OF BATS AND BUTTERFLIES AND COLD STORAGE - Winter World: The Ingenuity of Animal Survival - Bernd Heinrich

Winter World: The Ingenuity of Animal Survival - Bernd Heinrich (2003)


One of my fondest childhood memories is of the bats on summer evenings. As reliable as the swallows in the barn and the bobolinks in the hayfields, I saw bats zigzagging around the barn in the evening. They fluttered over the fields and close over the water surface of nearby Pease Pond as we fished at dusk for white perch. I don’t see them much now and I miss them.

My father was a bat enthusiast (in addition to his passion for ichneumon wasps and his interest in birds not to mention his pet Bulgarian weasel), and on some evenings we went out to hunt them with his shotgun. My mother, his preparator on many expeditions, skinned and stuffed them. Each species had its own flight signature in the way it fluttered or zigzagged, and the habitat where it could be found. It was challenging to learn about bats, and exciting to see them. His collection of perhaps two dozen species, which is displayed in glass-covered cases, ended up at the Bates Museum at the Hinckley-Good Will School in Maine. When I last saw those bats there in 1999, I was saddened. Not because we had killed them—their deaths, of course, brought us awareness and possibly knowledge. Rather, I was sad for the deep ignorance of those who have never seen, handled, or learned to appreciate bats, which is in part responsible for their population crashes all over the continent. Almost nobody sets out to do deliberate harm. Most evils happen inadvertently, through not knowing and uninformed notions.

At that time I did not wonder much about how bats spent the winter, nor did I (or anyone, until twenty-three years later) have a clue or care about the winter whereabouts of the monarch butterflies (Danaus plexippus), whose familiar yellow-white-and black-striped caterpillars fed on the milkweed patch next to the barn. I picked up caterpillars, fed them milkweed and raised them to adulthood in my room. I did not suspect that butterflies and bats had anything in common, nor that the continued survival of both depends on precise temperature regimes of their winter world, at pinpoints of the globe hundreds and even thousands of miles removed from the isolated Eden of the Maine woods, where they seemed part of the landscape. The official response of “protecting” these animals by making it illegal for curious kids to handle or collect them assumes that everyone wants to do it. By that logic one could just as well make it illegal to not handle wildlife, because some get enlightened by contact with it. Personally, I think that is ultimately more useful than everyone being distanced from it. Contact should be encouraged.

The monarch butterfly summers throughout the United States and into southern Canada, which is the northern limit of its food plant, milkweed. There are two major populations of the monarch that are separated by the Rocky Mountains. Those west of the Rockies migrate to the California coast in winter. There they overwinter in about forty colonies, including well-known ones at Muir Beach, Santa Cruz, and Pacific Grove.

For a long time it was not known where the eastern population spent the winter. In 1937, zoologist Fred A. Urquhart and his wife, Norah, suspecting that the butterflies migrated, started gluing tiny tags onto the wings of thousands of monarchs at their home base in Toronto, with instructions to send recoveries to them. By mapping recapture sites over a number of years, they were able to reconstruct the butterflies’ flight lines and determine that they were migrating all the way to Mexico to overwinter.

We now know that the eastern population extends from the eastern slope of the Rockies all the way to the Atlantic seaboard. Most of this population migrates south in the fall, with individuals in it traveling up to 4, 500 kilometers to over-winter in twelve extraordinarily small patches of pines and firs in the Transvolcanic Mountains in the Mexican state of Michoacan. The butterflies overwinter in these mountains at an altitude of 2, 900 to 3, 300 meters (9, 500 to 11, 000 feet) at preferred sites that have cool yet not too cold temperatures, high relative humidity, and little wind (Brower and Malcolm 1991). At one large colony where more than 14 million monarchs congregate in about 1.5 hectares—about 4 acres or less than a hundredth of a square mile—temperatures ranged from 5.6° to 15°C, near the butterflies’ threshold for shivering to get ready to fly. It is here, at these sites, that the vulnerable heart of the North American monarch population resides and spends most of the winter in torpor.

Monarch butterfly.

To keep the spectacular migration spectacle alive requires protecting the cool forests that promote the torpor and extend the insects, energy supplies. It is a sobering thought that most of the population of eastern North America could be wiped out by an irresponsible woodcutter with a chain saw. Continual survival is only as secure as the weakest link, of the innumerable links—thousands—to the existence of any species. In the long term, however, it is not only the roosting groves that are critical. Given environmental change, such as the global warming that is now melting the glaciers all over the world at a phenomenal rate, the alternative and as yet unused potential roosting sites will become important in the future.

The larger the aggregation, the less the individual butterflies in it risk predation. However, a main reason the butterflies use specific overwintering sites is that they can maintain the low body temperatures there required to maintain energy balance while at rest for three months of virtually no feeding (Masters, Malcolm, and Brower 1988). On average the butterflies’ body fat reserves are such that upon entering their hibernation site, they should last about ninety days at 15°C (ibid.). On the other hand, if the body temperature of resting butterflies were 30°C, then their rate of resting metabolism would be high enough to exhaust their fat reserves in fewer than ten days. In addition, they would likely dehydrate.

It is also important to note that the migratory behavior—restlessness, flight direction, and maybe duration and destination—has evolved. The butterflies won’t just stay at the first cool spot they hit, because it could become hot, or too cold. They rely on the genetic, or long-term, experience of the race. Hence the importance of specific overwintering sites that have proven to be safe for their ancestors.

By February as the days get longer and the monarchs’ critical photoperiod of 11.3 hours is passed, the hibernating butterflies can again become reproductively active. There is, of course, nothing magical about 11.3 hours of daylight per day as such for reproduction, except for monarchs. Like overwintering sites, that specific time represents an evolved memory of the race. It is the photoperiod that in theirevolutionary history has proven to be the best, for them to be prepared to be active. After this photoperiod is experienced, the butterflies simply wait for the next cue—temperature. Rising temperatures trigger a massive mating response in the colony (Brower et al. 1977). After mating (another cue), the females then migrate northward and eastward back into the United States and southern Canada. Along the way, they respond to the scent of milkweed, a cue for laying their green eggs on the newly emerging plants.

For a long time there was controversy on whether the monarchs colonized their entire eastern range with the first spring generation leaving the Mexican overwintering sites, or whether the northward march was achieved in steps, by successive generations. Thanks to the fact that milkweed contains cardenolides (to us nauseating chemicals that are also heart poisons), this issue has now been resolved: It requires up to four generations for the monarchs to reach their northernmost breeding grounds.

The method to generating the above answer exploited the fact that different milkweed populations contain specific chemically distinct arrays of cardenolides. The monarchs ingest these poisons as caterpillars, store them in the pupa and transfer them into the adult butterflies where they serve as a chemical defense against predators. By extracting these poisons from a butterfly, one can get a chemical “fingerprint” to match that found in the milkweed of different areas. For example, the overwintering monarchs in Mexico and those on the early leg (March and April) of the migration had cardenolides that are found in milkweeds that are not found in Mexico or in the southern United States. Thus by such biochemical sleuthing it could be deduced that the overwintering monarchs and the early spring migrants were derived from caterpillars that had grown up the previous summer in the northern United States and Canada. In contrast, the butterflies collected in May and June in North Dakota had cardenolide fingerprints matching those of milkweeds growing only in the southern United States.

Every fall I now eagerly and admiringly watch monarchs, our most conspicuous insect migrant. Day after day in October, the handsome orange-and-black-striped butterflies flap and sail lazily over the sunny fields, the woods, and water, all flying individually yet all heading in a southerly direction. In the evening they stop and gather on the purple New England asters to sip nectar, and in the morning they bask and shiver, rise into the air, and resume their journeys.

Individual butterflies tagged in Canada in the fall have been recovered thousands of miles south. By winter most of the eastern population has settled into their winter mountain retreat near Mexico City where their great-great-grandparents had been before them. It is a destination they seek out with incredible energy expense, never having been there, nor knowing where they are going. By the tons, in a spectacular shimmering orange display, they festoon the trees.

The million-dollar question is: Why do monarchs bother? Why don’t they all hibernate and stay north, as do most butterflies? Like most questions that relate to history, this one does not have a simple answer: because history, especially evolutionary history, is never just one thing acting in isolation of everything else.

The monarch butterfly is a member of the family called the Daneidae, a tropical group. Monarch’s relatives live in the tropical lowlands of New Guinea, and they are prominent in the American tropics as well. The ancestors of the present-day monarch butterfly, Danaus plexippus, were presumably also adapted to a tropical climate. Like most butterflies, they are predisposed to disperse when the larval food runs out. Not being able to survive freezing temperatures, there was then strong selective pressure for dispersion in a specific rather than a random direction; many dispersed in the wrong direction but all of those individuals left no offspring to pass on their trait. Only those who lucked out by flying southward survived; thus an evolutionary direction and destination was born and then grew.

At the same time they were evolving directional dispersal, monarchs had to surmount another problem. On their annual southern treks they had to cross into the hot, arid environments of the Mexican deserts. Here there was little chance for these strong fliers to refuel, and facing a long interlude until feeding was again possible, they must have experienced intense selective pressure to conserve energy. Partly by chance, some individuals probably ended up in the mountains, perhaps blown there by tropical updrafts. I once saw aggregations of insects on Mount Meru in Tanzania, and all of them were torpid. The cool mountain air had reduced the insects’ rate of energy expenditure to such an ebb that they could not even fly. They were now in cold storage and along with that went a reprieve from needing to feed, until they were again warmed.

It seems probable that, given an insect’s high reproductive rate, those few monarchs that took a flight path that somehow landed them in cold storage for the duration when no food was available would have a huge selective advantage over those that would have exhausted their energy supplies by staying in the heat in an environment with little food. By sifting for survivors, evolution selected where the population would overwinter. Generalities such as these should, given the right circumstances, also apply to other animals, including Lugong moths and bats.

In Australia, the Lugong moth (Agrotis infusa) also migrates to cool mountain areas where it clusters in large numbers (and where it was once an important food for Australian aborigines). The principle of the moths’ migration is the same as that of the monarchs’—to conserve their fat reserves during a long quiescence—but rather than migrating to escape freezing, they migrate to escape hot conditions.

In bats, we are given a fine example involving escape from both low and high temperatures. Bats are, like the Daneidae and also the Hominidae, animals of the tropics. Those that live in the north are outliers (as are Danaus plexippus among the Daneidae, and Homo sapiens among the Hominidae). Like us, bats are now able to live in the north, not because they tolerate freezing, but because they manage to avoid it. Like monarchs, many bats migrate, but their ability to do so leaves them much more leeway as to destination.

We tend to mostly think of migration as north-south movement, but migration can be in any direction whatsoever. Blackcap warblers from central Europe, for example, have traditionally migrated south, into Africa, in the winter. But within several decades a part of their population has evolved, by natural selection, to fly east-west instead, wintering in Great Britain where the weather is milder and bird feeders have become available. Similarly, northern bats of many species also migrate to where they can keep in energy balance. But that energy balance is achieved without feeding. Like the monarch butterflies, they migrate to cold storage environments where they can both conserve their fat reserves and not be endangered by freezing. With many bats, that means overwintering in caves.

If no feeding is possible for months, then just any cave won’t do. Cave temperatures can’t be below about 0°C, or else the bats risk death by freezing or energy exhaustion by shivering to prevent freezing. At the same time, cave temperatures can’t be high if no food is available outside, because then even the animal’s idling or resting metabolism would eventually exhaust their fat reserves. In general, each 10°C rise in body temperature doubles the rate of resting metabolism (i.e., resting energy expenditure).

In the south, some bat populations migrate north where cave temperatures (and lowest possible body temperatures) are low enough for them to remain in extended torpor (McNab 1974). Few bats are able to hibernate at cave temperatures above 14°C. The exceptions are very small bats and those that don’t cluster, and thus enhance their ability to cool.

Bat in summer, resting on a leaf.

A bat entering a cave for the first time cannot know beforehand if the temperatures within will be suitable to maintain a positive energy until the end of the winter, any more than monarchs can actively choose specific mountain retreats where their energy balance will come out just right by spring. However, if the animal ends up surviving, then conditions were suitable—the energy balance came out favorable, and the bat’s survivors will likely return to that site the next winter. This is what bats do. It’s not only natural selection that’s operating on bats to survive winter; there is also selection for caves that become bat caves; in those caves that are not suitable, the populations never build up. Conversely, once having built up, they decline if conditions become unfavorable.

Bats are long-lived animals that learn by experience, returning year after year to caves that have proven themselves to be safe, probably for centuries. Little had disturbed the constant and specific environment of their traditional caves until humans came along. Not surprisingly, therefore, human disturbance of bats gathered in specific caves has been a big factor in some bats’ declines. Merlin D. Tuttle from the Milwaukee Public Museum reviewed the association of decline with disturbance by people in caves, specifically of the endangered gray bat (Myotis grisescens).

Like other bats, gray bats are restricted to specific caves. They cluster in densities of over 1, 800 per square meter, and cave populations can be assessed by estimating the square meters of cave ceiling covered with bats. Their colonies are restricted to fewer than 5 percent of available caves, and in these caves the human disturbance has mainly been due to traffic by spelunkers and to vandalism, including by health authorities who have been known to torch a cave full of bats after receiving an erroneous rabies claim. The two most heavily disturbed caves in Alabama and Tennessee lost 90 percent of their bats, while the population in five of the rarely disturbed caves there remained stable.

In an attempt to stop the sometimes catastrophic declines, cave entrances were in many instances altered to restrict or limit human intrusion. Ironically, however, the results of these well-meaning measures were mixed; sometimes the population recovered, but in other cases improperly constructed gates resulted in the loss of entire colonies. Potential causes are illustrated in the endangered Indiana bats, Myotis sodalis. Female Indiana bats live nearly fifteen years and males slightly less (Humphrey and Cope 1977). Reproduction is slow. Females have their first pup at age two, and after that have only one per year.

This bats’ summer range covers most of the eastern United States, but about 85 percent of the population winters in seven caves; and half of the population can be found in just two. Since gaining legal protection in 1973, winter populations of the Indiana bat have decreased by about 28 percent until 1980-1981, and additionally by 36 percent in the next decade. A recent study by four researchers (Richter et al. 1993) from four different museums suggests that the bat’s perplexing declines were due to modification of cave entrances. For example, from in the early 1960s when entrance modifications were made, to the early 1990s the bat population of Hundred Dome Cave in Kentucky declined from 100, 000 to 50 bats. When the entrance of the Wyandotte Cave in Indiana was constricted by a man-made stone wall, the bat population declined from 15, 000 to 1, 400 bats by 1957, in twenty-five years. One thousand to 2, 000 bats continued to overwinter there until 1977, when the stone wall was removed. Immediately after that the population rebounded until fifteen years later, when it was back up to nearly what it had been originally. The researchers ultimately concluded that the modifications of the cave entrances had their main effect of restricting airflow so that temperatures inside had become higher. Those at Hundred Dome Cave, where there had been the most precipitous decline, had increased from 4° to 6° to 11°C. As a result, these hibernating bats, normally found in conditions of 4° to 8°C, were insufficiently cooled.

In this species the body temperature during hibernation is essentially identical to that of the air, from -3° to 30°C (Henshaw and Folk 1966). At the very lowest end of this temperature range the animals became aroused and exhibit mild shivering, to heat themselves up slightly above air temperature. (In a closely related species, Myotis lucifugus, the individuals cannot arouse from such low temperatures and they freeze to death at near -5°C.) However, the main danger to the Indiana bats in their traditional caves is not quick freezing, but slowly starving to death in temperatures above 10°C when their elevated resting metabolism eventually exhausts their fat reserves by the end of the winter.

To test the latter hypothesis, biologist Andreas Richter from Earlham College in Indiana, and three colleagues, compared body weight losses of bats in two caves of different temperatures. The body mass loss was 42 percent more rapid in bats roosting at higher temperatures, and the dead bats were emaciated bats. The mortality inferred by the conditions in the altered Wyandotte Cave, from 1953 to 1978, should actually have been high enough to eliminate the entire population at that cave. But bats attract each other, and the apparent stabilization of the cave population of one to three thousand individuals was more bad news than good. It was created by influx of other animals from elsewhere. The cave had become a sink, a death trap. The deleterious effects of just 5°C higher temperature extended far beyond that of the cave itself. The fate of bats and butterflies is balanced on the winter world to which they are adapted.