Deep in the Mines of Bees
Crowded neighborhoods
In Tallahassee lawns and parks, dozens to thousands of small heaps of soil, each with a hole in the center appear annually during the waning days of February, as if by magic. Unnoticed by most, the scale of this sudden activity is astounding, for the piles appear in large aggregations, each with far too many piles for a direct count. In a small park nearby, forty small random samples averaged 36 piles per square meter (up to 80). Walking the periphery of the aggregation showed it to cover nearly 1000 square meters, and thus to contain about 22,000 of these earthen piles. Another park nearby had an even larger aggregation, and cruising neighborhoods often found smaller aggregations in front lawns.
As I strolled through this aggregation on a sunny day, thousands of small bees zipped and zigzagged in a crazy layer swarm about ankle height. Catching a few for identification was easy, and peering at the holes in the dirt piles, it wasn’t long before a little face and head appeared, pondering whether the world above was safe enough to emerge. Capturing a couple of these was not really that hard either and showed them to be much larger than the swarming bees, suggesting that these were females, and the swarming bees were males. As each female bee departed from her burrow, she made a few orientation sweeps, ignored the swarming males and then headed off into the distance.
Identifying bees can be frustrating and confusing. Thousands of species of solitary bees in several families nest in the ground, so that fact doesn’t get you very far. Identification to genus requires that you evaluate subtle features of wing venation, head/facial details, and most critical, patches of fine hairs on the face. After all this, congratulations, you have identified these bees to the family Andrenidae, of which there are “only” 1200 species in the United States, and then pinpointed it to the genus Andrena, of which Florida is home to 35 species. Identifying the bees to species takes an expert with many years of experience, not to mention a reference collection and a large amount of patience. I was more than satisfied to narrow the identity to one of these 35 species of Andrena. Here is the face of the female of one of these species showing the diagnostic patch of facial hair.
These thousands of males zipping over the nest aggregation were a mating swarm, each male buzzing back and forth randomly, waiting for a chance to mate with a female as she left her burrow. Some of the more impatient males entered a burrow only to reappear, apparently unsuccessful, a few moments later. This was a game as old as sex itself--- males desperately vying for a chance to mate with a female, their only chance to leave descendants behind. But in most animals, females hold the stronger hand because they invest a lot more in eggs, provisioning, and/or parental care than males invest in cheap sperm.
This is the battle between the sexes, for what benefits the reproductive future of one sex does not necessarily benefit the other, and each sex tries to maximize its own reproductive success. The “game” is messy, fluid, and often unpredictable. All sexually-reproducing animals, including humans, are players in this game.
But in the Hymenoptera (ants, wasps, bees), this battle has an additional wrinkle. Whereas in most animals, males and females are produced in a 1:1 ratio, in the Hymenoptera, the ratio is flexible and under the control of the female. This is because males develop from unfertilized eggs (and are thus haploid), while females develop from fertilized (diploid) eggs. Thus, by either fertilizing or not fertilizing the egg from her store of sperm, females can adjust how many males to produce and thus the total to invest in male offspring. How she makes this decision is still a deep mystery, but it gives her another tool in the game of reproduction. It is unlikely that she makes this decision consciously, and to believe she does reveals a peculiarly human conceit. In our Andrena, just for a start, males are one-sixth the size of females (and thus much cheaper), and on top of that, depending on conditions and season, she can produce more males than females. The exact number is a gamble.
Andrena bees, like all bees, are totally dependent on flowers, having evolved with them for over a hundred million years by trading pollination services for pollen and nectar. Each Andrenid bee species specializes on a narrow range of flower species, and is only active for the short season when “their” flowers bloom. Thus, there are early spring bees, summer bees, early fall bees etc. Perhaps that that is why there are so many species of andrenid bees and of Andrena spp.
There didn’t seem to be a lot blooming within easy sight of the aggregation in February , mostly trees in the rose family, such as hog plum, pear, and so on. The scarcity of blooming trees near the aggregation suggested that the bees must be flying much farther than I could see, possibly miles.
The females collect pollen on their very hairy bodies, especially their hind legs, and are essentially flying, pollen-saturated carpets. They imbibe nectar and store it in a crop from which they can regurgitate it. Upon returning to their burrows, they scrape off the pollen, mix it with regurgitated nectar and form it into a ball on which they lay an egg. Individually, because the bees are small, this may not seem like a lot of pollen and nectar, but there are at least 22,000 females, each collecting provisions for (I am guessing) ten or twenty offspring. If the average bee weighs 0.1 g, and the pollen to tissue conversion is 25%, then each bee must provide two to four grams of pollen and nectar, and the bees altogether must collect 44 to 88 kg within flight distance of the aggregation. Considering the modest blooms around the park vicinity, it seemed like a mystery, and brought home once again how different our worlds are from those of other (especially small) creatures.
But there are more mysteries in sight. Here were 22,000 bee nests all scrunched into an area of 1000 square meters despite the existence of many-fold that area in the park (see image above) that was apparently suitable. The scientific literature declares emphatically that these bees are not social, that is, that each nest is created by and serves a single, solitary female bee. If this is indeed a fact, it means that each time the female returns from a foraging trip, she must find the nest that is hers and only hers. In the picture below, you can see what she is up against, because there are often neighbors whose nest entrances are only centimeters away. Study the picture and ask yourself whether you, after an hour of buzzing from flower to flower and tree to tree over distances of (at least) hundreds of meters, could find the same nest again. And yet, the bees do. Imagine the navigational ability required, and you will surely be impressed.
Not less impressive is that this tiny bee, with a brain of a couple of tens-of-thousands of cells, performs several quite different types of tasks in the course of reproduction, and does them in the correct sequence--- precise navigation and orientation in a wide world, locating and collecting specific provisions for her offspring and forming these into a ball of specific composition, excavating soil to produce a precise nest architecture, lining the cells, mating and laying eggs, sealing each cell to last the duration of most of a year. Then repeat. What competence!
But in case you are still not impressed, let’s talk about the burrow this little bee inhabits. That pile of dirt on top of the burrow was excavated from below, so it should tell us something about the excavated volume. To reveal the nest’s depth, volume, and shape, I made several casts by pouring molten zinc into the opening, then digging out the frozen cast. A representative cast is pictured below. Inside the white circle is a magnified view of a male and female. The average diameter of the burrow was about 8 mm, about double the diameter of the female. Conclusion: a female Andrena 12 mm long from head to tail appears to have excavated a burrow more than 850 mm deep, with a volume of about 40 ml and an excavated soil weight of 60 g (for the entire aggregation this would be 1.3 metric tons). For perspective, our individual bee weighs a bit over 0.1 g, or 1/600th of the soil removed to form the burrow. This was as if I had excavated 22 metric tons of soil in one short event. Can one little bee really do that? Or is there another possibility? Is it possible that the burrow is inherited at birth, a sort of trust fund for a bee baby, a leg up in the struggle for reproduction?
The cast above was made while the nests were still open and the bees still foraging. After the end of this season, the rain had washed away all surface evidence of the bees’ presence, but of course they must have left offspring behind underground.
When I shaved off the top 10 cm of turf, I found, not collapsed and dirt-filled burrows, but abundant open burrows going to depth. As before, I filled several of these openings with molten zinc, and upon excavating these casts, I found that they were very much the same as those of the open burrows during the foraging season.
With a simple scrape of a shovel, I had come to the inescapable insight that the burrows that had hosted so much bee traffic were legacy burrows, reused by generation after generation, year after year. It has been more than a quarter century since I first noticed these aggregations and they have reappeared every year. The firmness of the high-clay soil assured that the burrows remained open over the course of each year’s “gestation.” The stability of this soil could be the reason why so many bees aggregate in such a small area--- multi-generational success made possible by the stable burrows may simply be higher there, boosting the population over many generations.
The second insight was that the piles of soil that made these aggregations so conspicuous derived only from the lateral cells that the females dug for their brood, not from the entire depth of the burrow. Whew! Maybe my digging performance was not so pitiful compared to that of a tiny bee. The brood cells that the bees stocked with a pollen ball were seldom cast because, once completed, the mother sealed them, thus preventing the molten zinc from filling them.
The consistently stepped appearance of the deepest section of nest, neater in some than others, was intriguing. My hypothesis is that the female digs a horizontal brood cell to one side at the bottom of the burrow and plugs it, as in the illustration below, then deepens the shaft a little for the next cell. Each additional cell is thus offset along the shaft. Only the open volume would be filled with zinc during casting.
In such firm soil, I was unable to specify the exact relationship of the brood cells with the shafts, but I collected several brood cells with larvae of the next generation, waiting to make their appearance in the upper world at the end of the next February, almost a year later. Because by late April the nests had been closed for at least a month, the larvae had eaten the pollen balls and were fully grown. Each cell was lacquered with a smooth, secreted lining that helped keep the cells largely intact and the brood healthy for nearly a year. They would live on the metabolic reserves gained from their only pollen and nectar meal, and as spring approached, they would draw on this reserve to transform into a pupa and finally, an adult bee. Each adult bee would then dig his or her way through the earthen plug of the cell and the plug at the top of their burrow and begin all the complex behavior it takes to produce the next generation, beginning the cycle all over again.
Clearly, each generation inherits the burrow from the previous generation, but this raises many perplexing questions. If a female produces more than one daughter, which one inherits the burrow? The first, the biggest, the last? Do they hire apid lawyers and fight over ownership? Or do multiple daughters share the burrow without social cooperation, that is, does each female raise her own offspring, paying no attention to her sister? How would we know? The truth is, we wouldn’t, because all bees look alike to us, and the only way to answer the question is to mark bees as they exit and return to the burrow. This would also establish whether the bees return to their own nest only.
For this year, I have squeezed out what knowledge I could, given the short season, my late start, and the inaccessibility of so much of what the bees do underground and in their flight rounds. When February 2025 rolls around, I will have an impossibly long list of questions. Will the aggregation expand, contract or remain stable? Are nests on the fringes of the aggregation newer, therefore shorter, dug by bees without a claim in the main aggregation? What flowers do the bees collect pollen from? If I can get the cooperation of colleagues who can analyze DNA, are neighboring bees more related than distant ones? If more than one bee occupies a burrow (determined by marking), are they siblings? Unrelated? Does each female mate only once? What is the ratio of male to female brood? Are the burrows as stable as they seem, remaining open for perhaps years?
Karl von Frisch, the discoverer of the dance language of the honeybee said that honeybees are like a magic well--- the more you draw from the well, the more there is to draw. I think this is true for the natural history of every species, including my miner bees. Or to put it less poetically, new questions appear like mosquitos at dusk. Maybe next year I will be able to swat down a few questions and draw some more from this magic well. My shovel is ready, and my fingers are crossed.
Spectacular work and post, Walter -- a classic in natural history, replete with your inquisitiveness, determination, knowledge, and still more questions for the next field season. Perhaps you'll publish on this? And might you get any specimens identified to species?
I noticed that there is quite a large patch of clover blooming around the aggregation. Would that be the bees' source of nectar? The genus name Andrena makes me think of a high school friend who was named Aurelia by her father, a professor at the nearby university. I loved her name and told her that I would consider using it to name a future daughter. Aurelia told me that it wasn't the Latin meaning of the name (golden) that inspired her dad but rather the moon jellyfish he once studied. After hearing her say that, even though I still loved her name, I opted for a more common name for my daughter when she was born.