A Buzz in the Meadow

by Dave Goulson

  Could the small spots on the underside of the hindwing have a similar purpose, relating to predation? Many hairstreak butterflies have an elaborate false eye near the edge of their hindwing, often with slender tails that resemble antennae, creating the impression that the back of the insect is in fact the front. To further enhance this impression, hairsteaks often perform a swift 180-degree turn as soon as they land on a perch or flower. The idea is that this may deflect the peck of a predatory bird from the real head of the insect to the margin of the wing, which readily snaps off, allowing the butterfly to escape. It is common to find butterflies with peck-marks nipped out of the edges of their wings.

  In the early 1980s Paul Brakefield, an English scientist based in Leiden, proposed an explanation for the variation in spot numbers in meadow browns and their relatives. He suggested that the spots did serve to deflect attacks, but that the trade-off was that they might make the butterfly more obvious to predators when sitting still. When flying about, visiting flowers and looking for mates, butterflies are very obvious to predators such as birds, so deflective spots might be helpful. In contrast, if the spots make them less well camouflaged when stationary, they would be best not to show them when sitting still. Female butterflies spend much more time sitting still than males, who fly around a lot, which might explain why females tended to have no spots whilst the majority of males had two. Brakefield went on to predict that in populations inhabiting cold, wet climates, where the butterflies spend a lot of time sitting around waiting for the sun to come out, spots ought to be a disadvantage and hence rare, whilst in sunnier places the spots ought to be more common. The latter certainly appears to be true in the large heath butterfly, a relative of the meadow brown in which spottiness decreases in populations that are further north or west or at higher altitudes.

  This theory was quite neat, but no one had ever shown that these spots actually did deflect the attacks of predators. I decided to try to find out. I also became interested in the genitalia of meadow browns. The genitalia of male butterflies consist of a pair of rather barbaric claspers, which lock on to the female during mating, and between which the tube-like phallus protrudes. Place your wrists together with the palms of your hands facing one another and you get a rough idea of the design of the claspers. They are hinged at the base, so that they can open out and then close on the female like grappling irons. In some butterflies the claspers are armed with sharp, incurved, talon-like hooks to help them grip. Pity the female speckled wood butterfly. In the meadow brown there are no sharp hooks, but there is a bristly ‘thumb’ protruding from their upper edge. The genitalia of male butterflies, and of male insects in general, tend to be very useful in identifying species that are otherwise similar. They usually differ in obvious ways between species, whilst being fairly uniform within species. One theory that had been put forward to explain this was that the male and female genitalia are like a key and lock; they only fit together if the male and female are of the same species, helping to prevent unfruitful mating between members of different species. The exception is the meadow brown, in which the male claspers are very variable. In some the ‘thumb’ is no more than a gentle bump, while in others it is very pronounced with a swollen end capped in bristles, resembling a tiny pollarded willow tree. So far as I could tell, no one had ever looked at the fit between female and male insect genitalia before, or explained why meadow browns have such variable genitalia, and this seemed worth exploring.

  Questioning the function of tiny spots on butterfly wings, or explaining why their genitalia come in various shapes and sizes, might seem fantastically obscure subjects to pursue. Answering these questions was never likely to change the world and, with the benefit of hindsight and experience, I can think of many more profound topics that I might have tackled, but in the spring of 1989 this was all I had.

  To get to grips with the function of wing-spots, I counted their number in meadow brown populations all over southern England. I had a lovely blue 650cc Suzuki motorbike on which I roared about the countryside, with a net, notebook and countless small cardboard pots in my rucksack. I wanted to test whether butterflies had fewer spots in cooler, shadier sites and more on sunny, south-facing sites, as Brakefield’s theory would predict, but disappointingly this didn’t seem to be true. I went down to Cornwall to look for Ford’s boundary, where the proportion of spotted butterflies was said to change suddenly, but it was no longer there, so far as I could tell. I didn’t seem to be getting very far, so I tried more experimental approaches.

  I killed a range of spotted and unspotted butterflies, dried them with their wings open or closed, and then tied them to grass seedheads in Bernwood Meadows and waited to see whether they were eaten by birds. Butterflies with their wings open were more likely to be scoffed, but whether or not they had spots on their hindwings appeared not to make the slightest difference.

  I tried a different tack. I caught 600 butterflies from Bernwood Meadows and changed their spots artificially. It is quite easy to remove these small spots by simply brushing away the dark wing scales with the tip of a damp paintbrush, and equally it is easy to add small black spots with a marker pen. So I randomly assigned individuals to either spotted or unspotted groups, made the necessary changes, gave them an additional discreet mark on the topside of their wings, so that I could subsequently identify them, and released them back where I had found them. Three days later I went back and hunted for my marked butterflies, to see which ones were still alive. In theory, if females spend most of their time sitting still, spots should make them more conspicuous and hence more likely to be eaten, while males that spend most of their time flying around should benefit from having spots to deflect attacks. So I predicted that females with added spots and males with spots removed should be predated more highly that unspotted females and spotty males. Of my 600 butterflies I managed to recover ninety-one – it was hard going because there are countless thousands of meadow browns in that meadow, so finding the ones I had marked was like looking for a needle in a haystack. To my slight surprise, the results followed the prediction. In particular, adding a spot to females did seem to make them more likely to be eaten.

  Studying the genitalia proved much harder. To measure them the poor butterfly has to be killed, partially dissolved in strong alkali, and then the genitalia pulled out and spread on a slide to look at them under a microscope. Studying them in action was still more challenging. There were umpteen published studies describing the genitalia of male insects of different species, but no one seemed to have looked to see what exactly they did when in contact with the female. Did they really form a key that perfectly matched the female lock? Finding mating butterflies in the field is fairly easy, particularly with common species such as the meadow brown. They can sometimes be seen flying around, the larger female carrying the male dangling behind her, but usually when mating they sit still on a stout grass stem. However, at the slightest disturbance they tend to separate. In any case it is impossible to see what is really going on with the naked eye, as the genitalia are too small. I needed somehow to persuade the mating couple to sit on the stage of a microscope, but that was hardly practical.

  After much thought I came up with a cunning plan. I filled a square polystyrene cool-box with liquid nitrogen, strapped it to the rear seat of my bike and rode out to Bernwood. Liquid nitrogen is very cool stuff, in both senses of the word. It boils at -196°C. It can render rubber or metal so cold that they become as fragile as glass – even the most expensive padlock will shatter like a cheap plastic toy if dipped in liquid nitrogen and then given a gentle tap with a hammer. When it is exposed it rapidly boils, releasing super-cool nitrogen gas, which freezes water vapour and carbon dioxide in the surrounding air.

  As I banked around the roundabout at the top of the Headington Road, some liquid nitrogen spilled, creating a brief cloud of white vapour behind me, which must have momentarily confused other motorists. But otherwise all went well. Once in the meadow I searched for mating butterflie
s, carrying the cool-box with me. Before long I spotted a pair, dangling from one of the seedheads of a tussock of cocksfoot grass. I took the lid off the cool-box, placed the container beneath them, then gave the seedhead a firm tap. As I had hoped, the pair tumbled down into the liquid nitrogen and were instantly frozen, still locked together in copulation. I left them there and collected a few more in the same fashion, before returning to the lab at Oxford Brookes.

  Back at the university I set up a microscope in one of the walk-in freezer rooms, and there I could examine my frozen couples at leisure. It became clear that only parts of the male valves were actually in contact with the female. To return to my analogy of paired hands, the main area that gripped the female was the lower edge – the little finger and side of the palm. The ‘thumb’ was nowhere near contacting the female, so presumably it didn’t matter what shape it was. This seemed to explain why this part of the valve was so variable: if it doesn’t really do anything, then natural selection would not act upon it, whereas those parts that grip the female would be under strong selective pressure to match precisely the female’s shape.

  I investigated all of this further with a second experiment in which I tried to measure the strength of the bond between male and female. I wondered if any attributes of the male genitalia – such as size or the shape of the ‘thumb’ – might affect the strength of the bond. If I was correct in thinking that the thumb wasn’t gripping the female, then there should be no relationship. I thawed out my couples, clipped the female to a stand and then attached successively heavier weights to the male, to see at what point the pair fell apart. Of course it might not have been hugely realistic, since the butterflies were dead and so presumably mating with less enthusiasm than usual, but it was the best I could come up with. It worked and, as predicted, the size or shape of the thumb did not seem to affect the strength of the bond. I never did explain why male meadow browns have more variable genitalia than other butterflies. It would have been good to study how the genitalia of lots of other species fit together when mating, but I didn’t have time.

  During my PhD I also studied whether spottier butterflies tended to fly more than unspotty butterflies – they did not. I looked to see if spottiness affected how often a butterfly mated, or whether it affected mate choices – it did not. I spent a long time grinding up butterflies and running their enzymes along electrophoretic gels in the lab, to get an indirect measure of how much meadow brown butterflies move about in the landscape. The answer was: quite a lot. I tested how long butterflies could sustain flight at different temperatures, and whether they differed in the lower temperature limit at which they could fly, but it didn’t reveal much of great interest – more- or less-spotty butterflies all performed much the same. I heated pupae gently from one side, and found that this produced adults with more and bigger spots on the warmer side. This rather undermined much of the work that I had done on spots, and Ford and Dowdeswell before me, for if they were influenced strongly by the environment, then differences in spottiness between populations could simply be due to microclimatic differences. The whole point of Ford’s work was to study genetic change, on the assumption that the visible differences in wing patterns of individual butterflies reflected genetic differences. If they simply reflected whether the caterpillar had happened to pupate in a slightly warmer or cooler spot, then the whole thing was a bit of a waste of time.

  I followed this up by doing a little work on whether temperature affected the wing patterns of scarlet tiger moths. Oddly, Ford never seems to have bred scarlet tigers himself, to prove beyond doubt that the different colour forms were genetically controlled, although they are quite easy to breed in captivity. I collected some moths from Cothill and did some simple rearing experiments at different temperatures. I found that storing pupae at slightly elevated temperatures resulted in adults that had lost some spots and resembled Ford’s intermediate colour morph. If switches between colour morphs could be brought about by changes in temperature, then all Ford was recording throughout those decades may simply have been evidence that the weather at Cothill varied from year to year. I suspect that Sewall Wright would smile, if he were still alive.

  Looking back, it is fair to say that my PhD was not a fabulous success, but fortunately I passed. My supervisor didn’t really speak to me at all until I was writing it up at the end of three years, and at the time I slightly resented that he gave me such scant advice, but with hindsight I perhaps learned more than I would otherwise have done by having to think for myself. Coming up with lots of duff ideas and trying them out was frustrating, but I guess it may have helped me work out what good ideas look like. That said, I do try to give my own PhD students rather more help than I received.

  When next time you are lucky enough to find yourself in a meadow in high summer, keep an eye out for the meadow brown. They are not glamorous as butterflies go, but they have an understated charm. The decades of intense scientific scrutiny are long forgotten, and they seem content to go quietly and unfussily about their unspectacular business, the tiny black dots on their wings mattering not one jot. It seems remarkable now that they could ever have been the subject of such intense and heated debate.

  Butterflies are one of the most beautiful of insect groups, for the wings of many types are stunningly colourful, or tastefully ornate, or subtly but intricately shaded, and all possess a symmetry that is lovely to behold. We know that some patterns seem to provide camouflage, that big spots might frighten predators and that bright colours might please a mate or warn a predator that the butterfly is poisonous, but beyond that we can hardly begin to guess what purposes their beauty serves – if, indeed, it serves any at all.

  CHAPTER SEVEN

  Paper Wasps and Drifting Bees

  5 July 2009. Run: 37 mins 27 secs. Personal best! I was perhaps helped by a vicious little black spaniel in the hamlet of L’ge Marenche, which chased me, nipping at my heels for 100 metres or more. People: none. Dogs: 7. Butterfly species: 18, including a fabulous Queen of Spain fritillary, with silver spots flashing on her underside as she flew. I also got a distant view of a pair of stone curlews in a fallow field to the north – peculiar boggle-eyed, long-legged birds that prefer running to flying. They are a great rarity, even here.

  Karl Marx was right, socialism works, it is just that he had the wrong species.

  E. O. Wilson

  Between the farmhouse at Chez Nauche and the northern boundary I have planted an apple orchard. I’m not really sure why, but I’ve always loved orchards. My grandparents on my mother’s side had a lovely orchard at the end of their large garden in Norfolk. My grandfather had planted the trees himself as a young man – not the short, stunted trees on dwarfing rootstocks that are always used these days (it makes the fruits easier to pick), but proper trees that had grown ten or more metres high. Picking the fruit was a hazardous business requiring long wooden ladders, and much of it fell to the floor, where it was fought over by my grandfather’s free-range chickens and swarms of wasps. It was a lovely place in late summer, alive with the buzz of insects. (Sadly, it is now a housing estate.) Old orchards with full-sized trees are rare these days, and are havens for insect and bird life, so I really wanted one in France, but there was a problem. I couldn’t find anyone who sold apple trees on rootstocks that would allow them to grow to full size. In any case I couldn’t really afford to buy enough of them for a proper orchard, so I decided to grow my own from pips. I deliberately bought a range of apple varieties and collected the pips from every one I ate. I sowed them in the greenhouses at Southampton University, pretending that they were for an important research project. They grew well, and after a year were big enough to plant out. My dad often came down to France with me and it was he who planted them out in 2004 and 2005. He planted fifty in total: five wonky rows of ten, with a generous spacing of ten metres between each tree. The ground is pretty stony and hard to dig, so he often had to use a pickaxe to make a hole, but he stuck at it stubbornly and got there in the end. E
ach small tree he protected against rabbits with a green plastic tube just over a metre tall, tied to a wooden stake.

  To my father’s continuing annoyance, cows break into the meadow from the farm to the south on a regular basis, and invariably make a beeline for the orchard. The stakes seem to make perfect scratching posts for them, but more often than not the weight of the cow leaning against it snaps the stake and pushes the tree over to a precarious angle, so that the orchard needs endless running repairs. My dad seems to have taken this maintenance as a personal battle between himself and his bovine arch-enemies.

  Every year since the orchard was planted, when I go down to Chez Nauche for my first spring visit, I rush eagerly to see how the apple trees are coming along. Apples don’t self-pollinate, so the pips will all grow into crosses between the variety of apple that I ate and whatever it was that pollinated it. This has made watching the trees grow particularly exciting, as I have little idea what type of apple each tree will one day produce. It was not until 2011 that I got my first blossom, on one of the most northerly trees near the hedge. Some bees must have brought pollen from apples in the village a kilometre or so to the east, for the blossom duly set and by late summer the little tree was carrying dozens of tiny, bright-red crab apples. They looked beautiful, but were toe-curlingly sour. Crab apples are great for jelly and cider, but I do hope some of the trees one day produce apples that I can eat.