Winter World: The Ingenuity of Animal Survival - Bernd Heinrich (2003)
BEES’ WINTER GAMBLE
Worker honeybees flying in and out of the hive and ranging over some fifty square miles may look as though they are all independent. Yet they are as bound to one another as if they were physically joined. Honeybees (Apis mellifera) are social animals and the colony as a whole acts as a single organism and the individuals in it are subservient to the colony’s well-being. It is individually in their best genetic interest.
Of the many surprises that have been revealed in these insects over the last century, one that is almost taken for granted is the colony response of regulating its temperature. Even in winter, temperatures in the center of bee clusters remain within a degree or two of 36°C. Whether it’s -40°C outside the hive or 40°C, the bees regulate the same hive temperature. Honeybees are the only insects in the Northern Hemisphere that can and do keep themselves active and heated up throughout the northern winter. In winter, they are able to regulate their microclimate protecting themselves and their developing young. Should any one bee leave the communal group in winter, it would, like a cell taken outside an animal’s body, die almost instantly by freezing. And if by some miracle it survived the cold, starvation would inevitably kill it. Yet, if a physiologist were to isolate a single honeybee and compare it with any one individual of thousands of other bee species, he or she might not detect anything remarkable. It is only in the context of the colony that much of the marvelous is revealed.
I’ll start by considering the highlights of how the bees regulate the temperature of their collective winter cluster, which in late winter and early spring contains eggs and tender larvae. As in overwintering by flying squirrels, kinglets, and most other organisms (including us), choosing the proper shelter or nest site is a primary prerequisite. In honeybees not only must the nest space be adequate for crowds of tens of thousands; it must also be large enough to accommodate nurseries for eggs, larvae, and pupae as well as having huge storage space for a hoard of energy supplies. Choice of proper nest site is important, and when necessary when the colony divides; that choice is not left up to chance.
The colony divides in the spring or early summer when the old queen leaves or is evicted by her daughters if she does not leave voluntarily. The old queen takes with her some 10, 000-20, 000 daughter helpers. Together the old queen and her many daughters constitute a swarm, which upon leaving the parent colony does not yet have a place to go. The colony at first temporarily clusters on a branch, and from there scout bees then fly forth in search of a new home. Analogous to our own evaluations of a potential house to occupy, bees pace out the dimensions of the place and evaluate other relevant parameters. The scouts then return to the potential site repeatedly, rechecking. Gradually each bee makes a decision, and if she deems the site potentially suitable, then she leaves a scent mark there and then reports back to the swarm.
“Report back” may sound anthropomorphic or overblown. But that’s precisely what the bee does. By a series of body movements called the bee dance (a ritualized flight behavior to the potential new home or a good food source), she indicates on the surface of the swarm cluster not only the distance and direction but also an approximation of the suitability of the nest site she has carefully examined. Bees that will soon fly out to examine her indicated site are able to “read” her message because they follow her instructions by dancing with her; by following her body language and accurately deciphering her body movements through their own. Her information is so accurate that others that have never been to the site indicated can fly out and check on it themselves, even if it is miles away.
Any nest search involves numerous scouts, and it usually continues until several scouts have each found potential shelters. Since the whole colony must stay together and thus can go to only one nest site, the next obvious problem is that of achieving a consensus on the best site after several are indicated. The queen does not make that decision. She has nothing to do with it. She is a follower. Unanimity is reached, instead, first because different scouts check out each other’s finds, and secondly because they readily convert if they encounter a better nest site than the one they themselves had found. However, consensus, without the aid of individual intelligence, is reached mainly because the scouts advertising inferior sites stop dancing, while the best sites are advertised more strongly; each potential nest site is advertised honestly according to its relative worth.
A swarm that has left the hive may hang at its temporary home on the branch for hours or days while scouts search for a nest site. During this time the swarm maintains its cluster core temperature near 34° to 36°C, but its cluster-mantle temperature is barely above 15°C (Heinrich 1981). All of the bees on the mantle are too cold to be able to fly, until they warm up by shivering, which costs much energy. The low mantle temperature helps to conserve the swarm’s energy supplies, which is critical especially during all of this time they are house-hunting. But how do the mantle bees know when to shiver and get ready to fly? A recent study gives us the answer.
Honeybees’ nests were once man’s only source of sugar, and humans have maintained an active interest in these insects for this reason alone for thousands of years, as judged by cave paintings, and possibly for millions of years as judged by our sweet tooth and inventiveness to satisfy it. Since early in the last century the bee’s inestimable value as pollinators, both in agro-and wild ecosystems, has boosted our perceptions of their lives and their ways even more. With all of the interest and nonstop research on honeybees for over a century, especially that brought to the attention of the whole world by the spectacular discoveries of the dance language by the Austrian Nobel laureate Karl von Frisch and his numerous students and their students and associates and recruits, one would think that the well of discoveries in them would by now be dry.
Not so. Every discovery sets the stage for the next. While von Frisch disclosed to us their stunning dance language as well as their sensory world, neurobiologist Randolf Menzel at the Free University of Berlin deciphered the connections of the bee’s senses with their short-and long-term memories. In recent decades we have discovered the mechanisms of how they regulate their individual body temperatures, and how they communally regulate their swarm temperature. Cornell biologist Thomas D. Seeley elucidated how scout bees evaluate the suitability of a potential nest site, which I alluded to previously, and only last year (2001) he with Jürgen Tautz, a colleague from the Theodor-Boveri Institute in Germany, discovered and documented an acoustical “piping” signal bees make by contractions of the flight muscles that is mechanically much like their shivering. Scout bees giving those signals stimulate cool bees on the outermost layers of a swarm cluster to shiver and warm up. Like the bee dance, which can be interpreted as an abstract or greatly abbreviated enactment of a flight toward the intended location, the piping signal similarly symbolizes preflight warm-up. As in a warm-up, the sound (vibration) frequency in any one piping sequence starts low (as at low body temperature) and then ends at a high frequency (as at high body temperature). It differs from warm-up vibrations in that bees normally dampen the warm-up or shivering vibrations so that there is little or no sound, as in a smoothly running motor.
Once the cool bees on the swarm mantle are warmed up and capable of flight, another signal, called “buzz running,” made also by the scouts, initiates takeoff of the cloud of thousands of bees. It launches them into flight and on their way to their new home. The more synchronized the bees are, the fewer members of the colony will be left behind. The next problem is of bees potentially getting lost from the huge crowd of thousands flying to the new nest site, which only a few of the bees in the swarm have seen.
Only some of the bees in the swarm actually know where they are heading. But the swarm crowd is guided by what scientists have dubbed “streakers” (scouts presumably) who zip through the swarm drawing attention to themselves and leading it in the proper direction. The others, and the queen, follow. However, the bees continue to fly on only if the queen is with them; they detect her presence by scent.
After the swarm is ensconced in its new nest site, which in the wild is generally a hollow tree, its next main task is foraging for nectar and pollen and building receptacles (out of wax produced from special glands in the abdomen) for the pollen and honey that will be hoarded. Honey is the bee’s energy fuel for heat production, and pollen or “bee bread” is the primary protein food fed to the young for growth. Honey is an almost pure sugar concentrate, and it is collected as nectar in the bee worker’s stomachs and then regurgitated into the wax storage cells.
A colony of north temperate honeybees with ample fields surrounding them can produce nearly two hundred pounds of honey in a single summer. This is more than enough fuel to keep the hive warm all winter, so that we can in good conscience collect and eat the hive’s surplus without destroying the colony. Two or threee hives are sufficient for providing all of my family’s sugar needs for a year.
Honey, as such, of course gives off no heat until it is combusted (burned), or metabolized. In both cases the retrieval of the energy from the carbon-carbon bonds of the sugar molecules requires oxygen and yields carbon dioxide and water. Honeybees metabolize honey (i.e., the sugar in it) during flight while collecting pollen and more honey, and exclusively to get heat during shivering. Shivering involves the same muscles used for flight, only the wings don’t move because the upstroke and downstroke wing muscles are each in a slow tetanus contraction, one pulling against the other until both are pulled taut.
Shivering, since it uses up valuable honey stores, is minimized by the bees if it can be. Instead, their first response in the winter cluster, which is much like a swarm cluster, is energy conservation. As temperatures outside and then within the hive get lower, the bees begin to draw closer toward one another to form an ever-smaller and -tighter cluster.
The overall effect of cluster temperature regulation can be explained by distinguishing the bees on the outside of the bee cluster—the mantle bees—from those in the center of the cluster—the core bees. The lower the external temperatures, the more the mantle bees try to crawl into the cluster. When the cluster has shrunk to near minimum size, then the outermost mantle bees can finally only force their front ends inside. They plug every hole, and heat produced by bees’ metabolism within the cluster becomes trapped. Of course, some heat still leaks out by convection and conduction, and for a while the mantle bees are still sufficiently warmed by it. But eventually the mantle may become cold enough for the bees in it to finally have to shiver, to rely on heat produced on their own. In contrast, when external temperatures rise, then there is a lesser temperature gradient from the inside to the outside of the cluster. Less heat then leaves, so the bees inside may start to heat up. After becoming too hot, they crawl out to where it is cooler, onto the mantle, creating cavities and holes through the cluster. As a result of the bees’ escaping the heat, the bee cluster then expands, more air channels are created through it, and even more heat leaves.
No central control is required to achieve this communal response that automatically stabilizes the cluster microclimate. No chemical signal from the queen in the center serves as a thermoregulatory directive, since groups of bees with and without their queen react similarly. Neither do bees carry messages back and forth from outside to inside, because when the core bees are experimentally separated from the mantle bees by a thin gauze there is also no temperature change. That is, even when bees of the core are prevented from individually sampling the temperature surrounding the cluster, the core still maintains the same temperature. I also found no change in bee cluster temperature when I played back recordings of buzzing sounds generated by bees either in the core or the mantle at high or low temperature through a small speaker placed in a cluster core or its mantle. Additionally, I exchanged air by pumping it from the core to mantle, and vice versa, and also found no effect. Apparently, the bees in the core and the mantle do not inform each other about local temperature in order to coordinate a colony response. Instead, the high and relatively stable core temperature and the lower and more variable mantle temperatures can both be reasonably well explained by the response of the individual bees regulating their own temperature. The summed response, however, serves all in terms of energy economy.
Sometimes, however, the individual’s sacrifice is best for the colony, and given that bees are communal animals and the individual sterile workers (who are all female) produce offspring only indirectly through their siblings (new queens), that sacrifice is then selected through evolution. The most obvious sacrifice workers make is their attack on nest predators by stinging them. (When a honeybee worker stings just once, its barbed stinger is detached from its body along with the attached poison sac, and that bee soon dies.)
Worker bees may sacrifice their lives in another way. They may die not only by losing body parts, but also by quickly freezing to death. At least so it seemed to me when I watched my hives in the 2000-2001 winter. As is to be expected when examining something of sufficient complexity and interest, I made false starts, but learned along the way. Like the CIA.
During the Vietnam era, GIs discovered mysterious yellow spots on jungle foliage. The CIA was brought in to investigate the so-called mysterious “yellow rain,” which was soon suspected to be a new chemical weapon sprayed by the Vietcong. But entomologists later revealed that the smelly yellow mystery droplets came…[from bees.
Yellow spots are much more visible on white snow than on jungle foliage, and everyone can see them in the winter near their beehives here in northern climates. One also sees bees flying out of the hive in the winter whenever there is a thaw, and the prevailing wisdom is that they leave to take a poop if that is what they do. It made sense, just like yellow rain. But that didn’t make it true.
Forty thousand or so physically active honeybees exercising all winter to keep warm while crammed into one small space with lethally low temperatures outside face a hygiene problem, just like a bear does while in its winter den. But solutions are found. Bees won’t defecate within the hive any more than a bear will, which is to say never. The difference is that unlike a bear in winter, bees eat a lot, and they eat the same food a bear finds irresistible, honey and pollen. As the hive in winter is always clean of poop (although sometimes littered with corpses), we may see no problem at all, simply because the bees have solved it so well. But how long can they wait? Till spring? Do they die rather than poop? January 2001 provided a unique opportunity to make observations to shed light on the problem, because we had almost daily or at least weekly snowfall interspersed with sporadic bouts of sunshine with temperatures rising all the way to 2°C.
We had our first letup of the bitter cold at the end of the first week in January. The weatherman talked of “the January thaw.” It was warm enough so that the kids could get out and play in the snow without running back inside within two minutes crying from the cold. Kids were not the only warm-blooded creatures who ventured out, at least briefly. Some of my bees did so as well, and bees are decidedly more vulnerable to cold than kids, given their huge size-disadvantage for heat retention.
The bees had by then already been confined in the hive for about two months. Admittedly, they had been fueled with honey, a relatively clean-burning fuel. But the honey also contains small amounts of impurities (such as amino acids) that result in bulk uric acid wastes accumulating in the gut. The thaw came just in time, I thought, for some cleansing flights.
At the first hint of warmer weather, my honeybees flew out quickly and some of them left yellow stains on the snow. They also left corpses; not all bees survived the hazardous outdoor ventures to void their bowels: The snow in front of my three hives under the roof against the side of the chicken pen was pocked with fifty-three seemingly dead bees.
Unlike other insects here in the north, honeybees cannot survive freezing. They must keep body temperature above about 15°C at all times to be able to stay active (or crawl), and they need a muscle temperature of at least 30°C to operate their wing muscles to generateenough power to achieve lift for level flight. Within the hive in winter, many bees tolerate their body temperature dropping to 12° to 15°C. These temperatures are their lower tolerable limit for walking, and it is also the low body temperature set-point that they “defend” when on the swarm or bee cluster mantle, because at still lower body temperatures they become immobile. At body temperatures below about 12°C they start losing physiological control. They cannot shiver to warm themselves back up by their own metabolism, and they are then also unable to crawl back into the social cluster to be warmed by the collective metabolism of the colony. Thus, if a bee should get separated from the winter colony cluster, it would die as soon as the temperature surrounding them (such as on snow) is about 3° to 4°C lower than 0°C since once outside the hive, and at a body temperature of -2°C, internal ice-crystal formation kills them. When honeybees fly out to void themselves at near 0°C, they can therefore not drop their body temperature appreciably before they must return to the warmth of the bee cluster in the hive.
Honeybees are only capable of maintaining a modest difference (of about 15°C) between body and air temperature by shivering and/or flight metabolism; thus if they leave the hive into 0°C air, they are in mortal danger. The bees’ corpses littering the snow in front of my hives were of those individuals whose body temperatures had first declined to below 30°C, and then plummeted to lethal temperatures because they lost the ability to control their body temperature. That is, they were those that lost power, fell to the snow, and then cooled to -2°C or less, to freeze solid.
Do the bees experience a reluctance similar to my own to go to the outhouse at my Maine cabin on subzero nights? And when they do fly out do they try to be as brief as possible, since to tarry even a minute means to court death? Do they take off as hot as possible, to thus increase flight speed and delay the inevitable cooling to lethal low temperatures?
Given the bees’ small body size, cooling occurs in seconds. Caution in leaving is likely an important variable for natural selection and caution differs among different populations. I found previously that African honeybees (the so-called “killer” bees), for example, are at least as able as our native (European) honeybees at regulating their body temperatures through shivering. Yet, as soon as the African bees reach northern latitudes they suffer huge colony mortality because their workers are insufficiently inhibited from leaving the hive into the cold winter air over the dangerous icy blanket of snow that they have not experienced in their evolutionary history. Unlike the northern honeybees, these bees incautiously rush forth into cold, whereas the northerners proceed much more reluctantly. However, I thought that my bees proceeded not reluctantly enough, even at 1° to 2°C.
Two days later temperatures had dipped to -7°C, and no bees whatsoever were then venturing out spontaneously, providing an ideal opportunity to test their physiological limits. Poking a twig into the hive I generated a crowd of bees rushing to and congregating at the entrance. After a little more poking, I succeeded in provoking a few individuals to fly at and around me. I timed the flight durations of ten of them. Most nose-dived into the snow in just 2 seconds. None lasted over 6 seconds (the mean was 3.6 seconds) before it hit the snow, buzzed briefly, stopped moving, and then froze solid. Between takeoff and landing at flight cessation, the bee’s thoracic temperatures declined from 38° to 40°C at takeoff to 29° to 33°C (the mean was 30.9), right after they crashed when I grabbed them and determined their thoracic temperature with my electronic thermometer by the time-tested “grab and stab” technique. (Head temperatures would have been several degrees Celsius lower.) None made it farther than fifteen feet from the hive. After these measurements I agitated thirty-three more of them to leave the hive to see if any could make it back. None did. All fifty-five bees that I examined had the foul-smelling yellow paste in their rectums. My crude experiment showed that if they do leave at -7°C, which they were only willing to do in defense of the hive, they risk certain death. At what temperature would they risk flying out on their own?
On January 20 we had sunshine in the afternoon, although air temperatures remained low, near -9°C. But at about 2:30 P.M. the sun hit the hives broadside and bees started coming out spontaneously. In the half hour that I watched as an innocent bystander, 125 flew out. Every single one of these bees took its (involuntary) kamikaze dive into the snow after a few seconds of very rapid cooling in flight. Not one of these 125 eager leavers made it back into the hive. All solidified from internal icing. Most (112) of these bees had not voided their rectums, as I could easily ascertain visually by pulling open their abdomens. I was puzzled now, wondering: Why didn’t they defecate when they had the chance? They could not have flown out to commit suicide! Why had they risked death? I was determined to get to the bottom of this mystery. The next day, when it was warmer, I got another clue.
There was again a short period of sunshine in the afternoon. This time over three hundred bees had come out spontaneously—I found them dead and strewn all over the snow in front of the hives. All had died there, as before, since the snow was still near -6°C and so they all froze solid. Also as before, there was only modest fecal speckling on the snow; there was no soiling like one might expect if hundreds of bees had rushed out to relieve themselves. Were those bees at the entrance, the ones that rushed out, the subpopulation that most urgently had to relieve themselves but that died from cold before they had a chance? With that question in mind, I lifted a hive cover (the point in the hive farthest removed from the entrance) and retrieved fifty bees from the bee cluster just underneath it. All fifty of these had feces in their rectums, and I could detect no difference in the amounts they had from those in bees that had risked flying out into the cold. Neither did it seem that the abdominal temperatures of those outside had been too cold to perform their function; the abdominal temperature of those hitting the snow was still relatively high (11° to 19°C with a mean of 12° to 15.5°C).
Apparently the bees had not come out just to defecate. I also doubted that they failed to get back into the hive only because of the cold since many of the bees hit the snow in fully powered dives. Might the bees (who had of course never seen snow before) have been disoriented by not seeing dark ground under them, and so they had accidentally dived into the powdery white and featureless snow? To find out I now spread wood shavings all around the hives, and I then provoked more bees to come out. Air temperatures were -8.3°C. Voila! Although many bees crashed as before, sixteen out of forty now made it safely back inside, whereas none had done so before even at considerably higher temperatures. Therefore, at least some of the earlier deaths were probably due to disorientation over the light featureless snow that slowed their ability to get back.
On January 22 of that year we had a thaw and temperatures finally reached a few degrees Celsius above freezing. The shavings were still spread around. This time there were fewer than a dozen new dead bees near the hive itself, but there were at least sixty strewn all over the snow at 100 to 200 feet. Several bees had even flown up to 100 yards beyond the hive before landing in the snow. Why did they fly so far? I gathered up as many as I could find, and again examined their bowels. This time twenty-five of them had voided but the rest still retained their fecal load. Unloading is thus something that they do, but it seemed more and more unlikely that the primary reason the bees risk their dangerous exiting is for gut evacuation.
By Friday the twenty-sixth, it had again warmed to just barely above freezing, and new snow had covered the many dead bees so the new corpses could be counted. I counted 225 bees that had recently crashed into the snow in the hive area. I then watched my hives for forty minutes in early afternoon. Many bees were still coming out spontaneously. I kept my eye on individual bees, noting their typical back-and-forth orientation flights, circling, and then their departure into the distance till they were out of sight or till they crashed! Of 171 bees that I followed visually, 96 crashed into the snow, while 52 went out of my vision into the distance. I saw only three defecations, finally convincing me that although the bees proximally “cleanse” on some of their so-called “cleansing flights,” the ultimate reason for those flights had to be something different. Could the flights be scout bees searching for flowers to get food, or water to drink?
On New Year’s Day I had picked willow twigs and brought them into the house. In two weeks male catkins were shedding pollen. Quaking aspen buds brought in at the end of January opened in only four days. It was not yet spring, but the plants were ready. The bee cannot know if or when the red maple, willow, and poplar trees in the surrounding bogs and forest will burst forth with their very brief one-time offerings. The colony can’t know by divine inspiration, and it cannot afford to miss the early spring harvest. But it can afford to lose some workers to buy information.
Red maple. Female
Quaking aspen. (Populus tremuloides)
There is a huge premium for swarms to leave the colony early in spring, to allow for sufficient time to find a new nest site, build honeycomb, rear young, and build up the large honey stores required to get them through the winter. The only way for the bees to get information on when the first blooms are available, so that swarms can be launched sufficiently early to accomplish all this, is to venture out and search. A few hundred, or a few thousand, worker casualties may be a small price to pay for being at the first bloom (or being first at the bloom). After all, the colony is a superorganism whose success is measured by the reproductive output of one queen, and the queen’s output depends on honey and pollen input.
The fifteenth of March was finally a “warm” (8° to 10°C) sunny day. On this day I saw a first no-doubt-honest-to-goodness cleansing flight: On this day the air was loudly abuzz with thousands of bees at any one time, and on this day it fairly rained yellow droplets continuously. I cleared five 1-square-foot sections of snow and found 80, 95, 94, 102, and 160 fresh droplets collected on them, respectively, in just thirty minutes. There were almost no dead bees on the snow. Bees repeatedly landed on the snow, but they all got up to fly again. Most bees vanished from sight before again returning. They were foraging. They were seeking flowers, and the wind-pollinated trees from which they gather a major pollen crop bloom early. The poplars and red maples open their blossoms in late March. No other pollen is then available, but I counted up to 154 bees laden with poplar pollen returning to one hive per minute on the day after the poplars first bloomed, and when winter was not yet over. (There are then still frequent nightly frosts, and in 2002, the next year, a storm dumped six inches of snow on April 22, three weeks after the poplars had finished blooming.) The bees’ sacrifices paid off. All the colonies survived the winter, issued swarms, and made near-record amounts of honey that spring and summer.