 December 2002/January 2003 |
Dry, Dry Again
To survive in its desert home, the tortoise of the American
Southwest must tolerate immense swings in its body chemistry.
By Kenneth A. Nagy
|
|
Animals that persist in such arid regions do so largely because they are able to maintain a constant internal environment in the face of harsh and changing external conditions. In most vertebrates, when body temperature, water and salt concentrations, or a host of other factors stray from their optimum levels, regulatory mechanisms kick in to reestablish internal equilibrium. The cells of many mammals, for instance, live in a water-based solution that must be kept at relatively unvarying conditions of temperature, pH, and osmotic pressure with respect to the surrounding environment. The cell's internal chemical stability is maintained despite changing rates of nutrient input and waste output, as well as changing concentrations of dissolved minerals in the fluid surrounding the cell. This complex internal balancing act gets repeated above the cellular level as well, because tissues and organs, too, can function efficiently only within a narrow range of conditions. The general process of maintaining equilibrium in the body is called homeostasis.
Among vertebrates, mammals and birds are the masters of homeostasis. They are endotherms, or warm-blooded animals, generating their own body heat, and they can finely tune the thermal, water, and chemical balance of their bodies from minute to minute. That fine-tuning, and the self-containment it makes possible, has enabled mammals and birds to occupy many of the habitats on Earth, including deserts.
Reptiles, in contrast, tend to respond more slowly to environmental changes than endotherms do, and their physiological adjustments are less precise. As ectotherms, or cold-blooded animals, most desert reptiles control their body temperature, for instance, by basking on a sun-warmed rock in the morning and seeking shade at noon. The method is energy-efficient, but it also affords less exact and less continuous control over temperature than does the internal furnace of mammals.
But most reptiles don't really “go with the flow” and allow their body composition to change when their surroundings vary. They maintain chemical homeostasis nearly as well as birds and mammals do. That, of course, consumes resources, and suggests that even in a resource-poor environment such as the desert, internal stability is well worth the relatively expensive homeostatic lifestyle. Yet life is always on the lookout for an open niche; it would be surprising indeed if every form of vertebrate life showed blind devotion to the homeostatic dogma. Two species of reptile—the ornate dragon, a lizard of western Australian deserts, and Gopherus agassizii, the desert tortoise of the Mojave—are known to tolerate wide swings in their internal biochemistry. And the desert tortoise stands alone in appearing, at times, to abandon homeostasis altogether.
The desert tortoise begins the year in a state of hibernation, “sleeping” from roughly November through February in a slanting burrow dug three to six feet deep in sandy soil. The burrow provides the tortoise with a relatively humid and cool, but not freezing, microhabitat during winter. A hibernating tortoise burns little energy from its store of fat, and the humid air in the burrow keeps the animal from dehydrating.
In decades of fieldwork, my students and I have followed more than a hundred tortoises—some for as long as five years—at four study sites across the Mojave Desert. By tagging individuals with miniature radio transmitters, we discovered that the tortoises often hibernate in the same burrow over several years. We also determined that most tortoises weigh roughly as much after hibernation as they did when they entered their burrows the preceding fall—about six and a half pounds for an average middle-aged (thirty- to forty-year-old) adult. Their constant weight attests to their amazing ability to conserve both water and energy over the winter—a key factor in their survival.
Imagine now that you are a vegetarian tortoise in the Mojave Desert, and you have to depend solely on the plants around you (mostly the annuals) for all of your nutritional needs, including water. The Mojave is green only every other year or so, when enough winter rain has fallen. Even then, new plant growth lasts only from February to mid-May. During long dry periods nothing grows for two or even three years, and the desert becomes dry and brown. In such conditions, your survival depends on having a “relaxed” homeostasis—in this case, a high tolerance for nutritional stress. My students and I have often been surprised to find tortoises active even when no green food is available.
In March, rousing yourself from hibernation, you emerge from your burrow and begin to eat. If the winter rains have been kind, your menu can include desert dandelion, evening primrose, bristly langlosia, and other succulent young wildflowers. Such a diet is easy to digest, and it provides you with more than enough protein, water, and minerals to meet your immediate needs. But rather than excreting the excess in urine, as would most other animals, you retain it. That water, which can be reabsorbed as needed through your bladder wall, will carry you through the inevitable dry periods later in the year. When your internal “canteen” is full, it makes up as much as 30 percent of your total body weight.
In good—that is, rainy—springs you gain weight, but at the same time you may be slowly losing body fat. Succulent greens can contain so much water that a stomach full of food holds fewer calories than you burn while moving around the desert. Even when the spring desert is a flower garden, it's more important to store extra water and protein for the stresses ahead than to sustain perfect nutritional balance. You simply make up for the energy deficit by burning stored fat.
The green season, if it has come at all, lasts only until mid-May, and by June the desert plants have mostly wilted and died. For a while, you continue to devour the dry grasses, but you also retreat more often into your burrow to escape the heat and dryness. By this time, the extra water you gained in the spring has been lost through defecation and respiration. But you still don't empty your bladder, and the concentrations of dissolved mineral salts (mainly potassium, sodium, and chloride ions) absorbed from your food are building up in the scant liquid that is not reabsorbed by your body. Unlike marine turtles and many desert lizards, you have no specialized glands that help you get rid of extra salts. So your “canteen” becomes packed with excess salts and waste uric acid and urea, but holds relatively little water.
If you continue to lose water—but not salts or other dissolved substances—by respiratory evaporation, and if the osmotic concentration of salts and other wastes in your urine reaches the osmotic concentration in your blood, the concentrations in your blood and urine will begin to increase together. By the time the full-blown summer drought hits, you are spending nearly all your time underground, dropping any pretensions to maintaining osmotic homeostasis. All you can do is hunker down in your burrow, enduring internal concentrations of chemicals well beyond those that would kill any mammal or bird and nearly all other reptiles.
How do we know all this? One of the goals of our research is to account for all the water the tortoise obtains, uses, and retains. The basic technique is to label the tortoise's body water by injecting it with “heavy” water, which is made up chemically of heavy isotopes of hydrogen or oxygen. Heavy water acts like ordinary water to the tortoise, but for us it tags any water it mixes with and tells us the volume of water in the animal by the principle of dilution. When we recapture the tortoise weeks or months later, we measure the rate of isotope loss from its body water over time, which tells us its rate of water gain and rate of water loss. Charles C. Peterson, a physiologist at the College of New Jersey in Ewing, and others have found that dehydrated desert tortoises can survive with osmotic concentrations in their blood as much as 200 percent greater than those of well-watered tortoises. People and many other mammals are in trouble if dehydration raises blood osmotic concentration by as little as 8 percent. Even desert camels can tolerate only an increase of 40 percent.
If the summer and fall remain dry, tortoises stay in their burrows and go directly into hibernation in October, without having eaten any food since early summer. If it rains, however, they rouse themselves and emerge en masse to drink copiously and replenish their “canteens.” No one knows how tortoises, while still in their burrows, realize that it is about to rain. Philip A. Medica, a biologist at the U.S. Fish and Wildlife Service in Las Vegas, observed some tortoises emerge from their burrows as a summer thunderstorm approached. The tortoises scraped out shallow depressions in the soil, which caught the rain. Then more tortoises emerged, put their faces into the puddles, and sucked the water in through their noses and mouths for long periods.
If the tortoises get a chance to drink their fill before the onset of winter's hibernation, they will finally discharge the old urine they have been holding since the preceding winter or spring. Then they drink some more. In a day or two their osmotic concentrations are back to normal, their bladders are full of clear, dilute urine, and they resume feeding, mainly on dry grasses left over from spring.
When the weather is dry, the tortoises can take in extra calories and build up fat deposits rapidly. Because they consume so much more plant matter per stomachful of food on the dry diet of summer and fall than they do on the wet spring diet, the tortoises can store more energy than they burn. But there is a downside. Dry grasses contain salts but little protein or water, and so once again the tortoises' chemistry falls out of balance.
To tolerate all the chemical seesawing in the course of a year, tortoises orchestrate a distinct brand of chemical management. They do not balance their nutrient budgets day to day, as endotherms do, or even week to week; their schedule is an annual one. But if no rains fall during the warm seasons and the tortoises don't get a chance to drink, they will enter hibernation dehydrated, malnourished, and with a bladder full of toxic waste. Some tortoises may perish in hibernation after a dry year, and multiyear droughts can be particularly deadly. During a prolonged dry spell at one of Peterson's study sites, many tortoises died, apparently from lack of food and water.
In spite of near-constant challenges to their survival, tortoises must nonetheless attend to the task of perpetuating the species. Males, always interested in sex, court females throughout the spring and summer. (Although desert tortoises usually hibernate alone, a male may try to “body block” a female into a burrow for the winter, thereby gaining exclusive access to her when it's time to emerge for spring breeding.) Males contribute only sperm, which is easy to produce. Females, however, must generate much more organic material in the form of eggs, and that requires more resources.
In good, wet years females may have little difficulty finding food that provides them with enough water, energy, and protein to produce eggs. In May or June they normally lay about seven eggs, which are deposited in shallow holes dug just inside the burrows. Even in lean years, though, many females still manage to lay three or four eggs, as Brian T. Henen, a physiologist at the University of the Western Cape in Cape Town, South Africa, has discovered. Thus, instead of skipping reproduction for a year, as some other desert reptiles and birds do, female tortoises sacrifice their own body stores of proteins, fats, and water—the very materials on which their own survival may depend—to reproduce.
How might such a seemingly unfavorable reproductive option have evolved? One possible explanation is that natural selection has favored the descendants of female tortoises that hedged their bets. Producing eggs takes time, and so female tortoises must begin the reproductive sequence of events for the year in the early spring. Yet if the offspring are to survive, the eggs need somewhat moist sand in summer, and the young need green food and perhaps a drink of water in the fall, before they enter their first hibernation. But the vagaries of the desert climate make it impossible to predict when rains will occur. The females can't know in early spring whether or not the energy they spend in reproduction is likely to pay off in surviving babies. So they risk their own well-being every year on the gamble that rain will soon come, and that their hatchlings will emerge from the burrows into conditions conducive to feeding and growth.
Once she lays and buries her eggs, the female desert tortoise is finished with her parental role. She has, however, provisioned each egg with a grubstake: a substantial amount of nourishing yolk, which, soon after the egg hatches, is safely enclosed in the baby's gut. The energy and water in the yolk lasts for weeks, giving the hatchling time to stray from the nest site, find or dig a burrow, and locate sources of food.
Recently a team of investigators led by David Morafka, a biologist at the California Academy of Sciences in San Francisco, found that young desert tortoises are much more vulnerable than adults to dehydration, starvation, and predation. The shells of hatchlings and juveniles stay soft until they reach six or seven years of age. While desert predators, particularly ravens and coyotes, can't do much damage to adults, they can easily penetrate the shells of young tortoises.
Although relaxed homeostasis enables adult desert tortoises to make it through tough times, nutritional stress is a nearly constant feature of their lives. Exactly what effects that stress may have on tortoises is not known, but in vertebrates, stress of any kind generally triggers the release of the stress hormones corticosterone and cortisone. Prolonged high levels of those hormones can reduce the effectiveness of the immune system, thereby allowing infections or diseases to become established.
Whatever the mechanism, stress combined with disease has proved to be deadly for tortoises. In the late 1980s and early 1990s in the western Mojave, desert tortoise populations crashed [see sidebar below]. Elliott R. Jacobson, a veterinarian and zoologist at the University of Florida in Gainesville, and his colleagues discovered that a respiratory disease caused by Mycoplasma microbes was spreading rapidly in wild tortoises that were already weakened by drought. The benefit of relaxed homeostasis—having a better chance of surviving drought—comes at the cost of greater susceptibility to disease. In the modern world of disease microorganisms that spread by jet plane, that cost may be a high one.
Tortoises and turtles are the descendants of an ancient lineage, well known for their keen survival skills. However precarious their lives in the desert, tortoises have persisted for millennia by adapting their biochemistry in unusual but effective ways. But those techniques could soon become a lost art. Today there may be fewer desert tortoises in the Mojave Desert than there are living as captive pets in the backyards of Los Angeles County. Our ongoing efforts to understand how tortoises live in the wild can help ensure that after conquering the desert, they will still be able to survive without being relegated to captivity in suburbia.
|
Copyright © Natural History Magazine, Inc., 2002