The Bug That Almost Destroyed the Wine Industry
On the slopes of Sicily’s Mount Etna lies the black, rubbly Calderara Sottana vineyard, locally renowned for the excellence of the wines it produces from Nerello Mascalese and Nerello Cappuccio grapes. When the phylloxera insect ravaged the mountainside in the late nineteenth century, vines in two tiny sections of this vineyard miraculously survived the infestation. Today these vines, still growing on their own roots, are more than 130 years old, and their grapes are vinified separately from those of the grafted vines around them. We had the good fortune to try wines from both sets of vines. They were obviously close relatives, sharing a mineral-like, earthy quality with a hint of tar. The regular Calderara Sottana was wonderful, with dark fruit flavors backed by supple tannins and a lingering finish. But the Prephylloxera blew us away with the brightness and clarity of its fruit, and what we can only describe as an extra layer of finesse.
Although the 1860s did not end that way, they began tranquilly for Jules-Émile Planchon, head of the department of botany at the University of Montpellier, an ancient town in the heart of the southern French wine country. When he had assumed his chair in 1853, the huge French wine industry, which in one way or another employed a third of the national workforce, had been in the throes of dealing with a strange fungal blight. Known as oidium, or powdery mildew, this disease was devastating vineyards across the country. Although viticulturists did not realize it, the fungus responsible had been introduced from the United States during an energetic transatlantic interchange of vine cuttings following the Napoleonic wars. Fortunately, the blight yielded to treatment of the vineyards with sulfur compounds, so by dint of heroic efforts it had been eradicated from most parts of France within a dozen years of its appearance. Indeed, the reorganization of the vineyards entailed by the struggle against the disease proved to be something of a blessing in disguise, and the early 1860s turned out to be a boom period for the modernizing wine trade, as it benefited from massive improvements to France’s transportation infrastructure.
But the serene conditions were not to last. In July 1866, grapevines mysteriously started dying once more in the vineyards of Saint-Martin-du-Crau, a hamlet near Arles, not far from Montpellier. Green leaves turned red and fell; developing grape bunches withered and dried; root tips began to rot. By the following spring the first affected plants were all dead; within a couple of years, symptoms of the disease were appearing in vineyards throughout the Rhône Valley and the breadth of southern France. As Christy Campbell recounts in his entertaining The Botanist and the Vintner, it was clear from the beginning that urgent action was necessary. And in spring 1867 Professor Planchon was appointed to the local Commission to Combat the New Vine Disease. At first, the commission members closely examined vines that had already succumbed to the disease; but even using a microscope, they found no obvious cause. Then Planchon had the idea of pulling up apparently healthy plants growing near the victims. And there was the answer. The roots of these plants were swarming with unfamiliar tiny yellowish insects, all energetically engaged in sucking the sap from their hosts. Planchon immediately concluded that they were the cause of the malady: vampire-like, these insects were sucking the lifeblood out of the plants. Soon he had formally baptized the culprit Rhizaphis vastatrix: “vine-devastating root aphid” (aphids belong to the insect order known as “true bugs,” or Heteroptera, along with greenflies and plant lice). For technical reasons the creature’s official designation eventually became Daktulosphaira vitifoliae (finger-sphere of vine leaves), via the also-abandoned appellation Phylloxera (dry leaf), the name under which it informally continues to strike chills into the hearts of viticulturists worldwide.
After naming the culprit and tracing its first appearance in the region as far back as 1863, Planchon applied his considerable energies to trying to understand its life cycle. This was no matter of idle scientific curiosity: the best way to eliminate any pest is to find a way to interrupt its development. But although Planchon’s meticulous observations taught him a great deal about the bug, he never got the whole story. This is hardly surprising—whereas most insects have only a few stages of development, this one has eighteen. What’s more, the phylloxera bug has specialized on the grapevine to such an extent that all those stages are divided into four major life guilds—sexual, leaf, root, and winged—which coincide exactly with the phases of the vine.
As with all insects, phylloxera bugs start out as eggs, which are laid on the underside of burgeoning grape leaves. When they hatch, the emerging nymphs do not begin eating—in fact, they have no mouth or digestive tract to speak of—because their sole purpose in life at this point is to reproduce. The female and male leaf nymphs find each other, have sex, and then die. Before dying, the female lays a single egg in the bark of the vine’s trunk. At this point, the sexual guild of the life cycle ends, and the leaf guild begins. Usually laid in the early winter, the egg stays dormant until warm weather returns, at which point it hatches and the nymph seeks out the leaves of the grape plant. The nymph is always female and has the remarkable property for an animal that she can reproduce and lay fertile eggs without having sex. She creates a hospitable environment for herself and her eggs by injecting saliva into the leaf, causing a bulbous gall to form. When these new eggs hatch and the nymphs leave the gall, they either stay on the leaves or make the long trek down to the root of the vine. If they make it to the root, they enter the third guild stage and lay more eggs through virgin birth (technically known as parthenogenesis).
Unlike their sexual guild counterparts, at this stage the nymphs’ only goal in life is to eat. As a result, they inflict great damage on the root, especially since one eating strategy involves injecting a secretion that causes the root to soften. This secretion eventually poisons the root, and is one of several reasons for the eventual death of the vine. As the summer proceeds, the nymphs continue to eat and to reproduce through virgin birth for a few more generations. At this stage they can move, though not far, crawling through the soil from one vine to the next. Nevertheless, they can do substantial damage during a single summer and autumn, before winter arrives and the vine becomes dormant.
Life cycle of the Phylloxera bug. Redrawn and modified from Murdick M. McLeod and Roger N. Williams, Grape phylloxera: Ohio State University Extension fact sheet.
When the next summer arrives, the insects become active again, and can disseminate in two ways. One strategy is to remain in the same vineyard, in which case the nymphs emerge and lay both male and female eggs on the undersides of the new leaves, starting a new cycle. But alternatively—and this is how the phylloxera bug really gets around—they may enter the fourth guild of the life cycle by developing wings that allow them to fly away and infect new areas. When they arrive, they lay male and female eggs on pristine new vine leaves, and the cycle starts over.
The sheer complexity of this life cycle might make it seem easy to disrupt, but the reverse proved to be true. For the various stages are so bizarre and apparently unconnected that Planchon had extreme difficulty putting his observations together into a clear picture. So when a solution was finally found to the phylloxera infestation, it came from another direction entirely. But in the interim Planchon’s technical problems paled in comparison to those he encountered in convincing his colleagues that the insect was the cause of the mysterious malady. Most of the members of the commission on which he served agreed with him that the bug was somehow at fault, but a few influential commissioners felt that its presence on diseased plants merely showed that the plants had already been weakened by some other factor. This was probably climatic or the result of bad viticultural practices, or due to inbreeding caused by propagation via cuttings. Such was the conclusion of eminent entomologists in Paris to whom samples of the bug had been sent, and experts from the dominant wine-growing region of Bordeaux echoed it.
The dispute over the cause of the disease raged for years, even as the southern French wine industry continued its slow-motion collapse, and Planchon worked frantically to find ways to combat the disease in the face of official denial of its cause. During 1870 and 1871, in the midst of the chaos of the Franco-Prussian War and the Paris Commune, French officialdom had greater headaches than phylloxera to contend with, but when these conflicts began to settle it was evident even in the capital that France had a major problem on its hands. A prize was offered to anyone who could find the solution.
By this time the vineyards of the Médoc had also become affected, and the root rot was continuing its exponential spread. Between 1875 and 1889, annual French wine production plunged from 84.5 million hectoliters to a paltry 23.4 million. By the end of the 1870s the ravages of the disease were also evident in vineyards in Spain, Germany, and Italy; and as early as 1873 phylloxera had been detected in previously isolated California vineyards, where the bug had probably already been present for a decade or two. A mere four years later, phylloxera was reported from as far afield as Australia. A major economic disaster was unfolding, not only for the wine industry and the millions of people directly dependent on it, but also for the overall economies of France and Europe and eventually of almost the entire wine-producing world.
By the mid-1870s it was beginning to be widely acknowledged outside Montpellier that the phylloxera bug was indeed the primary problem. One major key to this recognition came from the many ingenious efforts made by French growers to control the disease, which had resisted the sulfur treatment that had driven away the powdery mildew. The most successful such expedient involved flooding affected vineyards during the dormant winter season, a practice introduced by the savvy vine grower Louis Faucon. When his diseased vines rebounded after his riverside vineyard had been inundated for a month by freak flooding in early 1869, Faucon asked Planchon to research the effects of water on the phylloxera bug. The professor showed that little more than three weeks’ flooding was enough to drown all the insects and save a vineyard; eventually this simple though labor-intensive approach became widely adopted in France.
Of course, most vineyards are not situated on valley bottoms or carefully constructed terraces that can be flooded and drained at will. Indeed, the majority are on hillsides specifically selected for their good drainage. Nonetheless, although flooding was never going to be a cure-all for the phylloxera blight, Faucon’s insight empirically demonstrated the direct connection that Planchon had already made between the parasite and the disease: do away with the insects, and the disease symptoms disappear.
Also crucial to demonstrating this connection was the discovery of where the pest had originated. And again, Planchon was at the forefront of the search. Almost as soon as the phylloxera bug had been reported and identified in France, an Anglo-American entomologist named C. V. Riley began to wonder whether the European sapsucker was the same as the aphidlike creature, now known as Daktulosphaira vitifoliae, which the New York entomologist Asa Fitch had found living on the leaves of his home-state grapevines in 1854.
An immediate problem, resulting from incomplete knowledge of the pest’s life cycle, was that as far as was known the American insect lived on the vine leaves and didn’t cause disease, while the European variety infested vine roots and did. But this issue was partly resolved when Riley determined that different growth stages were involved in the observed root and leaf infestations. Working closely with Planchon, who visited America in 1873, Riley next showed that when an American vine was grafted onto a European stock the bugs rapidly descended to the roots and stayed there, killing the vine. Riley’s microscopic studies also confirmed that the two insects were identical in both appearance and habits: they were indeed the same bug. It was not lost on Planchon and his colleagues that American vine roots apparently had some feature that the insects preferred to avoid: the bugs confined themselves to the leaves, which might not have been their preferred habitat but from which they could do no long-term harm.
Jules-Émile Planchon (left) and C. V. Riley
Riley’s findings additionally implied—although some resisted this idea, too—that the parasite had been inadvertently introduced into France (at least twice, since the infestations in the Rhône Valley and the Médoc were discovered to have been independent) on vine cuttings imported from America. For although most viticulture in France was proudly based on traditional noble varieties of the Old World vine species Vitis vinifera, some curious French vine growers had taken up the cultivation of American vines for both experimental and decorative purposes. These growers included the Bordeaux winegrower Léo Laliman who, at the same congress in 1869 at which Faucon had presented his ideas on flooding, had reported that while he had lost all his European vines that year, his rows of American vines were still flourishing. Imported to test their resistance to powdery mildew, the American vines were evidently also resistant to the new pest.
But there was a problem. Luxuriantly as they might have grown in the Bordelais environment, the American vines produced wines with unfamiliar “foxy” (grape-jelly) flavors that even Laliman had to pronounce atrocious. So, even if the issue of whether the phylloxera bug was the cause or an effect of the disease was not as yet settled, the search was already under way for American varieties better suited for winemaking than those Laliman had planted.
During the mid-1870s, desperate French winegrowers imported hundreds of thousands of vine cuttings from the United States. They did so against official resistance aimed at preserving the traditional noble French varieties. It is hardly surprising that, after the United States had been identified as the source of the blight, the French government fought against the importation of New World vine varieties. After all, how could the problem provide the solution? Still, even as official approval and funding flowed toward such ploys as submersion, pesticide treatments, enhanced vineyard techniques, the introduction of potential predators, and the shifting of vineyard sites to sterile sandy soils, French vines continued to die.
By the early 1880s, even Paris had to yield to the reality that the most successful attempts at phylloxera control were being made by the provincial winegrowers who a decade earlier, at the urging of Planchon and his Montpellier colleagues, had begun to experiment with the officially disfavored American vine varieties. Soon it became evident that the solution to the phylloxera problem would in some way involve American vines, and the question became how.
The most obvious expedient was to identify American vine strains that would produce a better wine than Laliman’s had, and there were plenty of candidates from which to choose. Many local grapevine species had been domesticated in the United States during the nineteenth century after efforts to raise European vine varieties had failed miserably there, probably because of phylloxera. What’s more, the early introduction of European vines had made it possible for the many native vine species to hybridize with the newcomers, as vines will do, and such mixing events evidently occurred spontaneously on numerous occasions. Promisingly, the offspring of such events tended to combine the qualities of their progenitor lineages. When the American parent was phylloxera-resistant as a result of having co-evolved with the parasite over millions of years (something that Riley, an enthusiastic Darwinian, had noted as early as 1871), the offspring would show at least some of this resistance. At the same time, its European heritage would typically show through in the production of grapes with higher sugar content and a diminution of the foxy flavors that made wine produced from the pure native species unappealing to the Old World palate.
Both hybrid and pure American grapevines of many kinds—it wasn’t always clear which was which—were imported into Europe during the 1870s and 1880s. Not all of them successfully accommodated to their new conditions, sometimes failing to root properly, to propagate effectively, or to grow well. The American Vitis labrusca, for example, a species from the cloudy, rainy Northeast, failed when planted in the hot, arid vinelands of southern France. Still, in the end half a dozen different robust américains became well established both in France and elsewhere east of the Atlantic. Indeed, many European consumers of the inferior wines became accustomed to the foxy flavors that Laliman had deplored—so much so that some French winemakers are even today deeply attached to the American vines and their products, as are many of their clients, including us. Whenever we are in the Dordogne we make a point of visiting a rustic hostelry where the proprietor still surreptitiously grows the American Noah grape, and makes an assertive wine from it that goes particularly well with his braised wild boar.
This does not mean, however, that we aren’t happy to return to the much more subtle vinifera wines after a brief hybrid dalliance. And, indeed, the américains did not turn out to be universally successful. In the Cahors region, for example, famed since medieval times for its dark, tannic “black wines,” the growers who turned to French-American hybrids encountered eventual disaster. Although one apparently accidental cross between the local Auxerrois (Malbec) grape and a variety of the American Vitis rupestris produced an acceptable wine, and hybrid grapes kept the local wine industry ticking over in much diminished form for several decades, in the end the wine made from these vines could not compete with the cheap vinifera wines that began flooding in from Algeria in the first half of the twentieth century. From 175,000 barrels a year in 1816, wine production in Cahors plummeted to a paltry 650 barrels in 1958. But for the efforts of an unsung hero, José Baudel, who revived the local cooperative, and a handful of small growers who managed to keep the Auxerrois going through thick and thin, the Cahors wine industry would have been finished. Now Cahors stands proud again as a producer of wines that may not be as black as they were before, but that, with the toughness of the Auxerrois now tamed by blending with some Merlot and Tannat, can claim to be among France’s most interesting.
The experience of the Cahors growers suggested that almost any viable alternative to the américains would have a good chance of succeeding; and when push came to shove, nearly all straightforward efforts to introduce American vines to France foundered not only on the issue of quality but also in the face of official opposition. The américains were irredeemably tainted by their association with the phylloxera bug as well as by accusations that they were high in methanol—a belief that, unfounded as it may be, still lingers today as your hosts nervously admonish you not to drink too much of that Noah. Government hostility to American vines increased in proportion to their adoption by desperate wine producers, and as the areas of France planted to American vines expanded, official antagonism became implacable. Eventually laws were passed that forbade outright their cultivation anywhere on French soil.
Yet from the beginning of the phylloxera saga an alternative to the wholesale planting of American vines had been available. It depended on the ability of vine cuttings to be grafted onto roots of different stocks. The key factor to a successful graft is that both the scion and the root retain their parental qualities as the plant grows. East Coast North American vine strains had long coexisted with the root-biting phylloxera insect, and many though not all had evolved resistance to its depredations. In its turn, the European species Vitis vinifera had been bred over millennia to produce the finest wine grapes in the world. The combination of American roots and European tops thus potentially offered an ideal marriage.
This fact was recognized early on in the phylloxera crisis. Indeed, at the same time Léo Laliman was initially reporting the demise of the European vines in his Médoc vineyards while their American neighbors flourished, he also noted the potential inherent in grafting. Planchon himself was an advocate, and by 1871 his close colleague the Provençal vine grower Gaston Bazille had already joined European tops to American roots. But this exercise proved to be difficult, and progress was slow. In Cahors, for example, it was found that grafting Auxerrois tops to American roots produced vines that were subject to coulure, a physiological condition in which the grapes failed to develop after flowering. In the end, it took years of trial and error to find the ideal grafting methods and the best scion-rootstock combinations for different soils and climatic conditions. Eventually, the growers learned that sometimes the best roots might actually themselves be hybrid.
Introducing unfamiliar and labor-intensive new practices to many thousands of vine growers around France took even longer, and despite official encouragement success came unevenly. Still, in the end grafting proved to be the way forward, and today all the noble French grape varieties are grown on roots with American ancestry. Only in a few isolated corners of the world—notably Chile—that managed to escape the introduction of the phylloxera bug are the great European Vitis vinifera varieties still grown on a large scale, ungrafted, on their own roots.
For unknown reasons, a few minuscule vineyards in France, Portugal, and Italy also contrived to escape the phylloxera infestation. And all of them have been praised by modern critics for the richness and concentration of their wines compared to grafted local counterparts. Such encomiums lead to the inevitable question: After a century and a half of technical advances in vine growing and winemaking, would the wines of Europe be yet better today if the vines producing them were still growing on their own roots? The reality is that we will never know with certainty, although many twentieth-century connoisseurs were convinced that they would have been. Nonetheless, while for many reasons it would have been much better if the phylloxera epidemic had never happened, the general experience of fruit-tree growers (who have long been enthusiastic grafters) suggests that the grafting process may not make much difference in the quality of the resulting fruit—and hence in the excellence of the wine produced. Still, it’s hard to resist a twinge of regretful nostalgia.
The phylloxera story didn’t end with the defeat of the insect in Europe and elsewhere around the turn of the twentieth century. In an ironic twist, the latest chapter of the saga has unfolded in the United States. For millions of years, California was essentially isolated from the phylloxera-plagued East Coast. So, although wild vines do grow in the western United States, the region was free of the insect when winemaking began in California during the sixteenth century, using the rather undistinguished Mission vine that Franciscan missionaries had imported from Spain. No other varieties were actively planted in California until the 1850s, when vinifera cuttings were introduced from both Europe and the eastern states. It was at this point that the phylloxera bug probably first appeared in California, although it was not formally identified there until 1873. The initial affliction spread relatively slowly, perhaps because, unlike its European counterpart, the California insect did not exhibit a winged phase and thus could not readily disperse. After a slow initial response to the disease, the California grape growers agreed that resistant rootstocks were the way forward, and extensive replanting of existing vineyards was done, based on experience in France and elsewhere. So by the time Prohibition came along, the phylloxera bug was no longer a serious issue in the state.
The more recent problem arose when the California wine industry began to boom during the 1960s and 1970s. Suddenly, demand for California wines soared, and growers began not only to bring new land into cultivation but also to search for rootstocks that would be more productive than the purely American Rupestris Saint George variety that most of them were using at the time. Urged by scientists at the University of California, Davis, and excited by its high yields and easy management, growers rushed to plant or replant with a rootstock known as AxR1, a French-American hybrid initially developed in France during the early period of experimentation. The scions it supported produced abundant grapes, and it was easy to graft and grow, but the AxR1 rootstock had been quickly abandoned in France because of low phylloxera resistance. Ominously, it later also succumbed to phylloxera when planted in Sicily, Spain, and South Africa. Nonetheless, Californian scientists and viticulturists either ignored these red flags, or managed to convince themselves that the parasite would not flourish on the AxR1 under West Coast conditions. Driven by visions of enormous productivity, California growers planted huge areas with this rootstock. By the end of the 1970s, up to two-thirds of the vine-growing areas of the Napa and Sonoma valleys were planted with AxR1.
Inevitably, AxR1 vines in a Napa vineyard began to sicken, in 1980. Soon the cause was confirmed to be phylloxera, and the disease raged through the state. In 1989, the experts at Davis issued a rather tardy warning against further plantings of AxR1, but by then it was too late, and by 1992, in the memorable words of the New York Times correspondent Frank Prial, “the scene across the Napa Valley was desolate. . . . Piles of dead vines pulled from the soil were being burned. . . . Winemakers watched grimly as their lifeworks went up in flames.” The total economic damage was estimated to be about $3 billion, and eventually California wine producers were forced to spend at least half a billion dollars to replant their vineyards with rootstocks of proven resistance.
Fortunately, this herculean effort at phylloxera eradication has so far proven successful; and, for all the trauma it inflicted, the disaster did give wine growers an opportunity to reconsider which varieties were best planted where, and to adjust the compositions of their vineyards accordingly. As a result, the California wine industry has rebounded since the mid-1990s, producing wines that are generally reckoned to be as good as their earlier counterparts.
Perhaps the most important single lesson to be learned from the sad saga of the phylloxera bug and the grapevine is that, if they want to continue making good wine, producers must be constantly on their guard, keeping at least one step ahead of the many organisms that are in competition with wine growers for what the vine has to offer. We can confidently expect that phylloxera will not be the last destructive scourge to infest the vineyards of the world. In addition to all the routine bacterial, fungal, and viral vine diseases, such as powdery mildew, bacterial blight, and leaf scorch, other highly mobile parasites are lurking. A recent bane in California has been the glassy-winged sharpshooter, a lumbering leaf-hopper insect technically known as Homalodisca vitripennis that is a vector for Pierce’s Disease. This bacterial condition blocks the flow of the xylem that conducts water and dissolved minerals around the plant. An infected vine may die within a couple of years. The sharpshooter is a particularly dangerous vehicle for the bacterium because it moves much faster than even the winged phylloxera bug, and can potentially infect large areas rapidly. Clearly, the price of good wine—or of any at all—is going to be eternal vigilance.
In his excellent Dying on the Vine, George Gale, a philosopher of science, makes a point that is of particular relevance in the United States, where in far too many domains we seem to feel that we are not bound by the rules that apply to the rest of the world. He identifies “California exception-alism” as the single most important influence in the unnecessary phylloxera debacle of the late twentieth century. Gale quotes one University of California, Davis, expert, writing shortly before the tragedy struck, as claiming that “both the climate and soils of California are natural agencies which tend to reduce the dangers of phylloxera.” This insouciant attitude was particularly remarkable given the abundant evidence to the contrary supplied by dreadful experiences that had unfolded a bare half-century earlier. Yes, it can happen here. Or anywhere.
