The test for the Hasler-Wisby hypothesis was bold and brilliant. The idea was to substitute a synthetic scent, one not found in natural streams, and to imprint salmon on it while they were young, and then to see if that scent could be used to decoy the adults during their spawning run to swim up a stream “flavored” with that chemical. This was a long-range and logistically difficult test, and a risky one as well, because it seems likely that salmon don’t normally orient to a single chemical, but to a mixture. How then would one imprint young salmon to test their responses years later? Wisby’s doctoral thesis was, first of all, to find and test a chemical that would be neither naturally repellent nor naturally attractive to the salmon, and the chemical he came up with was morpholine (MOR).
When Hasler and Wisby published their hypothesis and the planned experiment to test it, the only salmon populations where it could be tested were three thousand kilometers distant on the Pacific coast, not in Wisconsin, where they were. Since the Pacific was out of reach to them, they hoped someone else might become interested in the experiment and perform it. Nothing was done until almost twenty years later when an Atlantic fish, an invasive species, the alewife, became a nuisance fish in Lake Michigan. The Department of Natural Resources in Michigan planted coho salmon, Oncorhynchus kisutch, to control them. The coho thrived on the alewives and then spawned in the lake tributaries. Suddenly Hasler and Wisby recognized a serendipitous opportunity. With salmon in their own “backyard,” the hypothetical experiment could actually be done, and Hasler’s just-arrived new student Allan T. Scholz and other associates took on the challenge.
The test involved raising one group of the coho salmon hatchlings in a hatchery with water flavored with MOR and another group at the same hatchery in water flavored instead with phenylethyl alcohol (PEA). If the imprinting hypothesis was correct, each group of fish should have been imprinted on the respective unique chemicals found in their water. Then, to test if the scents would function in homing, the researchers released the hatchery-raised young fish of both populations into Lake Michigan. After these (marked) fish had grown to adults and were ready to migrate from the lake to spawn in streams, one stream entering the lake was flavored with PEA and another with MOR. These two streams and seventeen other (not artificially scented) potential spawning sites were monitored. The million-dollar question was, Which streams would their migrating salmon choose? The answer: over 90 percent of the fish chose the “correct” stream, the one flavored with the chemical they had known eighteen months earlier in the hatchery where they were “spawned.” The conclusion was unequivocal: the salmon had remembered. They had been guided to the scent they had experienced while developing. Hasler finally had the definitive proof, and it came just two years before his retirement, by which time he had guided fifty-two doctoral students.
Andrew Dittman and Thomas Quinn of the School of Aquatic and Fishery Science at the University of Washington have recently extended the salmon homing studies with Pacific salmon (Oncorhynchus spp.) in Alaska. In a large lake system in Bristol Bay, reproductively isolated populations of this salmon are genetically differentiated and adapted to specific local conditions. For example, those breeding in shallow streams are smaller in size and have less of a hump, while those spawning in places with a fine substratum lay smaller eggs. In these populations, separated into specific locations in the same watershed, the olfactory memory of the adults coming back to spawn reaches back to the time of hatching. Returning adults discriminate among increasingly similar scent sources until finding their eventual home site. Their sophisticated and precise homing ability suggests a high selective advantage not only to return to a suitable spawning ground of their species, but also to find the almost exact site where they were born. But “almost” exact is better than totally so.
Variability. Few things in nature are as impressive as the apparent perfection of the navigation mechanisms that allow animals to perform their miraculous homing feats. Yet, as the French philosopher Voltaire famously pointed out two and a half centuries ago, “Le mieux est l’ennemi du bien,” usually translated as “The best is the enemy of the good.” Perfection has a cost; it is difficult and takes a long time and a lot of effort to achieve, and it can lead to a liability—a specialization that limits options. In nature, including homing, there are instead mechanisms (such as sex) that create variability and act specifically to avoid present perfection in favor of compromise for future continuity in the face of unanticipated yet inevitable change. Nature and Voltaire, in other words, are in agreement that ever more perfected mechanisms generally do not achieve the best long-term results.
“Scent” of the water as such gives no guarantee that any given stream has suitable spawning areas, such as the gravel beds required by salmon. Some streams have neither suitable spawning nor feeding areas, while others may have both but be blocked by impassable waterfalls (and more or less guaranteed these days, also dams). Only that stream from which the fish came is sure to have access to both spawning and feeding grounds. The fish may make only one spawning migration in its life, and the homing journey may cover hundreds of kilometers, so if the wrong stream is taken, the fish may forfeit reproduction entirely. It has therefore little choice (if it could choose) but to return to the natal stream. But as I have mentioned, while Arthur D. Hasler and colleagues proved that most coho salmon are imprinted as young fish on the scent of their home stream, a small percentage of them chose another, or “wrong,” stream.
In general those fish that choose the wrong stream do indeed have a lesser chance of reproducing than those that do not, and as a consequence, one might on the face of that predict that there should be selection for ever-better homing and home discrimination. However, a locking in to current perfection is almost by definition disastrous in the long run, as long as change is a reality. And it usually is, given enough time. Variety is nature’s way of creating options in the face of future change, and in the long process of evolution, sex has evolved as a mechanism that scrambles the gene pool to create variety.
Over evolutionary history there were scenarios that eliminated the breeding opportunities at a salmon population’s home stream (such as a volcanic eruption poisoning the water, a watershed drying out, or a landslide creating an impassable waterfall), and at the same time, due to climate change, other waterways were created. The whole population at a stream could be wiped out. If, however, a salmon that spawns a thousand eggs has several offspring that end up at the one “wrong” stream that then turns out to be “right,” it could reap a huge reproductive bonanza at little cost because the new and uncontested resource would yield a whole population of descendants. That is, in analogy with the homily to not put all one’s eggs into one basket, “imperfect” homing can provide life-saving opportunity for some of the offspring, which then become the standard-bearers of a new population. Indeed, I think I found the perfect example of this right next to my cabin, but with amphibians.
My cabin is on a big steep hill, and it is deep in the woods. It is far from anything resembling a wetland where you would expect to find frogs and salamanders. Yet, I’ve found a red eft, a spotted salamander, and green and leopard frogs there. They looked as if they were lost, because they were in the “wrong” place, far from where they could live in the lowlands, and uphill at that. Later, though, it looked as if there is a method to such wandering. I happened to dig a hole about five meters across, for a possible decorative “pond.” It filled with water because there was a catchment of rock underneath. The first spring a couple of wood frogs found it and stayed to call. Now, the wood frog chorus from there is deafening every spring. During one later spring I heard a spring peeper there also—these frogs are no larger than my thumb, and I could not imagine how one of them had apparently traversed kilometers of forest to arrive at this spot. But several years later there was a small chorus of them. Then, the same thing happened with green frogs, and with salamanders. All of the amphibian species that come there now to reproduce also home to their p
laces of birth, but not all of the individuals do so. Some disperse, and when they do, they risk much but gain a small chance to “win the lottery.” Somehow a few individuals had found the right spot in a sea of unsuitable possibilities. But I doubt that either their willingness to wander, or their ability to find and recognize what they have found, is not associated with evolved behavior.
Picking the Spot
IN LATE APRIL AND EARLY MAY, AT THE END OF THE MAINE winter, the wood frogs are chorusing and mating and the birds are starting to rush north as though sucked up by a vacuum. The woods ring with their song, and the drone of bees fills the air. Willow, maple, and other tree flowers are opening, and bumblebees are fueling up with nectar, getting ready for the most important decision of their lives: where to build their nests. You see them here and there, zigzagging a few centimeters above the matted leaves and grass where there may not be a flower in sight. When there are flowers, these bees often ignore them. Now and then one of them lands and walks on the ground, then lifts off again, flying this way and that, to continue her close ground inspection at another place. Occasionally one of these recently overwintered bees crawls into a hole or crevice and disappears from view, only to emerge a minute or two later, wipe her antennae with her front pair of legs, and then fly on.
It is sometimes easy to follow a bumblebee for several hours, but only in the summer while she is foraging for nectar and by then also pollen as food for her larvae, making only short flights in an open field blanketed with flowers—because bees can work for an hour or more before gathering a full load of nectar or pollen. But these early spring bees show interest in the ground (and, in some species, in tree trunks), and they may fly for kilometers and keep it up day after day if they can tank up quickly at a patch of sugar-yielding flowers. They are all “queens,” females who mated the previous fall. They are hunting for something, but it certainly cannot be mates. They have no need for more sperm for the rest of their lives. Instead, they are searching for a place to home, where they will spend the rest of their one year of life, to raise a family of perhaps hundreds of sons and daughters. Not just any place will do.
In northern climates, the house-site-hunting bumblebee queen must be fussy. A queen who chooses a wrong home site forfeits her entire reproductive life. She needs to find a shelter that will remain dry and insulated from the not-infrequent cold rains and frosts. I do not know how these bees evaluate potential home sites, but they choose small dark dry cavities with fluffy material in them; many species of bumblebees take over existing old homes such as mouse and squirrel nests. Sometimes they even evict the nest’s rightful owners. One time I found an Arctic bumblebee queen, Bombus polaris, on Ellesmere Island taking over an active snow bunting nest of dry grass lined with feathers. These far northern bees have demanding requirements for a home, but honeybees have an arguably even more demanding task in finding a home site.
Honeybees originated in the tropics where they evolved to maintain a large year-round colony. They require a solid and roomy home, one that accommodates a population of thousands. A bird or mouse nest won’t do, and the primary reason they are now able to live in the north at all is because of highly refined homing behaviors. Bumblebees hibernate in the winter, and the queens, the colony founders in spring, burrow into the ground; the colony itself does not survive beyond fall. The honeybees’ home must serve as a shelter not only through summer, but throughout the coming winter or perhaps numerous winters as well. Their nest site must protect them from deep frosts, and it must be spacious to hold large honey and pollen stores in the winter. The colony needs these stores, not just to survive the winter but also to rear young then. The young not only are fed but must be kept warm in order to grow. This means the home must be heated, which requires a constant use of fuel. The colony starts rearing young while there is still snow on the ground to build up a large worker population to exploit the spring bloom. That is, honeybee homes must be large enough to accommodate not only tens of thousands of occupants but also to store huge amounts of honey to feed and fuel their heat generation through the winter. And because they contain the rich honey stores and brood nurseries that tempt predators, they must additionally be heavily defended. The upshot is, to ensure adequate protection from both the weather and predators, honeybees in the north temperate region must nest in a securely enclosed cavity, one where they can pack in perhaps twenty-five but up to fifty or one hundred kilograms of honey and pollen, and also have room for nurseries for rearing young, plus hold the population of several tens of thousands of bees.
In the wild, the usual site chosen by honeybees is a large hollow tree. Unlike bumblebees, where only one bee founds the colony, it takes a swarm of honeybees to found a colony in a new home. A swarm consists of about half to two-thirds of the home occupants and their old queen, which depart usually shortly before a new queen emerges (if the old queen does not leave, there is a life-and-death battle between her and her daughter). Perhaps a third of the bees in a colony stay after the swarm leaves, and they will soon be supplied with the newly emerged queen.
With honeybees, the decision of which home site to use is not made by the queen, as it is with bumblebees. It is instead a social decision that involves her sterile daughters, some ten thousand individuals, and that decision is based on an evaluation of alternative choices that representatives of the colony offer up. Each site is evaluated, and the results inform a democratic process and a unanimous choice.
The story of honeybees’ home choice arguably began with Karl von Frisch, when he elucidated the honeybee dance language. But in the early 1950s, his student Martin Lindauer used knowledge of the stunning von Frisch discovery as the lever that eventually solved part of the mystery of how honeybees choose their home sites.
Lindauer saw bees doing their waggle dancing on swarm clusters—on the surface of the mass of bees that forms after the bees of a hive have left their overcrowded home and before they have found another. Successful foragers inside the hive routinely use such dances to indicate the direction and distance of food. The foragers are usually dusted with pollen, and they carry two pollen packets in the two corbiculae (hairs adapted to hold pollen) on their hind pair of legs. But the bees Lindauer watched on the swarm clusters carried no pollen; they were instead smudged with dust and soot. Since swarms are groups of bees in need of a new home, Lindauer deduced that these “dirty dancer” bees were “scouts” that had examined cavities in the ruins (this was in postwar Munich) and were now advertising potential new home sites.
Lindauer’s subsequent work based on his acute observation was published in the now-classic paper titled (in translation) “Swarm Bees in Search of a Home.” In it he revealed that there were often several potential home sites being advertised simultaneously by different bee scouts, yet all the scouts eventually agreed on just one site, the best of the lot. After all the dancers had reached unanimity (were all indicating the same site), the more than ten thousand bees of the swarm left en masse and flew directly to the nest site. Being able to read the scout bees’ “language” that encoded the locations (approximate distance and direction) of these sites, Lindauer was able to predict the future home locations advertised by the scouts and was even able to arrive at the bees’ chosen home site before they themselves arrived to move in! But this left a fascinating question: How had the bees reached a consensus, and how had they achieved the social coordination to get to the chosen home that most of them had never seen?
When I was teaching insect physiology and conducting research on temperature regulation by bumblebees and honeybees at the University of California at Berkeley, I was puzzled by how it was possible that all of the bees of a swarm took off together. I knew that their flight muscles had to be heated to about thirty-five degrees Celsius before they could fly, but most of the bees in swarm clusters that I examined were in near torpor, because when I shook a swarm off a branch to capture it, most of the bees dropped straight down onto the ground (or into a container that I held under them);
they had apparently not yet shivered and warmed up. My measurements showed that only those bees that were in the core of a swarm were warm enough to fly, while the rest, which was most of the bees, were not. So how could all the bees of a swarm fly off at once at one specific time, as they needed to do in order not to be left behind when the swarm left to fly to its new home?
My wild swarms (procured mostly with the help of the Berkeley fire and police departments) were set up to hang at the windowsill of my upstairs lab over the Wellman Hall Entomology Department parking lot. I then installed temperature sensors in numerous locations in these swarms, recorded the temperatures electronically, and printed them out on a chart recorder so I could view them continuously from inside my lab. Days often went by with only a few bees coming and going, while the swarm, the mass of them, remained too cold to fly. But then suddenly one day the outside layers of bees on the swarm cluster started to warm up, and all these bees got hotter and hotter. And then, shortly before a swarm takeoff—the time during which a consensus of a single future home location is reached—the temperature of the swarm periphery finally reached the same as that of the swarm interior, which was also the body temperature the bees required in order to fly. The swarm then quite suddenly dissolved into a cloud, which enveloped much of the parking lot below my window, and not very quickly coalesced, and then took off in one direction, presumably to their newly chosen home. This proved what I wanted to find out. For various reasons my swarm studies were soon terminated, and I went on to other things. But, as almost always, answering one question raises others.
One of the first questions other scientists asked was: How do the bee scouts evaluate the suitability of a potential home site? How do they decide if one potential home site is better or worse than another? It took another “bee person,” Thomas D. Seeley, to take this on as a PhD project in 1975 at Harvard University. Seeley wanted to find out, as he put it, “what makes a dream home” for bees. Almost four decades and two important as well as entertaining books on bees later, he is now at Cornell University and still making important discoveries, after having plumbed the bees’ collective intelligence in their life-and-death decision concerning the best possible home available within a ten-kilometer radius from their original home.
The Homing Instinct Page 11
