Darwin Comes to Town

by Menno Schilthuizen

  In the previous chapters, we have seen animals and plants adapt to the physical features of the city: its countenance of glass and steel, the deadly pulse of its traffic-filled veins, the luminous mantle of artificial light that it cloaks itself in, and the trickles of foul chemicals oozing from its pores. All of these evolutionary events are the result of one particular type of close encounter between the urban environment and wild animals and plants. Let’s call those close encounters of the first kind: the evolving organism is the moving part, the physical feature is static.

  For example, in 2017, Sarah Diamond of Case Western Reserve University discovered that acorn ants (Temnothorax curvispinosus) adapt to the urban heat island. A colony of speck-like acorn ants fits inside a single acorn, and since oak trees occur both inside and outside the city, Diamond and her colleagues could investigate the ants’ tolerance of higher temperatures simply by picking up acorns with ants inside and moving them to warmer or colder places. In doing so, they discovered that the city ants could stand the heat a bit better than their rural formicine relatives and they also proved that this difference is partly genetic. Once again, a very nice example of urban evolution, similar to many others we have seen before. But it is important to remember that this is a one-way adaptation. The heat island itself is completely unaffected by the fact that this animal has adapted to it.

  Obviously, there will be no feedback between the acorn ant’s evolving ability to stand the urban heat and the heat island itself. But, the same is not necessarily true for close encounters of the second kind, such as the unfortunate interaction between catfish and pigeons in Albi, France. Here, a situation is created where both sides of the interaction could adapt to one another. The catfish could evolve to improve their bird-grabbing abilities, whereas the pigeons could evolve a greater wariness around water. At the moment there is no evidence yet that either species is evolving. Still, the scene is set for such two-way evolution.

  Being either one-way or two-way evolution is one important distinction between the close urban encounters of the first and second kind. But there is more. The first kind could, in principle, come to a standstill. As soon as, say, the mummichog of Bridgeport have reached peak tolerance to PCBs, this evolutionary process is completed. The newly evolved, PCB-adapted mummichog will continue living in its polluted waters for as long as it likes. With the second kind, such an evolutionary backwater may never be reached. If the pigeons evolve a more circumspect personality, this may result in the catfish evolving a greater speed of attack, leading to the pigeons evolving a quicker flight response, which could then precipitate a greater sensitivity of the catfish whiskers, and so on, and so forth. It is not likely that this will actually happen, if only because the catfish does not depend entirely on pigeons for food, and because there may be catfish-free places for the pigeons to do their daily ablutions. But, in theory, we could see endless cycles of mutual urban evolution of catfish offense and pigeon defense.

  The endlessness of evolutionary adaptation when the thing that one adapts to is not a physical feature but another organism that can itself evolve is what makes this second type of evolution so powerful. The evolution of one partner fuels the evolution of the other partner, and the net effect is that they remain locked in an ecological interaction with one another, like two countries forced to engage in a perpetual arms race simply to prevent one from overrunning the other. It is for this reason that evolutionary biologists call this type of antagonistic adaptation “The Red Queen,” after the character in Through the Looking Glass, who told Alice, “Now, here, you see, it takes all the running you can do, to keep in the same place.”

  But the evolving partners do not even have to be archenemies in order to influence each other’s evolution. All animal and plant species in the urban environment form knots in a gigantic, constantly changing tapestry of ecological interactions. Sure, there are plenty of species in this vast urban ecosystem that are at each other’s throats. But there are also many that simply jostle for space in the cracks of the pavement, or that help each other gain a foothold. Think of the sparrows nesting in the ivy growing on buildings, or the springtails finding shelter among the succulent plants on green roofs. Whatever the interaction, chances are that if one species evolves, this will also affect some of the other species that are tied with it in the urban ecological web. No species, after all, is an island.

  As we have seen before, cities are like mad scientists, creating their own crazy ecological concoctions by throwing all kinds of native and foreign elements into the urban melting pot. Our gardens, balconies, and parks are stocked with plants from all over the world, which then provide food for a motley crew of animals from all continents. In Paris, Indian ring-necked parakeets are eating seeds of the black locust trees from North America. In Malaysian cities, European rock pigeons are ripping out the flower buds of Chinese hibiscus bushes planted along the pavements. In Perth, the Indian northern palm squirrel was released in 1898 and since then has maintained a healthy population thanks to the abundant fruits of African date palms and other exotic palm trees in the city.

  The urban loom weaves food webs from weft and warp that are thrown together by chance, linking species in new and exciting patterns. Since such ecological interactions are marriages of convenience, rather than matches made in heaven, the species thus linked may evolve adaptations to dealing with their new ecological counterparts. Some of the finest examples of this come from plant-eating animals, so-called herbivores. In Florida, for example, one can find the native soapberry bug, Jadera haematoloma. This insect feeds on the seeds of the (also native) balloon vine, Cardiospermum corindum. The balloon vine is so named because it carries its tiny seeds inside a green bubble of two centimeters in diameter, and the soapberry bug plies its nearly 9-mm-long snout to pierce that bubble and juuuust manage to get to the seeds in the center.

  Around 1955, the Taiwanese raintree (Koelreuteria elegans) was one of the exotic trees that the Florida parks authorities began planting in parks and along roadsides. The raintree is related to the balloon vine, but has a much smaller and flatter seed capsule. At some point after its arrival, soapberry bugs began eating the seeds of the raintree as well. And, as Scott Carroll of the University of California discovered in the 1990s, as a consequence, the raintree-dwelling bugs evolved, almost to the extent of becoming a separate species. Just forty years after the raintree began to become a common sight along Florida’s streets, the bugs living on them lay more, but smaller, eggs, they develop faster, and they are attracted by the scent of raintrees, not balloon vine. But the most eye-catching difference is in their snouts, which, in the bugs on raintrees, are shorter: only about 6.5 to 7 mm long. Shorter than in their balloon vine–dwelling ancestors (in fact, too short to be any good on a balloon vine pod), but long enough to reach the seeds inside the much smaller seed capsules of the raintree. What’s more, Carroll showed that all these differences between the old and the new version of the soapberry bug are coded in their DNA.

  In 2005, Carroll announced a cute further twist to this story. For in Australia, the same sequence of events unfolded itself, but then, in good Notogean fashion, upside down. In Brisbane, another species of soapberry bug, Leptocoris tagalicus, lived mainly on the native woolly rambutan (Alectryon tomentosus), until the American balloon vine was introduced there, eventually becoming a nationwide pest around 1960. Roundabout that year, the Australian soapberry bugs, sufficiently provoked by the balloon vine’s abundance, hopped onto it. Carroll measured the snout lengths of pinned Leptocoris in Australian natural history museums and discovered that before 1965, they all had short snouts, whereas after that year, longer-snouted individuals began to appear. These pre-1965 longsnouters presumably were the first ones to have colonized and adapted to balloon vine. Today, as Carroll discovered, the Leptocoris tagalicus bugs on balloon vine have snouts a tad longer than those on the woolly rambutan, long enough better to reach into balloon vine seeds.

  The Pinocchio-like growing and shrin
king of soapberry bugs’ noses is a textbook example of herbivores evolving after they jump to a new, introduced food plant. Many of these cases come, of course, from agriculture, where such a shift onto a crop usually means the dreaded appearance of a new pest. In the Hudson River Valley of the US, for example, the native hawthorn fly spawned a new species that, over the past few hundred years, adapted to the apple after it was introduced there by settlers from Europe. The apple maggot fly (Rhagoletis pomonella) has by now become so different from the hawthorn fly that many consider it a separate species. And in Europe, Ostrinia scapulalis, a native moth burrowing in the stems of the native plant mugwort, also gave rise to a new species, Ostrinia nubilalis (the European corn borer) when maize was brought to Europe from America around 1500. Within that half millenium, the European corn borer has evolved lots of maize-specific adaptations, including one particularly delightful one. In late summer, the caterpillars chewing away inside the plant stalks go into so-called “diapause,” basically an extended holiday before the hard work of metamorphosis begins. But while Ostrinia scapulalis caterpillars install themselves somewhere in the middle of their plant’s stalk, those of Ostrinia nubilalis first burrow down the corn stalk until close to ground level. Why? Think of the decades of natural selection caused by the late summer onslaught of the corn harvesting combine, and you’ll probably know the answer!

  Scientists have now accumulated evidence of dozens of plant-eaters colonizing an exotic plant and then evolving in ways similar to the soapberry bug, the apple maggot fly, and the European corn borer. My students and I also contributed: we discovered that in the north of the Netherlands, the leaf beetle Gonioctena quinquepunctata moved from the native rowan tree (Sorbus aucuparia) to the notorious invasive American black cherry (Prunus serotina), a shift that is very recent (it happened around 1990), but that already shows up as changes in several of the beetle’s genes.

  Plant-eating animals adapting to a new food plant form one aspect of the Red Queen game. The reverse, plants adapting to new plant-eating animals, is another. Cordgrass, for example, is a tough type of grass that grows on coastal marshes along all coasts of the Atlantic Ocean. With such a reputation and an equally awe-inspiring scientific name, Spartina has been the plant of choice for constructing bull’s eyes on archery targets and has also been sturdy enough to hitch rides with humans across the globe to salt marshes on all the world’s shores. Smooth cordgrass, Spartina alterniflora, for example, is a species from the North American east coast, but humans have accidentally carried it to the continent’s west coast where it now thrives in places as diverse as Washington state’s pristine Willapa Bay (where it has lived since around 1900) and the urbanized shores of San Francisco Bay (year of arrival: 1970).

  But being in an urban or a rural environment is not the only difference between these two new homes for smooth cordgrass. For in Willapa Bay, the grass is blissfully unaffected by any insect pests, whereas in Frisco, it finds its leaves sucked dry by the plant-hopper Prokelisia marginata, an east coast insect that is as non-native to the city as people who say “Frisco.” Two researchers, Curtis Daehler and Donald Strong, studied in a greenhouse whether this difference in herbivory has made the cordgrass in both places evolve in different ways. Sure enough, they found that the San Francisco plants, when attacked by the plant-hoppers, only lost about 20 percent of their leaves and happily lived on, whereas the ones from three states up, evolutionarily unprepared for the insect, suffered 80 percent leaf loss and nearly half of them succumbed. Apparently, the two cordgrass colonies had evolved opposite pest resistance, perhaps having to do with the chemicals they use to make their leaves unpalatable.

  In a newly discovered twist, some of the chemicals that plants use to defend themselves against plant-eating insects pass through human hands, to be then used as natural insecticide by birds to fumigate their nests with. Okay, read that sentence once more. Sounds intriguingly convoluted, right? Well, imagine how intrigued the Mexican ornithologist Monserrat Suárez-Rodriguez was when, in 2011, she began discovering discarded cigarette butts in the nests of house sparrows and house finches at the Campus of the National University of Mexico in Mexico City. Discarded cigarette butts are a ubiquitous urban eyesore all over the world. We are all taught at school not to throw any litter on the street, but smokers appear to have collectively decided that this obviously does not apply to the cool photogenic finger flick with which they rid themselves of butt leftovers. Globally, 5 trillion (yes, that’s a five with twelve zeroes) filter cigarettes are smoked per year, and many of those filters end up in the environment, where they take several years to degrade. No wonder, perhaps, that the Mexican urban birds could not avoid mixing them in with their nest material. Suárez-Rodriguez found up to forty-eight butts per nest. Basically, these birds were brooding in an ashtray.

  But was it really an accidental inclusion into the birds’ nest material, or was there perhaps something else going on, Suárez-Rodriguez wondered. After all, some birds are known to incorporate green plants in their nests, because the chemical compounds in the leaves keep mites, fleas, and lice at bay. And since cigarettes are made of leaves of the tobacco plant, whose main anti-insect agent is nicotine, perhaps the campus birds benefited indirectly from the human penchant for that same chemical compound. To test this, Suárez-Rodriguez and her colleagues measured the amount of cigarette butts in some sixty nests and also counted the numbers of mites in them. They found a beautiful negative relationship: more butts meant fewer mites, while birds that refused to turn their nests into smokers’ dens paid a dear price for their cleanliness. They had to share their nests with up to a hundred blood-sucking mites, whereas the nests with more than ten grams of cigarette material were virtually free of mites.

  Unfortunately, we don’t know yet what lies at the root of these bird equivalents of the bug bomb. It could be that the birds are sensing nicotine in the butts and are treating them as if they were the fresh plant leaves they would otherwise have integrated with their nest material. It could also be that, over successive generations, the birds learned that nests with more butts were more comfy. Or, the behavior could have a genetic basis and be a newly evolved defense of bird against bug. If so, the next task for the Mexican researchers would be to see if urban bird-nest mites are evolving a nicotine resistance.

  Granted, what I have shown you here are not really full cycles of Red Queen evolution. We’ve seen herbivores adapting to plants that humans have brought into their environment, and we’ve seen other plants adapting to herbivores that feed on them thanks to human intervention. We have even seen birds controlling their parasitic mites with insecticides derived from plants and made available by urbanites’ smoking habits. What we haven’t got yet are good examples of the same ecological interaction going through successive evolutionary cycles of attack, defense, counterattack, and counter-defense. This probably has to do more with the fact that most biologists are either zoologists or botanists (so they will view the interaction either from the plant’s or the herbivore’s viewpoint), than with a rarity of such events. We see fragments of such cycles in different species, so it is quite likely that there are new urban ecological relations that are actually going through such tit-for-tat adaptation right here, right now.

  15

  SELF-DOMESTICATION

  A crumbling concrete wall, a ramp, and a vast expanse of tarmac on which identical silvery-gray sedans are slowly circling and zigzagging between traffic cones. It does not seem like much, but to urban biologists the Kadan driving school in the Japanese city of Sendai is hallowed ground. The four of us (biology students Minoru Chiba and Yawara Takeda, biologist Iva Njunjić, and I) have been sitting on that crumbling wall now for several hours, hoping to observe what this place is famous for.

  It is here that, in 1975, the local carrion crows (Corvus corone) discovered how to use cars as nutcrackers. The crows have a predilection for the Japanese walnut (Juglans ailantifolia), which grows abundantly in the city. The pretty nuts (a bit sm
aller than commercial walnuts, and with a handsome heart-shaped interior) are too tough for the crows to crack with their beaks, so for time immemorial they have been dropping them from the air onto rocks to open them. Everywhere in the city, you find parking lots strewn with the empty nutshells: the crows either drop them in flight or carry them to the tops of adjoining buildings and then throw them over the edge onto the asphalt below.

  But all this flying up and down is tiring, and sometimes the nuts need to be dropped repeatedly before they split. So, at some point, these crows came up with a better idea. They would drop nuts among the wheels of slow-driving cars, and pick up the flesh after the car had passed. The behavior started at the Kadan driving school, where there are plenty of slow-moving cars, was copied by other crows, and so spread to other places in the city where slow-moving giant nutcrackers were common, such as near sharp bends in the road, and at intersections. At such places, rather than dropping the nuts from above, the crows would station themselves by the roadside and place them more accurately on the road. Since then, the fad has also turned up in other cities in Japan.

  A zoologist of Sendai’s Tohoku University, Yoshiaki Nihei, made a detailed study of the behavior. He observed how the crows would wait near a traffic light, wait for it to turn red, then step in front of the cars, place their nuts, and hop back to the curb to wait for the lights to turn. When the traffic had passed, they would return onto the tarmac to retrieve their quarry. His work revealed the crows’ finesse in handling their “tool.” For example, the birds would sometimes move a walnut a few centimeters if it took too long for it to be hit by a wheel. In one case, he even saw how a crow would walk into the path of an oncoming car, forcing it to brake, and then quickly toss a nut in front of its wheels.