by Dave Goulson
For the first couple of years the trees weren’t tall enough to poke out of the top of the tube, and I had to peer down to see how they were doing. This, I soon discovered, was a hairy business, because almost every tube contained not just a small apple tree, but also a paper-wasp nest. The tubes seem to provide a perfect, warm and sheltered environment for these wasps, which zoom out of the top of the tube aggressively if disturbed. However, they probably eat any greenfly or other pests on the apples, and don’t seem to do any harm, so they are welcome to their tubular homes as far as I am concerned.
I first came across paper wasps in 1995, when teaching on a field course in the south of Spain. Every year for the eleven years that I was at Southampton University we took all of the first-year biology students for a fortnight to a beautiful corner of Andalucia, about eighty kilometres west of Gibraltar, on the Atlantic coast. It was an epic undertaking, for there were usually more than 100 students, but it was great fun and a wonderful way to enthuse them with the excitement of field biology. The area is extraordinarily rich in wildlife. Rugged, craggy mountains cloaked in cork oaks rise steeply from the sandy beaches and coastal dunes, and griffon vultures soar about the steep cliffs. We went in late March, when the wild flowers are in riotous bloom in the rough meadows, rocky slopes and the damper slacks behind the dunes, and they attract innumerable bees, hoverflies and butterflies, such as the spectacular red, black and white Spanish festoon. This is also the time when birds that have migrated to Africa for the winter return to Europe, and many choose to cross here from Morocco, which is clearly visible across the chilly blue-grey Straits of Gibraltar. Storks, black kites and bee-eaters arrive in large flocks, often looking tired and flying low to the water, for there are no thermals to lift them when crossing the sea. The area is also particularly rich in reptiles: turtles bask on the banks of the streams, viperine snakes hunt the tadpoles of toads and tree frogs in the shallows, skinks, geckos and eyed lizards scamper amongst the sun-warmed rocks, and chameleons perch motionless in the bushes.
Many of the farmers in the area used prickly-pear hedges to separate one rough field from the next. Prickly pears are horrible plants. They are a native of the Americas, and have become very troublesome invasive weeds in other parts of the world, most notably in Australia. They have numerous exceedingly sharp spines and, to make matters worse, the spines are covered in microscopic barbs. This makes them very hard to pull out, once embedded in skin, and they often snap off and then cause festering sores. Having said all this, the prickly pears in Spain do provide excellent refuges for lizards and snakes, which can bask with impunity amongst the spines in full view of the frequent booted eagles that would otherwise love to eat them. They also provide a very popular nest site for paper wasps.
Paper wasps are, of course, not made of paper. They resemble the familiar yellow-and-black social wasps that plague picnic tables in late summer, but they are more slender and delicate in appearance. Their name comes from the material from which they construct their nests, which is, essentially, home-made paper. However, since many other wasps also use paper for their nests, the name isn’t especially helpful. Paper wasps and the common ‘picnic-table’ wasps all make nest material by chewing at dead dried wood and then regurgitating the chewed-wood fragments with saliva, to make a greyish paper from which they can construct the most elaborate combs of hexagonal cells. Garden fence panels and posts and untreated garden sheds all seem to be much favoured by wasps as a source of wood for paper, and they can often be seen – and even heard – chewing away at garden woodwork. The nests of social wasps in the UK can grow to a very large size, sometimes bigger than a basketball, but paper-wasp nests are, like the wasps themselves, relatively small and delicate. They have a single stalk supporting a plate of up to 100 or so hexagonal cells in which the offspring are reared. They make no protective shell around the nest, so that the growing grubs (and their tending by the adult wasps) are easily observed.
We would spend the first week of the field course in Spain teaching the students to identify plants and insects, and then in the second week they would conduct small research projects on a topic of their choice. It was always a bit of a challenge trying to find enough different projects for 100 students, and the paper wasps struck me as a species that could be interesting and fairly easy to study. On my first trip to Spain in 1995 I had not seen paper wasps before, and I spent a little time watching the nests. The wasps seemed to engage in a lot of fighting; they would regularly face one another, eyeball to eyeball on the surface of the nest, and then push and bite until one or other retreated. At the time I didn’t know anything about paper wasps, but this seemed intriguing. What were they fighting over? Did the same wasp always win? I got a couple of students to do a project that aimed to find out. They marked the wasps with different-coloured paints so that they could recognise individuals, and then watched the nests all day long.
It did seem that fights had predictable outcomes – one large female seemed to be the boss, and she would shove, bully and harass the other females on the nest. What was even odder was that new, unmarked wasps, which had not been seen before, seemed to turn up regularly on the nests, even though it was clear no pupae had recently hatched. Some of the marked wasps also disappeared, but we presumed they had died. It was when the students reported that a marked wasp from a different nest had arrived and, seemingly, integrated without much trouble into her new nest that I became really interested. I had only just begun to work seriously on bumblebees at the time and had not studied other social insects in any great detail, but I had never heard of social insects moving between nests. As an undergraduate I had been taught how ant and bee colonies consisted of a queen and her daughters, and how the close relatedness within the nest made this social system possible. I knew that ant colonies would often fight ferociously, and that honeybees would try to steal honey from each other’s nests, and would post guards on the entrance to the hive to keep out intruders. It didn’t seem to make any sense for wasps to move around like this, or for them to be welcomed into their new homes.
I became very excited, and pushed the students to mark huge numbers of wasps on every nest they could find. They got rather prickled by the pears, but stuck at it. They found that movement between nests was quite common. Some individuals seemed to move back and forth, switching their allegiance from day to day. To me this seemed most peculiar, and I excitedly planned writing up this discovery for Nature, a top-notch journal.
When I returned to Southampton I was in for a big disappointment. I dug out the literature on paper wasps and soon found that their movement between nests had already been described. Nonetheless, it was fascinating to read about them, as their biology was so similar to in some ways, but markedly different in others, to that of bumblebees. The social structure of bumblebees is seemingly simple. Each nest has a single queen and many daughter workers. Many ants and social wasps are much the same. Paper wasps, on the other hand, are decidedly flexible in their nesting arrangements. Nest-founding begins in spring when the females emerge from hibernation. Some females try to found a nest of their own, as does a bumblebee queen. Other females do so working as a small group – an uneasy alliance – although usually there is a hierarchy, with one female being clearly dominant. These groups often, but not always, consist of sisters, thought to recognise one another by smell and perhaps also by facial recognition: paper wasps tend to have highly variable face patterns. The nest produces female workers, most of them the daughters of the dominant foundress, and grows steadily through the spring and summer, producing new foundresses and males in late summer, much as a typical bumblebee nest does. However, unlike bumblebees, the workers are capable of mating, and sometimes do so. If the foundress dies and there is no subordinate foundress, then a worker will mate and take over her role. Both subordinate foundresses and workers sometimes switch allegiance from one nest to another, perhaps tending to move to nests containing related individuals. If a nest is destroyed, as often happens due to
attacks from predatory birds or mammals, then the foundresses and workers that survive will usually join another nest, or sometimes try to kill the foundress on another nest and take it over. If they succeed in the latter, they kill and eat the young brood in the nest so that they can replace it with their own, but they allow the older grubs and pupae to develop, presumably to increase their workforce. This makes single-handedly founding a nest a high-risk strategy for a female paper wasp, for her nest is easily commandeered by others. In all of this each wasp is presumably trying to maximise her reproductive success, either by helping relatives to reproduce or by producing her own offspring, wherever possible.
Paper-wasp societies seem to consist of a network of shifting, fickle alliances, rather than the more rigidly organised nests of bumblebees. Or so it seemed to me in 1995, but this turned out to be incorrect. Since then we have been slowly discovering that bumblebee nests are not quite what they seem. This has only become possible through advances in genetic ‘fingerprinting’ techniques, which enable us to identify who is related to whom. Of course these techniques are not only useful for bees; they have also been used in studies of many other animals, including humans, and the results are often surprising. For example, swallows were long considered to be monogamous. These charming, elegant birds form into pairs, which work together to build a nest and rear a clutch of young. I regularly have two or three pairs nesting in the rafters of my old barns at Chez Nauche, their cheerful and excited twittering as they gather mud for their nest from the edge of rain puddles in the yard a sure sign that spring is well under way. It was only when the DNA of the offspring and parents was compared that it became apparent that pairs of swallows were not quite as devoted to one another as they appeared. Many nests contained chicks that were the offspring of the mother, but were unrelated to their apparent father. The females clearly sneak off to engage in illicit copulations, so their cuckolded partners may spend much of their time rearing someone else’s offspring, while also presumably trying to obtain a few extra mating opportunities themselves.
This relates not just to swallows; chronic, serial infidelity seems to be the norm in most birds. Great reed warbler females routinely sneak off to mate with males other than their partner, preferring trysts with males that have an impressive song repertoire. And some birds take infidelity to extremes. Males of the superb fairy wrens – beautiful little Australian birds with turquoise-and-black markings – spend much of the breeding season sneaking off to court females in nearby nests, even resorting to picking flowers to present to them in the hope of being rewarded with a swift sexual encounter in the bushes. Of course it is not just birds that are unfaithful. Genetic studies of various human populations have revealed that anywhere between 2 and 30 per cent of children are the result of what biologists term ‘extra-pair copulations’.
In birds, such studies sometimes also reveal that offspring are unrelated to either parent. This seems to be particularly common in many species of duck, which routinely try to lay their eggs in the nests of others if they get the chance, hoping that their offspring will be looked after by somebody else. This most frequently happens in birds that have large clutches of eggs, perhaps because an extra egg or two in a nest that already contains a dozen eggs is not very obvious to the resident female when she returns. Of course cuckoos take this strategy to its logical conclusion, entirely abandoning building their own nests in favour of laying their eggs in the nests of other species.
It turns out that bumblebees are rather like ducks, at least in this respect. Worker bees are physiologically incapable of mating, but they can lay unfertilised eggs that develop as males. In 2004 bumblebee researcher Carlos Lopez-Vaamonde at London Zoo discovered that their experimental buff-tailed bumblebee nests were being infiltrated by unrelated workers that snuck in to lay eggs, essentially parasitising the nests of others. Some of these bees originated from other experimental colonies, but others were coming from wild buff-tailed nests in Regent’s Park. If they succeed, these workers get to produce sons that they will not have to look after at all, thereby passing on some extra genes to the next generation and so improving their fitness in evolutionary terms.
This all seemed pretty fascinating, and I discussed it with Steph O’Connor, who was working with me at the time as the handler of Toby, our bumblebee sniffer dog.1 Interesting though the work from the zoo was, it seemed a bit unnatural. The nests being infiltrated were reared in captivity and were contained in artificial boxes connected by tubes to the outside world. It seemed to us that natural, wild nests might be harder to find and invade. Steph’s project involved finding bumblebee nests with Toby, and then following how well they fared and what predators and parasites attacked them. She had found quite a few wild buff-tailed bumblebee nests in and around the university campus, and was planning to dig them up towards the end of the season when they had produced whatever new queens and males they were going to, in order to reveal what parasites were inside. It seemed like a great chance also to find out how many of the male bees produced by wild nests were the offspring of sneaky unrelated workers.
Steph duly dug up as many of the nests as she could. It was a horrendously difficult job, for some of the nests were at the end of tunnels three metres long, often down old rabbit burrows. The tunnels would frequently go under the roots of trees and deep underground, so that some nests were impossible to reach. The remaining bees weren’t too impressed, either. Buff-tails can be understandably aggressive when their nest is threatened and, even though the nests were old and declining, some of the workers would fly out and attack. Steph would catch them, one by one, and place them in pots. She persevered and eventually excavated fourteen nests in their entirety: worker bees, queen, pupae, grubs and eggs. She then genotyped them all, which was a hefty job, since there were well over a thousand individual bees at one stage or another. After several months in the lab she was finally able to piece together who was related to whom. The results contained some surprises.
Most of the males in the nests were sons of the queen, so long as the queen was still alive. Some (usually less than 1 per cent) were sons of the nest’s workers, and grandsons of the queen. This wasn’t particularly surprising, since we had known for many years that workers try to lay their own male eggs, preferring to rear sons rather than brothers, if they can get away with it (although if their mother, the queen, catches them, she roughs them up and gobbles up the eggs that would have become her grandsons). In total four males were entirely unrelated to the rest of the occupants – proof that workers really do sneak into the nests of others to lay eggs under natural conditions. Six of the worker bees in the nests were not daughters of the queen – presumably these were sneaky bees from nearby nests that we had caught in the act; they might just have been nipping in to lay their eggs when Steph came along, or they might have permanently moved into a new nest, perhaps because their own nest was destroyed by badgers or disease.
All of this was as we might have guessed. The surprise was that some nests also contained groups of females, including both adult workers and eggs, that were sisters to one another, but entirely unrelated to the rest of the nest. A group of adult sister bees could all be sneaky workers coming from a nearby nest, but clearly eggs do not move from nest to nest on their own, and it seems highly unlikely that adult bees would carry them. These bees had to be the result of a second queen, who had somehow snuck in and laid a batch of eggs.
In bumblebees ‘usurping’, whereby a queen invades a nest and attempts to kill the resident queen, has long been known and seems quite common. However, this was always thought to happen early in the spring when nests are small. Queens emerging late from hibernation might struggle to find a vacant nest site, but might instead find a young nest and opt to try to take it over.2 Steph’s nests were dug up in August and September, right at the end of the season. The nests had not been usurped; the resident queen was still in occupation in most of them. It appears that, just as workers opportunistically sneak into nests to lay e
ggs, so do queens. This seems rather odd, for it begs the question where these queens have come from. Perhaps they are old queens whose own nest has been destroyed somehow, and who are therefore forced to dash into the nests of others to lay batches of eggs in a desperate, last-ditch strategy to leave behind a few offspring. Or they might conceivably be new queens, just emerged from another nest and newly mated, but this seems unlikely, as the conventional wisdom is that queens do not mature their ovaries until after hibernation. A queen who poured energy into developing her ovaries in late summer would use up her fat stores and would probably be unlikely to survive the winter, so such a strategy would make little sense.
One of Steph’s nests did contain a second queen, unrelated to the rest of the occupants. She had not laid any eggs, or if she had they had been eaten by the nest’s residents. It is possible that she had attempted to usurp the nest earlier in the year, but had failed and then stayed on in the nest as a subordinate queen – rather as several mated females live together among paper wasps. Alternatively she may have arrived recently and been biding her time, in the hope of getting the chance to lay some eggs, or perhaps even attack and kill the resident queen, at some point in the future. Whatever the truth, studies such as Steph’s are revealing that the lives of bumblebees are neither as simple nor as regimented as was once supposed. Nests do not just contain a queen and her offspring, but may be a mix of multiple queens, workers from a range of nests, sons and grandsons of the queen and adoptee sons foisted on the nest by sneaky workers.
Social insects have sometimes been held up as examples of ideal, altruistic societies, where all struggle selflessly for the common good. Luminaries as diverse as Aristotle, Virgil and Shakespeare extolled their virtues; Socrates even went so far as to suggest that the most virtuous humans might hope to be reincarnated as ants or bees. In reality, bee, ant and wasp societies are far more interesting than the utopian ideals for which they were mistaken. Ruthless power struggles that would put the Borgias to shame are commonplace, with murder and even cannibalism being frequent. There is little here that we might wish to emulate, yet there is still a huge amount that we might learn from studying these wonderful, fascinating creatures.