines inflation and pointy spikes in one spectacular defense mechanism.

Also called balloonfish, spiny puffers belong to the Tetraodontiformes, an order of fishes known for their strange structures and odd behaviors. The boxfish, for example, is an aquatic tank with two bony skeletons, one on the inside to support its innards and one on the outside to deter predators. And the massive, tailless ocean sunfish, another relative, is essentially a huge disk--consisting of head and torso--pushed along by a couple of fins.

Compared with creatures like these, the spiny puffer seems relatively normal when relaxed. But when threatened, the puffer undergoes a remarkable transformation, its body swelling until the fish is three times its usual size and has become a rigid, near-perfect sphere covered in spiky armor--not a good design for swimming but decidedly discouraging to attackers.

Beth Brainerd, of the University of Massachusetts, studies the biomechanical tricks the puffer uses to accomplish its swell feat. A more accurate name for this fish would be "pumper," because it inflates not by puffing itself up but by pumping water into its stomach (which has ceded its digestive function entirely to the intestine). The stomach expands to nearly a hundred times its original volume, an astonishing increase made possible by the stomach's being pleated, like a skirt. An amazing amount of material can be hidden away in pleats. Consider that a typical Scottish kilt is made from eight yards of tartan fabric, whereas the typical Scotsman is only about a yard around. And the pleats of a puffer's stomach are more extensive than those of a kilt: inside the largest pleats (each of which is about three millimeters wide) are smaller folds, with yet smaller folds inside each one, and so on, down to pleats so tiny that they can be seen only through a microscope.

As the puffer fills with water, the fish's spine, already slightly curved, bends into an upside-down U shape; and the liver, intestines, and other internal organs become squeezed between the fish's backbone and its rapidly expanding stomach.

Meanwhile, the fish's skin is pushed out, obscuring most of the puffer's features. Only the mouth--a cartoonish orifice containing heavy, crushing plates capable of pinching a human finger to the bone--remains unaffected.

The skin of a fully inflated puffer is stretched to one and a half times its resting length. But while the skin's elasticity accounts for the change in the volume of the fish, stiffness and strength are required to turn the creature into a rigid ball. For this the puffer again turns to pleats. Brainerd discovered that the spiny puffer's skin consists of two layers--a thin, elastic outer layer and a fibrous inner layer. This inner layer of skin is pleated and, when extended, quite stiff. So why bother with the outer elastic layer? To answer that, one need only picture a deflated, pleated puffer--it would be a rumpled, hydrodynamically impaired laughingstock.

The skin also helps deploy the puffer's armor. The scales of this fish have been modified into slender spikes, each on a tripod-shaped, bony base embedded in the skin. Normally the tripod lies on its side, with the spike flat against the skin, pointing backward. But when the fish puffs up, the stretched skin pulls two of the tripod's legs backward and one leg forward, snapping the spike upright. The three legs provide a secure base that blunts the force of anything pushing against the spike's sharp tip.

Peter Wainwright, an evolutionary physiologist at the University of California, Davis, has found clues to the origins of puffing in the triggerfish Balistes capriscus, a close relative of the spiny puffer. Triggerfishes feed on unusually well defended prey: spiny sea urchins. The fish's usual modus operandi is to shoot jets of water at the urchin's side until it rolls over, exposing its unprotected "belly" (actually its mouth, with which it grazes on the seafloor). The triggerfish uses the same muscles to blow water out of the stomach that the spiny puffer uses to pump water into it. Both fish first expand their mouths to draw in water, but the puffer then pumps the water into its stomach, while the triggerfish opens its mouth and pumps the water back out. Natural selection may have taken advantage of a pumping mechanism that had evolved for disabling prey--turning it inward and transforming it into a mechanism for self-inflation.

Adam Summers is an assistant professor of ecology and evolutionary biology at the University of California, Irvine.