Photo by Kathy Keatley Garvey, UC Davis Department of Entomology

By Leon Kreitzman

Gardeners know that plants open and close their flowers at set times during the day. For example, the flowers of catmint open between 6:00 a.m. and 7:00 a.m.; orange hawkweed follows between 7:00 a.m. and 8:00 a.m.; field marigolds open at 9:00 a.m.

In “Philosophia Botanica” (1751), the great taxonomist Carl Linnaeus proposed that it should be possible to plant a floral clock. He noted that two species of daisy, the hawk’s-beard and the hawkbit, opened and closed at their respective times within about a half-hour each day. He suggested planting these daisies along with St. John’s Wort, marigolds, water-lilies and other species in a circle. The rhythmic opening and closing of the plants would be the effective hands of this clock.



Plants have carefully timed routines determined by internally generated rhythms. In 1729, Jean-Jacques d’Ortous de Mairan, a French astronomer, put a Mimosa plant in a cupboard to see what happened when it was kept in the dark. He peeked in at various times, and although the plant was permanently in the dark its leaves still opened and closed rhythmically – it was as though it had its own representation of day and night. The plant’s leaves still drooped during its subjective night and stiffened up during its subjective day. Furthermore, all the leaves moved at the same time. It took another 230 years or so to come up with the term circadian – about a day – to describe these rhythms.

In a similar vein, tobacco plants, stocks and evening primroses release their scent as the sun starts to go down at dusk. These plants attract pollinating moths and night-flying insects. The plants tend to be white or pale. Color vision is difficult under low light, and white best reflects the mainly bluish tinge of evening light.

But plants cannot release their scent in a timely manner simply in response to an environmental cue, like the lowering of the light levels. They need time to produce the oils. To coincide with the appearance of the nocturnal insects, the plant has to anticipate the sunset and produce the scent on a circadian schedule.

Flowers of a given species all produce nectar at about the same time each day, as this increases the chances of cross-pollination. The trick works because pollinators, which in most cases means the honeybee, concentrate foraging on a particular species into a narrow time-window. In effect the honeybee has a daily diary that can include as many as nine appointments — say, 10:00 a.m., lilac; 11:30 a.m., peonies; and so on. The bees’ time-keeping is accurate to about 20 minutes.

The bee can do this because, like the plants and just about every living creature, it has a circadian clock that is reset daily to run in time with the solar cycle. The bee can effectively consult this clock and “check” off the given time and associate this with a particular event.

Honeybees really are nature’s little treasures. They are a centimeter or so long, their brains are tiny, and a small set of simple rules can explain the sophisticated social behavior that produces the coordinated activity of a hive. They live by sets of instructions that are familiar to computer programmers as subroutines – do this until the stop code, then into the next subroutine, and so on.

These humble little bees have an innate ability to work out the location of a food source from its position in relation to the sun. They do this even on cloudy days by reading the pattern of the polarization of the light, and pass this information to other bees. In the dark of the hive, they transpose the location of a food source in the horizontal plane through the famous “waggle” dance into communication in the vertical plane of the hive.

Honeybees can tell their sisters how far away the food is up to a distance of about 15 kilometers. For good measure, they can also allow for the fact that the sun moves relative to the hive by about 15 degrees an hour and correct for this when they pass on the information. In other words, they have their own built-in global positioning system and a language that enables them to refer to objects and events that are distant in space or time.

German scientists in the early part of the last century called this ability of bees to learn the time of day when flowers start secreting nectar and visit the flowers at appropriate times Zeitgedächtnis, or time-sense. But the species of flowers in bloom, say, this week, is likely to be replaced by a different species at a different location next week or the week after. The bee needs a flexible, dynamic appointments system that it continually updates, and it has evolved an impressive ability to learn colors, odors, shapes and routes, within a time frame, quickly and accurately.

While the initial dance by a returning scout bee informs her sisters of the location and distance of food plants and the quality of their nectar, bees that visit the food source learn to synchronize their behavior with daily floral rhythms, foraging only when nectar and pollen are at their highest levels. At other times, they remain in the hive, conserving energy that otherwise would be exhausted on non-productive foraging flights.

Although most animals, including humans, cannot sustain long-lasting periods of activity without circadian rhythms, honeybees have developed a marked flexibility in their circadian rhythm that depends on the job they are doing. Whereas a particular circadian determined behavior is usually fixed to a certain phase of the cycle, in honeybees the circadian rhythm is dependent on the job the bee is doing.

Adult worker bees perform a number of tasks in the hive when they are young, like caring for eggs and larvae, and then shift to foraging for nectar and pollen as they age. However, if the hive has a shortage of foragers, some of the young nurse bees will switch jobs and become foragers. The job transition, whether triggered by age or social cues, involves changes in genes in the honeybee brain; some genes turn on, while others turn off.

Young worker bees less than two weeks of age who typically nurse the brood around-the-clock display no circadian rhythms. Older workers (more than three weeks) typically perform foraging activities and have strong circadian rhythms that are needed for the time-compensated sun-compass navigation and timing visits to flowers.

Recent research in Israel has shown that when young worker bees are removed from caring for the brood and placed in individual cages, they rapidly show circadian rhythms in their behavior. Newly emerged bees isolated in individual cages typically show circadian rhythms in locomotor activity when at 3 days to 14 days old, ages at which most bees in the hive perform around-the-clock nursing activities as mentioned above. Older foragers who revert to nursing duties switch back to around-the-clock brood care activity similar to that of young nurses in typical colonies.

The molecular clockwork mechanism that produces the circadian rhythm works by a series of feedback loops in which the proteins produced by several genes feedback to repress their own production. It is a complicated system, but the end result is a near-24-hour cycling in the levels of various proteins that in turn result in the cycling of the secretion of hormones and other substances.

It seems that there is a plasticity, or flexibility, in the organization of this molecular clockwork mechanism in honeybees, and that the social factors that influence division of labor in honeybee colonies are important also for the regulation of this circadian mechanism. As there is mounting evidence for increased pathologies and deterioration in performance when around-the-clock activity is imposed on most animals, including humans, detailed study of the plasticity of the circadian organization in honeybees may provide pointers for ways for us to have our 24/7 cake and eat it.

Honeybees are remarkable not just for the organization of their circadian clockwork. James Gould of Princeton first studied bees as an undergraduate. It was his pioneering study that showed conclusively that Karl von Frisch, who won a Nobel Prize for elucidating the waggle dance, had been right in concluding that the dance was a means of conveying information.

Ironically, an allergy meant that Gould had to stop working directly with the creatures, but his respect for them is enormous. As he has pointed out:

When a human decides whether to recommend a restaurant, taking into account its menus, the tastes of the friend being advised, the cost of the food, the distance to the establishment, the ambience of the dining room, the ease of parking and all the other factors that enter into such a decision, we have little hesitation in attributing conscious decision-making to the calculation. When a small frenetic creature enclosed in an exoskeleton and sprouting supernumerary legs and a sting performs an analogous integration of factors, however, our biases spur us to look for another explanation, different in kind.

We have been exploiting honeybees for thousands of years by systematically robbing them of their honey. The least we can do is take proper care of these wondrous creatures. Instead we are killing them off in their billions through our befouling of their environment. The honeybee brain has only a million or so neurons, several orders of magnitude less than ours. It is a moot point as to whether humans or honeybees make the best use of their neuronal resource.

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NOTES:

For a discussion about how bees know what to do, and when, see the appropriately titled paper by Pahl M., Zhu H, Pix W., Tautz J., Zhang S. “Circadian timed episodic-like memory – a bee knows what to do when, and also where ” J Exp Biol. 2007 Oct, 210(Pt 20):3559-67.

For circadian plasticity see Shemesh Y., Cohen M., Bloch G. “Natural plasticity in circadian rhythms is mediated by reorganization in the molecular clockwork in honeybees” FASEB J. 2007 Aug;21(10):2304-11.

James Gould quote from Gould, J. L. & Gould, C. G. (1999) “The Animal Mind.” W. H. Freeman, New York.