by Dave Goulson
The most intriguing supposed mate-location behaviour used by bumblebees is often called ‘patrolling’. Charles Darwin was deeply interested in this, and employed his many children as convenient and cheap labour to help him study patrolling bumblebees in his garden in Kent. He had noticed streams of male garden bumblebees passing along the hedges and ditches, generally all heading in the same direction and passing by every few seconds.
‘I could only follow them [the male bees] along this ditch by making several of my children crawl in, and lie on their tummies, but in this way I was able to track the bees for about twenty-five yards.’
I guess the children should have counted themselves lucky that he didn’t send them up to sweep out the chimneys too. Darwin noted that the bees would pause every few yards at what he described as buzzing places, before continuing along their route. To make it easier to see the bees as they flew, he equipped his children with sugar-sprinklers filled with flour, with which they sprinkled the bees as they passed, giving them a ghostly white appearance.
‘The routes remain the same for a considerable time, and the buzzing places are fixed within an inch. I was able to prove this by stationing five or six of my children each close to a buzzing place, and telling the one farthest away to shout out “here is a bee” as soon as one was buzzing around. The others followed this up, so that the same cry of “here is a bee” was passed on from child to child without interruption until the bees reached the buzzing place where I myself was standing.’
Fascinatingly, Darwin found garden bumblebee males patrolling more or less the same route in successive years, despite the fact that male bees do not survive from one year to the next.
Since Darwin, many other researchers have described patrolling in a range of other bumblebee species, including white-tails, buff-tails and red-tails. Scientists in Scandinavia seem to have taken a particular interest in this subject in the 1970s and 1980s, and thanks to their efforts, we now understand much more about this behaviour. Different species seem to prefer to patrol routes at different heights, which perhaps helps them to avoid accidentally mating with members of other species. For example, red-tailed bumblebees prefer routes across the treetops, while garden bumblebees patrol routes low to the ground, presumably explaining why it is garden bumblebees that are most often seen patrolling by humans. The males mark out the route in the morning, pausing every 5 or 10 metres to paint a pheromone on to a twig or leaf. The pheromones are produced in the labial glands inside their head, and painted on to the chosen object using a beard of bristles on their mandibles. Each species has a distinctive pheromone blend, which once again presumably helps to avoid confusion. These pheromone marks become the ‘buzzing places’ described by Darwin, where later in the day the bees simply pause and hover briefly. Each male patrolling a circuit will paste a different object at each buzzing place, and so will hover in a slightly different place, but all follow the same broad route. Routes are typically 200 or 300 metres long and male bees are swift fliers, so each bee can repeat the circuit every few minutes.
This elaborate and remarkable behaviour has only one conceivable purpose: to attract a mate. We presume that the pheromones attract virgin queens, and that the males circulate as fast as they can to maximise their chances of being the first to find any queen that comes along. However, queens are seldom seen to show any interest. My best guess is that when one does come along, she is rapidly found by a male and they quickly disappear off into the undergrowth to mate, so one would have to be very lucky to see it happen. I have tried collecting the pheromone from several dozen male red-tailed bumblebees by squashing their heads in a suitable solvent,21 then pasting the concentrated pheromone on to fence posts on the edge of Yew Tree Hill nature reserve in Hampshire. This area teems with red-tails so there should have been new queens around, but none came to my pheromone lures. Perhaps if I had painted the pheromone on to the tops of trees, where the males normally patrol, this would have worked.
It remains a mystery how males come together and agree the route, whilst the persistence of these routes over successive years adds an additional puzzle. Perhaps traces of the pheromones linger from year to year, or perhaps some physical attributes of the landscape – for example the shape, size or orientation of a particular hedge – are inherently suitable for a patrolling route in some way that is beyond our ken and so attract males year on year.
Hilltopping and patrolling are not the only strategies used by male bumblebees in apparent attempts to find mates. Males of a few species seek out nests from which virgin queens are emerging, and then hang around the entrance. How they find the nests, we do not know – I would guess it is probably by smell. When studying bumblebees in the Outer Hebrides, one of my PhD students, Ben Darvill, once observed a swarm of male moss carder bumblebees outside a nest. He wondered whether they were hanging around their own nest, perhaps with a view to making incestuous advances towards their sisters, and so took DNA samples of the males and some of the female workers. It is relatively straightforward to test whether bees are siblings using genetic markers. These were not, and neither were most of the males brothers of one another – it seemed that the males had come from a variety of other nests.
This is not to say that male bumblebees are averse to incest, as another of my PhD students, Penelope Whitehorn, has found. Penelope, a pretty and terribly well-spoken girl from Oxfordshire, spent much of her PhD encouraging brother and sister bumblebees to mate and then studying the consequences. She placed virgin queen buff-tailed bumblebees in cages with either a brother or an unrelated male, and found that the male bees showed no scruples whatsoever, vigorously attempting to copulate with the queen regardless of whether she was their sister or not. On the other hand, the queens were a little more restrained; although they often did allow their brothers to mate with them, on average they held out a bit longer when confined with a brother than when with an unrelated suitor. This all makes perfect sense. Males of most animals are very unfussy about whom they mate with, because they can mate many times and it costs them little – just some sperm. On the other hand, females often mate rarely and invest a huge amount in rearing their young, so they have a strong incentive to ensure that their offspring are sired by a healthy, attractive and unrelated father. Hence they tend to be much more picky. Breeding with close relatives is particularly risky since it can lead to genetic problems in the offspring, so most animals have mechanisms to avoid it if they possibly can.
Males of most common UK bumblebees do not swarm outside nests, but those of our newest species, the tree bumblebee, do so with great enthusiasm. This species invaded Britain from France in 2001 – quite by chance I was the first person to catch one here, when out hunting for bees in the New Forest. It is a very pretty and distinctive little bee; chestnut brown and black with a white bottom. The name derives from their penchant for nesting in holes in trees, and they also readily take over tit boxes. So far as we know this was a natural invasion, and they seem to be doing no harm. The press showed some interest in the arrival of this new species and dubbed it ‘Le Bee’, even speculating that it might have a distinctive French buzz, which sadly it does not.22 Tree bumblebee males swarm in their hundreds around nests, and since the nests are often in garden tit boxes, this can cause considerable alarm. Of course male bees cannot sting so they pose no danger, but it is not always easy to convince alarmed homeowners not to call in Rentokil.
There is one mate-location strategy used by bumblebees which I have not yet seen, largely because none of our UK bees do it. Only a handful of species do, and the males of all of them have distinctively large, bulging eyes. Three such boggle-eyed beasts can be found in North America – the Nevada bumblebee, the brown-belted bumblebee and the red-belted bumblebee – and these have been studied in some detail by Kevin O’Neill of Montana State University. The males select prominent perches in the early morning, and paste them with pheromones in the same way as do the patrolling species. As the day warms up, they sit upon their perch
and wait for females to heave into view. Despite their large eyes, they don’t seem able to distinguish queen bees from other large insects, so they dart out indiscriminately at any passing creature of roughly the right size. If it is a queen of their species they then try to grab her in flight, and subject her to an enthusiastic sexual assault in mid-air. O’Neill found that the pairs often flew away locked together, and he couldn’t be sure whether they mated or not. Some couples crashed to the ground and these he was able to watch, but in most cases the female was able to shake or kick off the male and escape by scurrying into dense vegetation. The males are fiercely aggressive towards one another, attempting to drive rivals from nearby perches or fighting to oust each other from the best perches, and these fights can result in serious injuries. Despite this the strongest males can hang on for a long time – O’Neill found one male on the same perch for twenty-six consecutive days.
Most of the research on bumblebee pheromones and mating behaviour has focused on males, but some fascinating and slightly gruesome studies carried out by John Free in the 1970s showed that virgin queens also produce a sex pheromone. Free was a great expert on the behaviour of honeybees and bumblebees who worked at Rothamsted Experimental Station (now Rothamsted Research) in Harpenden. He published dozens of papers on bees over forty-five years from the 1950s to the 1990s, and he has a particular interest in pheromones. Free found that if he tethered live, virgin bumblebee queens near the ‘buzzing places’ used by patrolling males, they were quickly located and courted. If he tethered old, mated queens, workers or males in the same places, the passing males very sensibly showed no interest. He went on to discover that males would happily attempt to mate with freshly killed virgin queens. Free reasonably assumed that the males could distinguish virgin queens from mated queens by smell; after all, they look the same. To determine which part of the queen produced this smell, he experimented with removing body parts from dead virgins. Males were undeterred by the removal of most body parts, but seemed unwilling to mate with decapitated queens. You might put this down to squeamishness, but if the headless bodies were smeared with chemicals squeezed from the head then they once more became attractive and the males resumed their amorous advances. Males were not completely indiscriminate; when presented with crude dummies smeared with the odour of virgin queens they showed brief interest, but quickly departed without attempting to mate, indicating that smell alone is not enough to keep them interested for long.
We should not judge males harshly for their fairly relaxed attitude as to what constitutes an eligible mate; with only a one-in-seven chance of mating at all in their life, they cannot afford to be especially fussy. Because mating in bumblebees is rarely seen, it tends to provoke considerable excitement when it is. I have been sent several photographs of male bees clinging enthusiastically to the back of a queen of entirely the wrong species, although in these circumstances it seems that they rarely persuade her to cooperate. Sometimes several males of an assortment of species will be pictured pushing and shoving one another for pole position, a tangle of legs and fur on the back of a disgruntled queen.
Although I have never observed successful courtship and copulation in the field, bees do mate readily enough in the lab. I recently played host to a Bangladeshi researcher named Ruhul Amin who was particularly interested in courtship and mating in bumblebees, and he spent many happy hours in a windowless room in the basement at Stirling watching buff-tailed bumblebees mate. He found that older males took longer to mate than young ones, but that they had better endurance, mating for longer. He offered some lucky males a chance to mate with a second virgin immediately after they had finished with the first, and found once again that older males took longer to perform in these circumstances, although when they eventually got going they mated for longer. He also found that bigger males mated more swiftly but had less endurance.
Amin found that during courtship the males invariably climbed on to the back of the queen. He observed that they held the thorax either side of her head with their forelegs, while stimulating her nether regions with their hind legs. The queens are much larger than the males, so the males are unable to force them to mate if they are not interested. Fascinatingly, when Amin confined a queen with two males, he found that on average the successful male was not the youngest or the biggest, but the one with the longest fore- and hind legs. We presume that longer limbs make them better able to hang on to and simultaneously stimulate the female.
As with most insects, the male bee has a powerful pair of claspers at the tip of his abdomen, with which he grips the female, and a tube-like endophallus which is inserted into the female and carries the sperm. Once his claspers are locked on, he lets go of the female with his legs and ‘lies back’, legs folded in front of him as if meditating, with the only point of contact between himself and the female being the genitalia. Mating typically lasts for about half an hour. Sperm is transferred in the first minute or two, but after that the male pumps a sticky glue into the queen, forming a ‘mating plug’, which prevents her from doing it again, and explains why queen bumblebees generally mate only once.
As you may have gathered, in general I think that bumblebees are among the most fascinating of creatures, and their mating habits are certainly intriguing and enigmatic, but in this one area I have to concede that their cousins the honeybees have them trumped. Unlike bumblebees, honeybee queens mate a dozen or so times, all during a single nuptial flight made early in life. Each young queen releases a pheromone which is enormously attractive to the males – known as drones – who eagerly swarm after her. They mate in mid-air, the male grasping the female’s abdomen with his claspers and then explosively squirting sperm into her. This explosion produces an audible pop and ruptures the male’s genitalia, usually causing fatal damage so that he falls to the ground and quickly expires, leaving behind fragments of his genitalia still attached to the queen. She continues her flight, and is swiftly mounted by a second male who scrapes off the remains of his predecessor before repeating the process. The new queen continues until she has stored enough sperm for a lifetime of egg production, at which point she returns to the nest, leaving behind a trail of dead lovers.
CHAPTER THIRTEEN
Does Size Matter?
I beg a million pardons. Abuse me to any degree, but forgive me: it is all an illusion about the bees. I do so hope you have not wasted any time for my stupid blunder – I hate myself, I hate clover and I hate bees.
Charles Darwin, letter to John Lubbock, 1862
In 2001 I took on a new PhD student named James Peat. James had been an undergraduate at Southampton, and my tutee. From a slightly posh family in Dorset, James was a bit of a charmer and a ladies’ man, often sporting amusing facial hair. I’d always found him to be very entertaining, with a quirky, lateral view of the world, and I thought he might be just what my research group needed. Among other things, he is the only man I’ve ever known who insisted on making all of his own trousers.
I decided to let James loose on a topic which had intrigued me for many years. Bumblebees differ from their close relative the honeybee in that the workers are enormously variable in size. The largest workers are roughly ten times heavier than the smallest, yet all live alongside one another in a single nest. Most insects vary little in size: one adult peacock butterfly is much the same size as another; and the same can be said of grasshoppers, dragonflies or stag beetles, for example. Even the relatives of bumblebees – wasps, stingless bees and honeybees, – tend to be more or less uniform in size. The only group of insects which exhibits something similar to bumblebees are the ants. In some ant species, most notably leafcutters from the rainforests of South America, the workers vary enormously in size and this relates to the jobs that they perform. The biggest workers are monsters, with huge scimitar-shaped jaws suspended from large heads packed with muscle. Their job is to defend the nest against large vertebrate predators such as anteaters or insectivorous birds and lizards, and they can deliver a ferocious bite. The
medium-sized workers forage for food, forming trails through the forest and up the trunks of trees to the foliage, where they snip semicircles of leaf to carry back to the nest. Collectively, they can strip a huge rainforest tree of leaves in a single night, so each night they set out in a different direction.
Tiny workers tend to the queen and brood, and also chew up the leaves brought in to the nest to feed to their fungus garden, in chambers deep underground. Leafcutter ants cannot digest leaves directly, so they have evolved a remarkable symbiosis with a species of fungus found only in their nests. The white, fluffy fungus turns unpalatable leaves into digestible fungal fronds, which are harvested by the tiny workers and fed to the rest of the ants in the nest. Some of the tiny workers also hitchhike on the backs of the foragers collecting leaves, and are thought to protect them from parasitoid wasps and flies, which would otherwise inject their eggs into the foragers.23
It clearly makes sense for different workers to have bodies suited to their jobs; the tiny workers would be hopelessly ineffective if called upon to attack an anteater, while the giant soldiers would not be small or nimble enough to care for the fungus garden. Does a similar line of reasoning explain why bumblebee workers vary so much in size?
The first step towards finding out the answer to this question was to determine if different-sized bees do different jobs. In fact it had long been suspected that the smallest bees tended to stay in the nest, and the bigger ones went foraging for food, but this had not previously been quantified. To do so, we simply reared up thirty buff-tailed bumblebee nests, then placed them out in the field and opened the doors to their boxes. These boxes consisted of an outer cardboard shell with a removable inner plastic box, and they were fitted with two doors, one which allowed bees both in and out, and the other with a valve which only allowed them in. We left the nests to settle down and forage naturally for four weeks, after which we returned in the middle of the day, when foragers were likely to be out doing their thing, and shut the doors. We then replaced the inner plastic box with an identical but empty one, and opened only the door which allowed bees in. Foragers returned home for the next few hours, loaded with food, but found that they had entered an empty nest from which there was no escape. James then had the tedious job of using Vernier callipers to measure the size – the width of the thorax – of all the bees from each nest, both those that were inside the nest when we sealed the door, and those that had been out foraging; about 4,500 bees in total, roughly one-third of which had been foraging.
