by Dave Goulson
As I have mentioned, badgers are among the best-known predators of bumblebee nests; they are seemingly impervious to stings and consume the entire nest, bees and all, if they can dig it up. When I have placed artificially reared bumblebee nests in the field I have often had them torn to shreds by badgers, for they are powerful animals, and Perthshire farmers who use commercial bumblebee boxes for raspberry pollination often suffer from similar problems. Luckily for Steph’s nests, which were mostly in and around the campus of Stirling University, there appear to be no badgers here. She did have other larger mammals such as squirrels investigate the nests, and hedgehogs regularly came by and snuffled around the entrances, but they were too big to get in and not good enough at digging to burrow down. On one occasion the camera recorded a cow’s hoof standing on the entrance hole and squashing it, but the bees soon repaired the damage. Foxes and weasels have also been claimed to attack bumblebee nests, but we have no idea how often or how serious these predators are, and Steph recorded neither visiting her nests. In North America, skunks are said to be partial to bumblebees, whilst in Iceland, escaped mink are thought to be important predators. Of course these days there are plenty of escaped mink in Britain, but whether they are eating bumblebees is not known.
Perhaps Steph’s most exciting discovery was that great tits do not confine themselves to plucking bumblebees from flowering trees. A number of Steph’s nests were regularly visited by great tits, which would sit by the entrance, picking off foragers as they came and went, and returning day after day. In general it seemed to be the biggest nests that were attacked, probably simply because these had more traffic going in and out and so were easier for the great tits to detect. Other observations of note were bees carrying grubs from their nest and dumping them outside – we have no idea why they do this, but they may have been sickly, or possibly unwanted male grubs. Steph also recorded red-tailed bumblebees entering a buff-tailed bumblebee nest. Again, we don’t know why, but they may be trying to steal honey. This work is in its early days, but we hope to learn much more about the relationships between bumblebees and their nest predators as it goes on.
As well as trying to record predators, Steph has looked into the other less obvious creatures that attack her bumblebee nests. From every nest that she has filmed she has taken weekly samples of faeces from the workers. Just as a doctor might inspect a stool sample to help diagnose a human illness, Steph screened these samples for gut diseases. Bumblebees can suffer from a range of nasty gut infections including both protozoans and fungi, some of which give them chronic diarrhoea, and these infections are usually evident when the faeces are inspected under a microscope. Some of the disease-causing organisms even swim around energetically like tiny tadpoles. Extracting faeces from bumblebees is a fiddly business. If they are contained within a plastic pot they sometimes defecate quite quickly, perhaps because the poor things are scared. Gentle agitation tends to speed the process up but some bees absolutely refuse – maybe they simply don’t need to go. If they do produce a sample, it has to be sucked up swiftly using a tiny glass tube – bee faeces are very liquid – or else the bees tend to stand in it and smear it all over the place.
Steph found that many of these diseases were common – for example almost every single nest she studied was infected by a gut parasite known as Crithidia bombi by the end of the season. Crithidia is a protozoan, related to the organism which causes sleeping sickness in humans and livestock in Africa. It is thought to spread rapidly through direct contact between nest mates, and spreads between nests via flowers, which get smeared with the disease by infected workers. Crithidia doesn’t do too much harm to individual workers so long as they have plenty of food, but if food is in short supply then the disease becomes more serious and can kill them. If young queens become infected they are generally less likely to survive through the winter and manage to found a new nest in spring, but young queens appear to have especially strong immune systems so they rarely get infected.
Once Steph’s nests died off, she attempted to dig them up to find out more about what had happened to them. This can be hard and frustrating work. I once spent a whole day trying to dig out an unwanted buff-tailed bumblebee nest in someone’s garden. The tunnel turned erratically underground, eventually going under a tarmac road so that I could follow it no further, leaving me with a trench about 10 feet long to fill back in. Many of Steph’s nest tunnels led amongst the roots of large trees, forcing her to abandon excavation. For perhaps half of them, she managed to get down to the nest itself. There was usually rather little left of the original structure. One of the major bumblebee nest predators seems to be the bumblebee wax moth, a small, nondescript cream-coloured moth that lays batches of eggs in bumblebee nests. When the eggs hatch, the caterpillars spin tough silken tubes that protect them from the bees, and tunnel through the nest, indiscriminately consuming wax, pollen, grubs and pupae. In heavy infestations, the nest is completely destroyed, the bees seemingly unable to do anything to fight back. These wax moths also seem to be particularly prevalent in bumblebee nests in gardens, perhaps simply because bumblebee nests are common in gardens so there is plenty for them to eat; 80 per cent of buff-tailed nests that I placed out in gardens in Hampshire were attacked by wax moths, many of them completely obliterated. The majority of Steph’s natural nests were also attacked. Once they have finished demolishing the nest, the caterpillars huddle together to hibernate in a conspicuous white mass of tightly woven silk tunnels, which is often the most obvious thing remaining.
Where nests have not been destroyed by wax moths, there is often much to see. The body of the old queen is usually there, sometimes with those of other queens who attempted to usurp her. Corpses of workers litter the nest, scattered amongst the wax nectar-storage pots and empty pupal cocoons. Queen cocoons are larger than those of workers or males, and so the number of them gives an indication of the number of new queens produced by the nest. Steph found that many nests produced few or no queens, but just a few very large nests managed to each produce more than one hundred.
Usually there are also lots of other insects in old bumblebee nests, so called commensal organisms which have no particular effect on their hosts but live alongside them, scavenging on bee faeces and other scraps; these include various flies, moths and beetles. There is often an assortment of maggots – fly larvae – of varying sizes wriggling around. Volucella bombylans, for instance, is a beautiful large furry hoverfly that mimics bumblebees; it occurs in various forms, which resemble different bumblebee species. Sladen observed that this fly is sometimes attacked and killed by the worker bees when trying to enter the nest, but that if this happens the fly immediately lays all of her eggs in her death throes, which the worker bees rarely notice. When the eggs hatch, the tiny maggots scurry away into the bottom of the nest where they can scavenge undisturbed. The beetle Antherophagus nigricornis finds its way into bumblebee nests by climbing on to a flower. It waits there for a bumblebee to arrive, then grabs hold with its mandibles. Being about 5 millimetres long, it is inevitably noticed by the bumblebee but she usually cannot shake it off. Once she gives up and returns to her nest, the beetle drops off and thereafter resides within the nest.
Aside from all of these insects, bumblebee nests almost invariably also contain a multitude of tiny mites. Mites are relatives of ticks and slightly more distantly of spiders; they have eight legs, and the ones found in bumblebee nests are usually tan-coloured. As with the maggots, they are scavengers within the nest. Maggots turn into adult flies, which can readily fly off to locate a new bumblebee nest each year, but mites cannot fly at any stage of their life, which poses a problem for them. Bumblebee nests die off each year, so that any mite left after the bees have gone will soon starve. To solve this problem, some mites climb on to new queens before they leave their natal nest, and then hibernate with them, hoping to colonise the new nest that they will attempt to found in the spring. These mites can be very common, so that many of the bumblebee queens that emerge in
spring have clusters of mites living in the crevices between the thorax and abdomen, behind their head and between the bases of their legs. They look revolting, but most do not actually feed on the bee – they are just hitching a lift. Some smaller mites live permanently amongst the bees’ fur. One very small species actually lives on the back of the larger mites, themselves on the bees, bringing to mind the phrase, ‘A flea hath smaller fleas that on him prey; and these have smaller fleas to bite ’em, and so proceed ad infinitum’ (Jonathan Swift, 1733). These mites probably do very little harm to their hosts, although they must weigh them down a little. Only one species of mite lives exclusively within bumblebees, inside their trachea (breathing tubes), sucking on their blood, and thus presumably they do their host no good at all.
Aside from the mites that hitchhike on queen bees, there is one other bumblebee parasite that specialises in attacking queens. This fascinating but repulsive beast is the nematode worm, Sphaerularia bombi, a distant relative of the pin worms and hook worms that infect humans. The young female worm burrows into a queen bee while she is hibernating in the soil, and takes up residence within her abdomen. Peculiarly, the worm everts her ovaries so that they are outside her body – these then grow enormously by absorbing nutrients from the host, to around 2 centimetres in length. They resemble a knobbly white sausage, dwarfing the rest of the worm’s body which is just visible to the naked eye as a tiny thread attached at the side. Somehow, the worm alters the behaviour of the poor host queen when she emerges from hibernation. Instead of trying to found a nest, she sits around listlessly, occasionally feeding, until May or June and then returns to her hibernation site where she wanders around on the soil surface, defecating. Her faeces are full of a multitude of tiny new worms; a single adult female can produce 100,000 or so. These burrow into the soil where they live for a few weeks, and mate. When the next generation of queen bees burrows into the soil to hibernate, the worms will be waiting for them.
Many other organisms have evolved to parasitise bumblebees. Wasps of the family Braconidae and flies of the family Conopidae lay their eggs in adult bees when they are feeding on flowers, with their larvae then consuming the host from the inside. When infected with the latter, worker bees sleep outside the nest at night where it is cooler, slowing the development of their parasite and so delaying their inevitable death. Flies of the family Sarcophagidae fly into bumblebee nests and give birth directly to maggots (there is no egg stage), which feed upon bumblebee pupae, slowly eating them from the outside. Velvet ants (Mutilidae), not ants at all but ant-like wingless furry wasps, will also walk into bumblebee nests and lay their eggs on bee pupae, which once again are then consumed.
Overall, bumblebee nests support a vast diversity of fascinating and sometimes rather stomach-churning creatures, many of which have been little studied, and about which we know only scraps. Clearly the importance of bumblebees in supporting biodiversity goes far beyond their role as pollinators of wild flowers.
As yet, we do not know how many bees die as a result of predators and parasites, but Steph’s work is beginning to give us some idea. The nests she has filmed suffer from an alarming mortality rate. Many die within a week or two of being discovered, despite Steph taking great care to leave them undisturbed. So far as we can tell, this is natural – many, many queens attempt to start nests in spring, but very few succeed in rearing a large healthy nest. Perhaps as many as 50 per cent of all nests die every two weeks. Fortunately those few nests that manage to grow to a large size then produce many queens – making up for the large majority of nests that have failed. Of course this means there is a delicate balance, and any factor that increases mortality even a little could push a bumblebee species into rapid decline.
CHAPTER TWELVE
The Birds and the Bees
Concerning the bees and the flowers
In the fields and the gardens and bowers,
You will note at a glance
That their ways of romance
Haven’t any resemblance to ours.
Anon.
Since moving to the University of Stirling I have taken to running up a local hill, named Dumyat (pronounced Dum-i-at), every Wednesday at lunchtime. The university campus is lovely, the ugly 1970s buildings hidden amongst trees around a beautiful loch. Just to the south-east rises a steep volcanic plug clothed in woodland, on which has been built the dramatic Gothic tower of the Wallace Monument. The Ochil Hills rise directly from the north-east end of the campus, and form a sharp escarpment running eastwards into Fife, marking the edge of the central Lowlands and the beginning of the Highlands beyond. Dumyat is the westernmost of the Ochils, rising only 400 metres or so, but with spectacular views into the Highlands to the north, to Edinburgh in the east and to Ben Lomond in the west.
I moved to Stirling in 2006, and in the late summer of that year I noticed something a little odd at the top of Dumyat. I was gasping to regain my breath, slumped against the cairn that marks the summit, when I noticed several bumblebees buzzing about. Closer inspection revealed that they were male white-tails. They were not feeding on flowers – indeed, there are no flowers anywhere near the top of Dumyat, just rocks and sheep-cropped grass. It is a fairly bleak and windswept spot – the bees were being buffeted about, but were stubbornly flying into the wind to maintain their position, whilst zigzagging around as if looking for something.
A week or two later I took my family for a walk up to the base of the Wallace Monument, a short but steep climb through the woods, which emerges into a grassy clearing at the top. There were a few flowers about, mostly creeping thistles, and they were covered in male forest cuckoo bumblebees, sometimes two or three to a flower. I was intrigued as to what these gangs of male bees were doing hanging around at the tops of hills. I enlisted the help of two Stirling undergraduates, Jill Young and Liz Sangster, persuading them that they should spend their summer walking up and down a range of Scottish hills while counting the numbers of male and female bumblebees, to see if this was a general phenomenon. They duly did so, and it seems that it is – every hill they climbed had unusual numbers of males at the top, and comparatively few on the slopes and at the bottom.
The explanation for the predilection of male bumblebees for hilltops is most likely that they are engaging in a behaviour appropriately known as ‘hilltopping’, something which has been studied in detail by John Alcock of Arizona State University, now retired but one of the world’s experts on insect mating behaviour. He has devoted his life to unravelling the mysteries of how insects find and choose their mates, doing much of his work in the exciting-sounding but presumably rather inhospitable Sonoran Desert. One recurring theme of his work is that males of many species, including such evocatively named beasts as the great purple hairstreak, the pipevine swallowtail and the tarantula-hawk wasp, aggregate on hilltops where they await the arrival of females. Often the males become territorial, choosing a particular perch and vigorously chasing away other males who encroach on their space. Competition for perches at the very top of the hill, which seems to be the prime location, can be fierce. Females of most insects need to mate only once or perhaps a few times in their life, while males try to mate as many times as they can. In hilltopping species, females that wish to find a mate simply head uphill, confident that when they get to the top there will be plenty of amorous suitors awaiting them. This also provides them with an opportunity to be choosy; they can quickly survey and compare a large number of males, and offer themselves to whichever one of them has the most desirable characteristics. Or, if they are in a hurry, they might simply mate with the male right at the top, on the assumption that he must be the fittest and strongest since he has managed to acquire and hang on to the best spot. With luck their sons will inherit these characteristics too, and will themselves become king of the hill. Once mated, the females quickly depart, usually to lay their eggs, perhaps returning to find a second mate a few days later when they have depleted their sperm stores.
In bumblebees, the males do
not appear to be territorial when gathered on hilltops. They simply hang around, often in amicable groups, drinking nectar when it is available, and presumably attempting to mate with females whenever they appear. The parallels with human behaviour are irresistible, particularly since male bees do little or no work in the nest, leaving all of that to the females. Hilltops seemingly represent the bumblebee equivalent of a nightclub or singles bar, somewhere to check out and chat up members of the opposite sex.
Unfortunately there is a rather crucial aspect in which the analogy falls down. To my knowledge, no virgin queen bumblebees have ever been observed heading for the high ground. Indeed, this is a recurring theme in studies of bumblebee mating behaviour. Prior to Jill and Liz’s work on hilltopping, many other odd behaviours have been described in male bumblebees and interpreted as mechanisms for locating a mate, but virtually none of them has ever been observed to succeed. Actual mating in bumblebees is seldom observed, and usually only once copulation has already started – the process of successful courtship is almost never seen in the wild. In fact, most bumblebee males never do mate. For reasons we do not yet understand, bumblebee nests seem to produce many more males than new queens; on average about seven males for every queen. Since queens generally mate only once in their entire lives, this means that six out of seven males will never manage to mate. As it is their sole function in life, I find this rather sad.
