A Buzz in the Meadow

by Dave Goulson

  Half an hour later another car came along the track; it doesn’t go anywhere, petering out just a kilometre beyond the meadow, so they were unlikely to be random passers-by. They too stopped and watched for a while, and then reversed away. Over the next few days perhaps a dozen different cars came by, roughly a dozen more than would normally pass the meadow. Clearly word had got out that the Englishman was up to something strange. I think I recognised the sturdy lady who had nearly shot me seven years earlier. Monsieur Fontaneau came back with his thin son. They all stopped and watched for a while, though none ever came over to ask what we were doing, and I didn’t attempt to approach them with an explanation, which I felt sure I would be unable to provide in my hopeless French. To this day I wonder what they thought we were doing, mowing endless neat squares in a vast field, then performing strange, ritual dances in them.

  I’ve been back to Chez Nauche every spring since to survey the plots, counting and identifying every plant species present. It takes several days, and is repetitive but rewarding work. Identifying some of the grasses is a particular headache, but I enjoy the challenge. The character of the meadow changes from year to year, depending on spring rainfall and temperature. Sometimes it is like a jungle, with the taller plants reaching head-height, while in drier years it is much sparser with patches of bare soil. Every year we find new plant species that I have not seen before. The yellow rattle has certainly established itself, though it is very patchy, and there is also some greater yellow rattle and small scatterings of the other species. Clovers seem to be spreading rapidly in many of the plots, so that they are thick with bees. Shrill carder queens, which love red clover, have become common in late May.

  It is too early to say yet whether the different hemiparasites are having any effect. I have long since forgotten which plot is which (although of course I have this written down and filed away) – a good thing because otherwise I might subconsciously bias the results. In a year or two I will analyse them and see what it shows. Whether the experiment produces positive results or not, it is clear that the meadow as a whole is slowly improving, with a few more flowers every year. I do not know whether it will ever reach the dizzy heights of floristic diversity found in an ancient hay meadow, but it seems to be turning into a fair facsimile.

  One of the few places in western Europe where there are still quite a few pristine flower-rich meadows is in the Alps. The sheer inaccessibility of many of the higher pastures has protected them to some extent from the ravages of modern agriculture, and the Alps remain the largest biodiversity ‘hotspot’ in Europe. A visit to these high meadows in late spring or summer is a must for any nature-lover. The weather is hugely unpredictable, but if you are lucky and catch the Alps on a sunny day they are breathtaking. Lush carpets of flowers tumble over the rocky slopes, buzzing with insect life making the most of the short summer. Of course the backdrop of dizzying snow-capped peaks and deep valleys with glimpses of distant lakes sets everything off nicely, too. Because of this extraordinary beauty and diversity, the staff at the University of Stirling decided that Switzerland would be an ideal place for a summer field course for our biology students. Despite the high cost of living in Switzerland, it was surprisingly cheap to rent a huge chalet high in the mountains, presumably because many of these buildings lie empty through the summer, the bigger influx of tourists coming during the winter to ski. To my delight, when we arrived at the chalet for the first time in June 2009, the first plant I noticed was yellow rattle, growing around the edges of the rough lawn. It turned out to be common in the area, not so much in the very high meadows, which tend to be heavily grazed by cattle, but in the lower areas downhill from our chalet, where the fields are kept free of livestock in the summer to provide a hay crop.

  We set the students to work on a range of projects, one of which I supervised, on the diet of Swiss bumblebees (no muesli or chocolate for them). The Alps have all sorts of bumblebee species, including almost all the British species and a whole heap more besides, and identifying them was initially a challenge. I was particularly excited to see great yellow bumblebees, in Britain a rarity largely confined to coastal grasslands of the Hebridean islands and seldom found more than a few metres above sea level, but here happily living a kilometre or two higher amongst the mountain peaks. Despite the lack of bilberries there were plentiful bilberry bumblebees, among the most colourful species, with huge red bottoms and yellow stripes. On our first morning we recorded sixteen different species within a short walk of the chalet.

  Amongst these was a species I had seen only once before, in the mountains of southern Poland – a species with no English name, Bombus wurflenii. It is one of a very small number of bumblebee species that has become a specialist nectar-robber, a professional thief, which makes its living by cutting holes into the side or back of flowers and stealing their nectar. Because it does not enter flowers by the conventional route it does not contact the reproductive parts and so does not pick up or transfer pollen. If flowers could speak (or think), one might imagine them shouting, ‘Oi, stop! Thief!’ Britain has species such as the buff-tailed and white-tailed bumblebees, which sometimes stoop to robbery if they are hungry and encounter a flower that is too deep for their short tongues – they are opportunistic thieves. In contrast Bombus wurflenii are incorrigible larcenists. They are well equipped for their profession. The mandibles of most bumblebee species are approximately smooth and paddle-shaped, well adapted for moulding wax and feeding broods. Buff-tailed and white-tailed bumblebees have small teeth on the edges of their mandibles, which help them to bite through the back of flowers when the need arises, but it takes them a little while to do so. In contrast the mandibles of wurflenii are armed with a row of long, curved and sharply pointed teeth, which enable it to slice though the sepals of most flowers in moments.

  In the high Alps there are many deep, nectar-rich flowers, such as kidney vetch and monkshood, that aim to attract long-tongued bumblebees such as garden bumblebees and great yellows, and it is these that wurflenii targets. We also noticed that they were visiting, and robbing, yellow rattle. I’d never seen yellow rattle robbed before; the tough sepals are enough to deter amateur thieves such as buff-tails, so the rattle in my French meadow remains unburgled, but here in the Alps almost every flower had been robbed. Just as a house break-in is given away by a shattered window pane or a splintered door, so nectar robbery leaves behind obvious marks; wurflenii create crescent-moon-shaped holes in the sides of the sepals. The holes stain brown around the edges, and so contrast with the fresh green of the undamaged sepals. There is a certain irony that rattle, itself a parasite of grasses, is in turn parasitised by bees (which are parasitised by other bees, which are parasitised by mites, and protozoans, and so on and so on).

  In the second week of our stay the students were assigned different projects, working in smaller groups, and one of the projects that we devised was to look at whether the robbing of rattle had a detrimental effect on seed set. The robbing holes remain visible long after the petals have wilted and the flower has set seed, and so for the older flowers on the plant – those low down on the stems – it was possible to count the seeds of both robbed and unrobbed flowers and compare them. If, by stealing nectar, robbing made the flowers less attractive to long-tongued, pollinating bumblebees, then we would predict fewer seeds in the robbed flowers. The students set to work, carefully pulling apart hundreds of old flowers and counting the flat green seeds within.

  After a while of this tedious work, one of them, a bearded, ginger-haired Scot named James Morrison, noticed something odd. Within the patch of rattle in which they were sitting, almost every flower had been robbed on the same side, the left. When he counted them up, 98 per cent of the holes were on the left-hand side, with just a very few on the right. He mentioned this to us and, once it was pointed out, the pattern became obvious. What is more, when we looked at other patches of rattle in different meadows nearby, almost all showed a strong pattern, but in some meadows all the flowers
were robbed on the right, while in others they were robbed on the left. Meadows just a few hundred metres apart showed opposing patterns.

  Many years earlier I had carried out a brief study of ‘handedness’ in bumblebees. Some flowers have lots of florets arranged in rings around a central stem – clovers, for example – and I’d noticed that some bees always seemed to go clockwise around each flower, while others went anticlockwise. I persuaded one of my PhD students, Andrea Kells, to spend a week following as many bees as she could and recording which way around flowers they went. She found that every bee seemed to have a preferred direction of rotation, although they did occasionally switch, but that there was no overall tendency within any particular bumblebee species to be either clockwise or anticlockwise bees. When I did a little digging in the literature I found all sorts of strange examples of similar behaviour, often called ‘handedness’ despite the creatures in question having a distinct lack of hands. Some of the more peculiar studies I unearthed involved creeping up behind animals and surprising them. When startled by something approaching them from the rear, apparently both goats and snakes tend to turn round quickly, with each individual always tending to turn the same way – either left or right. We published our work in a fairly obscure journal and it sank without trace, attracting no interest or attention whatsoever from other scientists.

  The ‘sidedness’ of robbing in rattle reminded me of this long-forgotten work. It was easy to imagine that wurflenii might have individual bias or handedness, but it was hard to see how that would result in every flower in a patch being robbed on the same side, unless a single bee had robbed all of them. Some of the patches were huge, with many thousands of flowers, so this just wasn’t possible. We were intrigued, and so for the next three summers, whenever we had a spare moment from teaching the students, one or other of the staff would sneak off to find patches of rattle and score the number of robbing holes on the left and the right. We also watched the bees, recording whether wurflenii tended to land on the right or left of a flower. We noticed white-tailed bumblebees acting as secondary robbers, using the holes sliced open by wurflenii, so we followed them too, recording the behaviour of each bee as it visited successive flowers.

  Year after year we found a strong bias in every patch, but no geographic pattern and no consistency across the years. A rattle patch might be robbed almost entirely on the left side one year, and on the right the next year. We found that pretty much every bee in a patch, both those robbing wurflenii and the secondary robbing white-tails, tended to approach flowers on the same side, be it left or right, and that this matched the location of the holes. So far as we could discern there was only one plausible explanation: the bees within each patch were copying each other. This might sound a little far-fetched, but actually it has been suspected for a very long time that bees might observe and learn from each other’s behaviour. In a letter to the Gardeners’ Chronicle written in 1857, Charles Darwin observed:

  One day I saw for the first time several large humble-bees visiting my rows of the tall scarlet Kidney Bean; they were not sucking at the mouth of the flower, but cutting holes through the calyx, and thus extracting the nectar … The very next day after the humble-bees had cut the holes, every single hive bee, without exception, instead of alighting on the left wing-petal, flew straight to the calyx and sucked through the cut hole … I am strongly inclined to believe that the hive-bees saw the humble-bees at work, and well understanding what they were at, rationally took immediate advantage of the shorter path thus made to the nectar.

  More than 150 years later Ellouise Leadbeater at Queen Mary, University of London, showed that buff-tailed bumblebee workers that encounter robbed flowers were more likely to become robbers themselves, so that the behaviour spread rapidly from one individual to many. What we seemed to have discovered was that bees could not only learn from others to rob flowers, but that they copied the particular technique – robbing on the left or the right.

  Our interpretation of the patterns of robbing found in our rattle patches in the Alps is as follows. In late May the first few flowers come into bloom. It probably takes a day or two before any bees discover them, for of course each year the worker bees have never seen rattle before, as none of them live for more than a few weeks. This is true of any flower – when it comes into bloom it takes a little while before any bees realise that it is worth visiting. Once one bee discovers it, others copy. The first wurflenii to discover rattle in a particular patch presumably has its own inherent bias, tending to land and rob on the left or the right, and if other bees in a patch then copy her behaviour, they will all end up being either left-handed or right-handed. We never had the opportunity to visit Switzerland earlier, in this formative stage of the process, because we were always occupied with end-of-semester exams at the time, but we were able to study it indirectly by examining the robbing patterns on flowers of different ages. The lowest flowers on a rattle stem open first, and the highest ones last, so that a single stem may be in flower for six weeks or more. Hence each stem carries a record as to what has been happening from when the very first flowers opened. We scored robbing of each flower from the lowest to the highest, and discovered that the patterns of robbing were less biased to one side or the other on the oldest (i.e. the first) flowers. One might imagine that sometimes more than one wurflenii might discover a patch at the same time, and if they have different strategies this would create a mix of holes on both left and right. This is not very efficient for the bees, for it is quicker to rob a flower using an existing hole than to cut a new one. Somehow over the next few days the bees seemed to settle on a common strategy, for flowers a little higher up the stem become uniformly robbed on one side or the other. Presumably newcomer bees benefit from adopting whatever is the most common strategy in the patch, which then makes the strategy even more common.

  This may all seem a little obscure – why does it matter where the robbing holes on rattle flowers are? It presumably makes no difference one way or the other to the plant, which has its nectar stolen either way. Of course in the grand scheme of things this probably doesn’t matter much, if at all, but it is a nice example of the ability of insects to adapt and learn from one another, and it is this ability that lies at the heart of the success of social insects.

  In fact, as far as the rattle is concerned, it seems not to matter that it is robbed at all – James and his fellow students could find no difference in the seed set of flowers that were robbed compared to those that were overlooked by the robbers. This seems counter-intuitive; after all, if they are having their nectar stolen, and the nectar is there to attract pollinators, surely this should reduce visits by the long-tongued bees – the legitimate pollinators – and thus reduce seed set? It turns out that it is not that simple. Many studies have been carried out on the impact of nectar robbery on a broad variety of flowers, and while some studies found that robbed flowers set fewer seeds, other studies did not, and a few even found that robbing increased seed set. The explanation is not clear. Sometimes nectar-robbers do touch the anthers and transport pollen, so although they are robbing they are also providing pollination by accident, as it were (of course almost all pollination is by accident, since few insects set out to pollinate flowers). It may also be that the low nectar levels that result from regular robbery make the long-tongued bees work harder to get enough food, forcing them to visit and pollinate more flowers. Of course if that were true, then flowers growing in areas without nectar-robbers would benefit from producing less nectar, both saving on nectar and getting better pollination.

  I am sure there is more to be discovered about rattle and its complex and unpredictable web of interactions with other plants and animals. James’s discovery of the sidedness of robbery in the Swiss mountains illustrates that almost anyone can discover something interesting and new, if they simply take the time to observe nature carefully. He needed no special equipment, just curiosity and a willingness to look and think. His observations may not have changed t
he world, but they did lead to some interesting research that has expanded our understanding of the natural world by a tiny increment, leaving us just a little wiser than we were before.

  CHAPTER TWELVE

  Smutty Campions

  1 September 2012. Run: 40 mins 40 secs. A lovely late-summer morning, with just a few puffs of white cloud in the sky. People: none. Dogs: 6, including that darned spaniel again, which managed to pull off my shoe in a surprise attack. Butterflies: 8 species, including lots of nymphalids – tortoiseshells, peacocks and red admirals – stocking up on buddleia nectar for the long winter ahead. There were also heaps of tired male bumblebees lolling around on the knapweed flowers, their fur bleached white by the sun – their days are numbered, their purpose done, for the new queens are by now all mated and safe in hibernation.

  Most people have never even considered the question ‘Why do males exist?’ We simply accept that there are two sexes, in roughly equal numbers, and that offspring are produced by sexual reproduction between a male and a female. Whilst most of us are content, perhaps even pleased, that this is the way things are, evolutionary biologists have been fiercely debating the explanation for the predominance of sexual reproduction in both animals and plants for fifty years or more. If females simply produced copies of themselves (reproduced asexually), life would be much simpler and there would be no need for males at all. There would be no need for all the angst and aggravation involved in finding and courting a mate; no males fighting over access to females; no sexually transmitted diseases; no jealousy, cuckoldry or unrequited love. A female who simply copied herself could quickly out-reproduce sexual competitors, for all of her offspring would be reproductive females, rather than half of them being males. Indeed, some animals and plants do use this strategy; they don’t bother with sex. Bdelloid rotifers (obscure microscopic animals found in ponds) eschew sex altogether, and seem to have survived perfectly well for many millions of years. Similarly some types of stick insect (including the Indian stick insects so often kept in schools), some nematode worms and even one or two species of lizard exist only as females. For most of the spring and summer, female aphids rapidly clone themselves so that one can become hundreds in a few weeks. So why is this not the norm?