Monitor Marathons

How one group of lizards turns a gasp into a gulp.

Story by Adam Summers   ~  Illustrations by Patricia J. Wynne

Making my way down a trail through rosemary scrub in Florida's central sandhills, I surprised a six-lined racerunner (Cnemidophorus sexlineatus, so named for the lines that run the length of its body) basking in a wheel rut. I gave chase and the lizard streaked off-easily keeping ahead of my stumbling run. For thirty yards the lizard churned through loose sand, before managing a darting escape under a shady bush. The sprint was impressive, particularly for a lizard less than a foot long, but what was even more amazing was that the lizard had to make its dash without taking a breath. The racerunner's mechanical systems for breathing and running are linked in such a way that the lizard can do one or the other, but not both.

Lungs in any animal are, of course, the site of oxygen and carbon dioxide exchange. But lungs themselves cannot draw air into an animal's body; they are really nothing more than stretchy bags that bring air into close proximity with blood. Lungs fill with air when the cavity housing them enlarges, enlarging the lungs as well; the resultant low gas pressure causes outside air to rush in. Mammals have two systems for ventilating the lungs. The rib muscles power one system: they expand the chest by lifting and rotating the long flat bones to which they attach. The diaphragm, a dome-shaped muscle between the lungs and the liver, powers the second system. It works by pulling the lung cavity rearwards, toward the tail. The diaphragm is a mammalian innovation. Crocodiles and alligators have independently evolved a muscle that pulls the liver backwards, also effectively inflating the lungs. But lizards and snakes lack any analogue to the diaphragm, and so they rely on their rib muscles alone to inflate their lungs.

David Carrier, a biomechanist at the University of Utah in Salt Lake City, observed that a lizard's rib muscles also play a vital role in locomotion: they stabilize the trunk, giving the forelimbs a steady platform from which to operate. But any locomotion also renders the rib muscles nearly useless for breathing; running makes them completely so. Studying the common green iguana (Iguana iguana), Carrier confirmed that the rib muscles are active during locomotion, and that the lizard holds its breath while sprinting.

Now, any athlete can tell you that holding your breath while running will seriously cut down on your endurance. So Carrier posited that lizards (not unlike me) are restricted to short bursts of anaerobic exercise (less than thirty seconds), followed by prolonged panting to pay back the oxygen debt. (An oxygen debt accrues when muscles work without oxygen; the result is that lactic acid accumulates, and it must be oxidized after the work is done.)

Carrier's hypothesis was controversial, particularly among respiratory physiologists. Other investigators had discovered that monitor lizards-a distant relative of Carrier's iguana-have high metabolic rates. That is, unlike most so-called cold-blooded animals, monitors burn a lot of energy rapidly. A good example is the savannah monitor (Varanus exanthematicus), an African monitor lizard weighing about ten pounds, which spends most of its day patrolling its territory for tasty insects. Its oxygen consumption is as high as that of such mammals as the armadillo, and so the monitor can't afford to hold its breath while moving. On the contrary, the animal should ventilate as often and as vigorously as a metabolically equivalent mammal. But if the lizard can't rely on its rib muscles to breathe while it walks, how does the monitor spend all day walking?

The resolution to this apparent paradox required the joint efforts of physiologists and biomechanists. Tomasz Owerkowicz of Harvard University and Beth Brainerd of the University of Massachusetts at Amherst trained savannah monitors to trot on a treadmill in front of an X-ray machine coupled to a video camera. The X-ray movies demonstrated that, as Carrier had predicted, when the animal ran relatively fast, respiration relying on the subatmospheric pressures generated by expansion of the rib cage was supplanted by a different method of breathing. Long, thin bones below the tongue and in the neck seemed to be causing the lizard's throat and the floor of its mouth to expand and contract: the animal was "gulping" air on the run.

Most lizards are like a clumsy person who can't walk and chew gum at the same time; the lizards' handicap, though, is that they can't breathe and run simultaneously. Their rib muscles, which expand the chest during each breath, must also brace the forelimbs during locomotion-especially running. The peripatetic monitor lizards have evolved an alternate route to get air into their lungs. As an animal moves (1), muscles attached to the hyobranchial apparatus (a collection of bones in the lizard's throat) depress the structure, expanding its gullet (2). Air flows into the cavity created; the lizard then closes its mouth and nares (3), and constricts its throat (4), pumping the air into its lungs.

This kind of lung ventilation, well known in frogs and salamanders, is called gular pumping [see illustration]. In fact, the use of head muscles rather than trunk muscles to power respiration predates the evolution of lungs. Fish, for example, pump water across their gills with their head muscles. But until the work of Owerkowicz and Brainerd, gular pumping had not been considered an important factor for lung ventilation in reptiles.

To show that gular pumping is the key to the monitor's endurance, Brainerd and Owerkowicz took a group of treadmill-trained lizards on a road trip to the University of California, Irvine. There, together with the physiologists James W. Hicks and Colleen Farmer, they custom-fitted the animals with small face masks, which enabled the biologists to measure the lizards' oxygen consumption while the animals ran a treadmill. First each lizard ran normally; then a plastic tube was inserted into the mouth to keep the animal's mouth open and prevent gular pumping. And sure enough, when the gular pumping was eliminated, the monitor lizards acted more like Carrier's green iguanas.

Gular pumping has turned out to be far more widespread in lizards than physiologists had previously thought. The monitors, though, with their high metabolic rate, rely on it more than their relatives do. For most other lizards, the drill remains: dash and pant, dash and pant . . . just like me.

Adam Summers (asummers@uci.edu) is an assistant professor of ecology and evolutionary biology at the University of California, Irvine.