by Dave Goulson
24 May 2009. Run: 38 mins 20 secs. People: one ancient man tending his splendid allotment, weeding his long rows of carrots and beans. Dogs: 6. Butterfly species: 13. A horseshoe bat flew in an open window last night, but then couldn’t find the way out, so it spent half the night circling above my bed, wafting me with its wings before I was forced to get up and catch it with my butterfly net and release it outside – hence I’m feeling a bit groggy this morning. On the last leg of my run I spied a ruderal bumblebee queen nectaring on the yellow rattle in the meadow – a wonderful, huge beast, a zeppelin of the insect world, with chocolate and velvet-black stripes. I also saw my first meadow brown butterfly of the year, a male, no doubt the first of very many more to come.
One of the most common butterflies to be found in my meadow at Chez Nauche is the meadow brown, properly known as Maniola jurtina. If you get down on your haunches on a sunny day in July and scan across the waist-deep vegetation of the meadow, you will see hundreds of them, flitting about from flower to flower and occasionally indulging in aerial dogfights. Indeed, meadow browns are amongst the most common butterflies to be found in more or less any meadow in Europe south of the Arctic Circle. They fly for ten weeks or so, from early June through July and much of August, but spend most of the year as green, hairless caterpillars quietly munching away on grass. They are decidedly drab, with a milk-chocolate upperside to their wings, and a camouflaged underside marked with wavy fawn and greyish bands. They generally sit with their wings closed, so that only the undersides are visible, and when they do so they are very hard to see amongst the yellowing, sun-bleached grasses of a summer meadow. If you look very closely you may see between one and five very tiny black spots along the margins of the hindwing, sometimes with a faint white halo surrounding them. These spots don’t look like much, but I spent two and a half years of my life counting them, and trying to make sense of the numbers I obtained.
To explain why, I need to take you back to Oxford in the 1940s, and to the eccentric career of Edmund Brisco ‘Henry’ Ford. The 1940s was an odd but exciting time for biology. Darwin’s concept of evolution by natural selection had revolutionised biological thinking, but the modern science of genetics did not yet exist. It was entirely unclear how evolution worked at a mechanistic level. Gregor Mendel, an Augustinian friar working in Austria in the 1860s, became posthumously famous for his experiments with peas, which demonstrated that characters were inherited in discrete units of some unknown material, which were passed from parent to offspring. We now use the word ‘gene’ to describe these units, and we know that they are made of DNA (deoxyribonucleic acid), but Mendel had no way of knowing this. He worked tirelessly for many years, rearing more than 29,000 individual pea plants from crosses that he had made by hand. One single experiment took him ten years. Sadly, the significance of his work was unrecognised at the time; if only his contemporary, Charles Darwin, had come across it, he would surely have realised that here was the very mechanism that underpinned inheritance, and hence his theory of evolution. Mendel’s work was rediscovered twenty years after his death in the early 1900s, but the heritable material was not identified as DNA until the 1940s, and even then no one knew how it carried information. It was not until James Watson, Francis Crick and Rosalind Franklin elucidated the structure of DNA in 1953 that genetics could really take off as a discipline, and it is staggering to think of the progress that has been made in the sixty years since then, with entire genomes now being sequenced.
To return to Ford, he was born in 1901 and spent his whole career based at Oxford. By the 1940s he was a lecturer in the Zoology Department. He more or less single-handedly founded a discipline that became known as ‘ecological genetics’ – the study of genetic change in natural populations – at a time when genetic change was impossible to measure directly, since no one knew what genes were made of. These days, modern genetic tools allow us to sequence genes and compare sequences between individuals and populations, but none of this was available to the early eco-logical geneticists. Instead Ford and his colleagues were forced to use visible differences between individuals, and between species, that might (or might not) serve as a proxy for genetic differences. Butterflies and moths had long been known to show variation in wing patterns between individuals; indeed, a popular and (with hindsight) rather eccentric hobby in the early twentieth century was to collect unusual variants of particular butterfly species and pin rows and rows of them in cabinets. Ford had collected butterflies as a youth and so he was aware of this variation.
Ford was convinced that natural selection was all-important in nature. At around the same time other geneticists, most notably the American Sewall Wright based at the University of Chicago, were developing theories which suggested that chance events alone could also lead to genetic change in populations. With a simple pen-and-paper argument, Wright showed beyond reasonable doubt that gene frequencies could change rapidly in small populations, due to a process that eventually became known as ‘genetic drift’. Wright’s work has long since been accepted, and indeed it forms the basis of our understanding of inbreeding in rare animals, which can and do rapidly lose genetic diversity through drift. Nonetheless, Ford seems to have taken offence at this notion, and spent much of his career trying to prove that Wright was wrong.
Ford looked for evidence for natural selection in the changing frequencies of different colour morphs of moths and butterflies. He settled on a trio of study species: the peppered moth, the scarlet tiger moth and, of course, the meadow brown. Peppered moths, the best known of the three species, exist as either a very pretty pale form, which has white wings decorated with an intricate pattern of black-and-grey spots, or as an entirely black form. The pale form is beautifully camouflaged when sitting on the lichen-crusted trunk of a tree. Naturalists had previously noted some remarkable changes in the relative abundance of the pale and black forms. In 1811 the black form was rare, but by the 1860s it was more common than the pale form in urban areas, and by the 1890s almost all peppered moths in cities were black. In the middle of the twentieth century the change began to go into reverse, with the black form becoming less common, and now it is quite scarce once again. Ford had a PhD student, Bernard Kettlewell, who studied this phenomenon and provided the experimental evidence to explain what was happening. In fact it was all fairly simple, and to this day provides one of the neatest textbook examples of natural selection in action. The genetic basis of the colour difference was easily established by lab crosses – the wing colour is controlled by a single gene, which gives the moths either the pale or black form. So the frequencies of the different forms of the gene had swung markedly over 100 or so years, but why? It turns out that it was all to do with pollution. Lichens are very susceptible to pollution, and during the Industrial Revolution they largely died off in cities. Indeed, the soot produced by early industry caked the trunks of trees so that they were more or less entirely black. Kettlewell used what are known as ‘mark-release-recapture experiments’, whereby moths are caught, marked with a dot of ink, released and then as many as possible are recaptured a few days later. In the blackened woodlands of industrial Birmingham, he found that the pale moths were much less likely to survive to be recaptured than the dark ones, but when he repeated this experiment in an unpolluted, lichen-rich woodland in Dorset the reverse occurred. He released both moths and great tits into large aviaries and found that, depending on the backgrounds available for the moths to perch upon, the birds tended to find and eat whichever colour morph most poorly matched the background. Pale moths stick out like a sore thumb to birds and humans alike, when resting on a soot-blackened tree, and so during the Industrial Revolution the dark moths had a huge advantage and more or less replaced the pale ones. When cities were cleaned up in the early twentieth century, the pale form started to creep back.
It is perhaps a shame that Ford didn’t stick to studying peppered moths. The two other species that he chose to study produced much more equivocal results. The scarlet tiger moth is a v
ery pretty red-and-black moth with cream-and-orange spots. It exists in three different forms, the most common of which has many spots, plus a rarer form with some spots missing, and a very rare form that is largely black. The moth itself is rather rare, being found near Oxford in only a handful of small sites. Ford studied one site in particular, Cothill, an odd little patch of fenland of just a couple of hectares, surrounded by woodland. This little patch of soggy ground seems to suit the moth, perhaps simply because there is plenty of its favourite food plant, comfrey, and so tiger moths are plentiful in most years. The adults are rather sedentary, and in the daytime in June and July they are easily spotted, sitting around on the vegetation. Ford counted the numbers of the three morphs each year from 1939 more or less until his death in 1988. He found that the frequency changed rapidly from year to year – so rapidly that it could surely only be explained by natural selection of some sort. Drift can’t result in rapid genetic change in large populations over one or two generations, as appeared to be the case here. Unfortunately it was never clear what the selection was – scarlet tiger moths are brightly coloured to advertise the fact that they are poisonous, so it was unlikely to be anything to do with predation. Nonetheless, Ford used his data from Cothill to castigate Sewall Wright in a series of articles from the late 1940s to the 1970s. With hindsight it all seems rather odd, for Wright never tried to claim that natural selection didn’t occur – he simply argued that chance events could also be important. Hence, even if Ford’s data had been watertight, it couldn’t possibly have proved Wright wrong.
And so we return to Ford’s third species, the meadow brown. But before we do so, let me explain how I became interested in it. In 1987 I graduated from Oxford with a degree in biology and the notion that I was going to become a conservationist and save the world. But first I decided to cycle across the Sahara with an old school chum (another Dave). We duly did so, more or less, ending up somewhere near the border between Algeria and Niger before flying home just before Christmas – more tanned, a little thinner and a lot poorer than we had left. We both signed on the dole, and joined the local Shropshire Conservation Volunteers to keep ourselves busy. A couple of months later I spotted an advert for a PhD on the ecology of butterflies in Bernwood Forest, based at Oxford Brookes University. I had pretty much ruled out doing a PhD, because I didn’t think I was cut out for academia. I also didn’t much fancy another three years of scrimping and saving on a student stipend (these days PhD stipends are more generous). But this PhD offered what seemed at the time like a reasonable salary in exchange for some basic teaching duties. What was more, I had always loved butterflies, and by bizarre coincidence I had done my undergraduate final-year project on the ecology of butterflies in this very same forest, which lies about eleven kilometres east of Oxford. It seemed like fate, so I applied and, sure enough, I got the post.
I started my PhD in April 1988. My PhD supervisor, Denis Owen, was an odd character. He had spent many years working out in Africa, and would often come to work in colourful East African gowns. He smoked like a chimney in his office, so much so that the room filled with smoke and he became a blurred, dimly visible silhouette when viewed through the glass window of his office door. He would spend his time in there hammering away on an old-fashioned manual typewriter so loudly that the thin office walls would gently shake. Denis barely spoke to me when I started, merely telling me to go and spend a lot of time in the field, looking at butterflies. I was rather intimidated and so didn’t push him for any more pointers, although I was in desperate need of them. I hadn’t really got a clue what to do. A PhD requires an idea, a hypothesis, an interesting question to pursue. I had none of these, so I went every day to Bernwood and wandered about looking for butterflies.
Bernwood has an interesting history. One thousand years ago it was a vast royal hunting forest, covering many hundreds of square kilometres, and it is said to have been a favourite hunting ground of Edward the Confessor. Over time it was gradually cleared and converted to arable land and pasture, as successive monarchs sold off chunks of the forest to raise cash. By the early twentieth century Bernwood had shrunk to occupy just 300 hectares, but despite its diminished size it had become well known as a hunting ground for butterfly-collectors. It supported many rare woodland species, including the spectacular purple emperor and the black hairstreak. Sadly, it was purchased by the Forestry Commission in the 1950s, and at the time this organisation had little interest in butterflies or in conservation. Virtually the entire wood was clear-felled and sprayed with herbicides from the air to kill off any regeneration. Dense stands of conifers were planted, and then sprayed with DDT to kill beetle pests that attacked the conifers. Remarkably, the forest remained a hotspot for rare butterflies through the 1960s and 1970s. Despite the herbicide sprays, woodland flowers and shrubs somehow survived, and so did most of the butterflies. When I first visited Bernwood in the mid-1980s, it still had many rare butterflies; it remains the only place in the UK where I have seen wood whites, brown hairstreaks and purple emperors. It was thought to have more breeding butterfly species than any other site in Britain. Sadly, though, most were in decline. The conifers were growing larger and larger, casting a dense shadow and thus shading out all of the native flora that provide butterflies with nectar and food plants for their caterpillars. My undergraduate project was on the effects of increasing shade on woodland butterflies, and its conclusion was that all but the most shade-tolerant butterflies, such as the speckled wood butterfly, would soon disappear.
Luckily, the Forestry Commission has evolved over time. Where once it was concerned solely with efficient timber production and with generating maximum profit, now it is far more interested in conserving biodiversity and managing forests in a way that balances commercial needs with those of wildlife. Changes were evident in the late 1980s at Bernwood, where the Forestry Commission began widening rides and cutting small clearings to combat the gloom cast by the towering spruce-tree plantations. It was pretty small-scale stuff, but it was a start.
I spent the spring and summer of 1988 walking these rides, looking for butterflies, and trying to come up with an idea as to what I should study for my PhD. Having a strong interest in conservation, I decided to study the ecology of a rare species, the Duke of Burgundy fritillary. It isn’t actually a fritillary, and it has no known connection to the Duke of Burgundy, so its name is hard to fathom, but it is a lovely little creature with a chequered orange-and-brown upperside and silver spots on the underside of its wings. The butterfly is on the wing in May, while for much of the rest of the year the caterpillars can be found on the leaves of their food plants, cowslips and primroses. At least in theory they can. In practice I walked through Bernwood every day in May when it wasn’t raining and saw one Duke of Burgundy, a female that promptly flew away. I searched diligently for eggs and caterpillars over the following months, but found none, although I did map out the locations of every primrose in Bernwood. By September I had exactly one data point, and there really wasn’t a great deal I could say based on that.
I spent the autumn and winter reading everything I could on butterflies, in search of inspiration. It felt as if time was slipping away. My PhD funding was for three years and there are, self-evidently, just three field seasons in three years; I had squandered one already. If my second field season was similarly unsuccessful I would be doomed to fail my PhD. It dawned on me, not before time, that studying rare creatures is rather difficult. For safety, I decided instead to study something very common, something that I could not fail to find by the thousand. And this is where we return to the meadow brown. It isn’t a woodland butterfly, but there were quite a few in the woodland rides and I had seen countless numbers of them in an adjacent meadow, known appropriately enough as Bernwood Meadows. But what exactly should I study? I came across Ford’s work on meadow browns and became intrigued. I knew of Ford, for he was author of the New Naturalist book Butterflies, which I had been given as a child. I’d also met him briefly when I was an u
ndergraduate student at Oxford, at which time he had been a very old but nonetheless rather intimidating figure.
Ford worked closely with Wilfrid Hogarth ‘Bunny’ Dowdeswell, a former Oxford undergraduate who became an academic at Winchester College, and together they counted the spots on the hindwings of meadow brown butterflies for twenty-five years, from the late 1940s to the 1970s. They obtained samples from all over Europe, and particularly from the Scilly Isles, which they visited repeatedly over many summers, camping together on the uninhabited islands.1 In most populations in Britain and Europe, the majority of male meadow browns have two spots, while most females have none. In some peripheral populations, such as some of the Isles of Scilly, females with one or two spots were very common. On some of the smaller of these islands the frequency of spotted and unspotted butterflies varied sharply from year to year, far more than could be explained by chance (or genetic drift, as Wright termed it). This, Ford declared once again, was clear evidence for natural selection, and proof that drift was inconsequential. What is more, Ford described a mysterious boundary phenomenon along a line roughly following the border between Devon and Cornwall, where the frequency of spotted and unspotted butterflies changed markedly from one side of a hedge to the other. Given that meadow brown butterflies can readily fly over hedges, this seemed odd, but was again attributed to some powerful selective force at play.
What interested me was whether these spots actually served any function that could explain the selective forces that seemed to change the frequency of more or less spotty individuals from place to place and year to year. Some butterflies, such as the peacock, have very prominent eye-spots near the tips of their forewings, which are thought to scare away potential predators by mimicking the eyes of some much larger beast. The eye-spots of a peacock are hidden when it sits with its wings closed, but if it is disturbed, it has only to open its wings to reveal huge eyes comprising concentric circles of blue, red and yellow. Owl butterflies – enormous creatures that live in the rainforests of South America – have eye-spots and associated wing patterns that convincingly resemble the face of an owl. Meadow browns also have far less impressive eye-spots near the tips of the forewing, on both the upper and lower sides, formed from a large black spot with a small white spot in the centre, resembling the glint of light reflected from the black pupil of an eye. These spots might serve to frighten predators, but this wasn’t especially interesting to either Ford or me, as all meadow browns were the same in this respect.
