Phylloxera is famous as the pest that destroyed vast areas of European vineyard in the 19th Century, almost wiping out some of the world's greatest wine regions.
As we reported earlier this month, it has now reared its head in the Washington subregion of Walla Walla; but what exactly is phylloxera?
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Grape phylloxera is a tiny pale yellow, aphid like insect from the Phylloxeridae family, within the Hempitera order of bugs. It was described in the 1860s crisis in France as Phylloxera vastratix (devastator of vines), and later found to be the same as the previously described Daktulosphaera vitifoliae or Phylloxera vitifoliae.
The insect is a sap sucker feeding on the roots and leaves of grapevines. Its complex life cycle has up to 18 stages. These can be grouped into four main forms; sexual, leaf, root and winged.
Sexual form infestation can start with one single insect. Firstly a nymph lays male and female eggs on the underside of leaves. These hatch into male and female forms (without mouth parts) which mate and die. But first the female first lays a winter egg in the bark of the vine's trunk. This develops into the leaf form.
The leaf-form nymph – the fundatrix or stem mother – climbs onto a leaf of suckers growing from the rootstock at the base of the vine. She creates galls using saliva; into these she lays eggs parthenogenically (without fertilization). There are no clear signs of phylloxera attack in the upper vine canopy at this stage. Adults can lay up to 200 eggs per cycle.
Root form In turn, these new nymphs may move to other leaves, or to the roots, where they begin new infections in their root form. They pierce the roots to find nourishment, secreting a poison to keep the wounds open. Swellings form on older roots, and characteristic hook-shaped galls form on root hairs. The latter stop the growth of feeder roots, eventually killing the vine. The root form lays eggs for up to seven more generations. Each can also reproduce parthenogenically each summer. Crawlers move to other roots on the same vine, or other vines through cracks in the soil, along the surface or through the canopy. Though unwinged, root form crawlers can be carried short distances in the wind.
Winged form nymphs hatch in autumn and hibernate in the roots until the following spring to feed on rising sap. They restart the cycle by laying new eggs on the leaf underside. In humid areas these nymphs develop winged forms, and so can fly to unaffected vines to start new cycles.
Individual vine plants can be affected at first. Where flying insects are not present, the infestation tends to spread along vine rows more quickly than it jumps across the inter-row spacing.
It is thought that plants affected at the time of planting tend to show signs of decline after a couple of seasons. When an established vineyard comes under attack it may be 10-15 years before the signs become unmissable. By then, ripping out the vines may be the only option.
Soil type and climate have been shown to affect the density of phylloxera populations. The bug prefers humid conditions above and below ground.
Vineyards in schist or sandy soils in warm dry regions fared better in the 19th Century global outbreak. The same applies to many of the areas which have best resisted phylloxera throughout the 20th Century. Examples include Colares in Portugal and Santorini in Greece.
Islands can be safe if the human transport of the insect is controlled. Similarly, Chile has been protected by the Andes on one side, the Pacific on the other and the Atacama desert to the north.
Assyrtiko on Santorini, and the Juan Garcia variety planted on manmade terraces along the Arribes River Canyon in Spain, may be the only two Vitis vinifera varieties with natural resistance to phylloxera. However growing conditions are also very particular in both cases.
There is a major caveat with very dry soils. If the bug does manage to survive, its impact is then amplified by the absence of moisture. This may exacerbate the recent outbreak in the Walla Walla region.
The reproductive cycle of phylloxera is thought to be disrupted by hard winters. However, climate change looks to be playing a role in new outbreaks as winters get milder in many regions. Walla Walla is again one such region.
Most crucially for vineyard owners, American vine species have evolved alongside the insect, and so have developed (varying) degrees of resistance. They exude a sticky sap that clogs the insects' mouth parts. Also, if an insect does open a wound, they can form a protective layer of tissue over it to protect against bacterial and fungal infection.
The phylloxera blight of the late 19th Century
Phylloxera did not suddenly appear in Europe from the ether. Paradoxically, it is understood that the insect was first brought to Europe on specimens of American vines collected by British and European botanists.
The interest in American vines had been prompted by the powdery mildew outbreaks in European vineyards in the 1850s. It was hoped the American vines would show more disease resistance. These vines were still thriving, so alarm bells did not ring.
Technological advances dictated the timing of the outbreak. These included the development of the Ward Case, a sealed glass container which allowed a plant to sit in sunlight on a ship's deck while protected from winds and spray. More generally, the advent of the steamship also contributed.
Vineyards in Britain were devastated first. Then the problem spread to France and much of Europe. In 1863, the first vineyards inexplicably began to die in the Rhône. By 1889, total wine output in France was less than 28 percent that of 1875.
Identifying phylloxera as the culprit
Knowledge spread slowly. Many growers saw their vineyards die without knowing the reason. In France, some took to burying live toads under each vine to draw out the poison.
The complex life cycle of phylloxera makes initial detection tricky. Furthermore, growers rarely dug up healthier-looking vines. By the time dead ones were scrubbed up and inspected, the insects had moved on. The 1866 discovery of phylloxera in vines in the lower Rhône by Jules-Émile Planchon and colleagues is said to have happened because they pulled up a still productive vine by mistake.
Unfortunately this discovery did not lead to a swift coordinated response. Some experts, especially in Paris and Bordeaux, rejected the findings of country bumpkins from the south who were not professional entomologists or plant scientists.
Crucially, many also felt the infestation was a symptom rather than a cause. This reflected the 19th-Century preoccupation with the physiological model of disease, focusing on internal imbalances in the plant rather than external forces acting upon it. Thus they continued to search elsewhere for possible solutions.
Though it would take another five years for opposition to fully dissipate, by around 1869 phylloxera was more widely accepted as the cause. An infested, dying vineyard in the southern Rhône suffered in the spring floods of that year. Once it dried out the insects had gone, and the vines flourished.
It had been noticed that sandy soils seemed to offer some protection. Vineyards were planted in the dunes in the Rhône delta, in areas that would not otherwise have been thought in any way suitable. The success of such plots also supported the idea of phylloxera as cause.
Figures such as Planchon suspected that the vines which carried the insect may also provide a response. Such ideas were supported by now-celebrated American figures such as CV Riley, the state entomologist of Missouri. His Darwinian beliefs led him to appreciate and focus on the resistance to phylloxera in American species.
Hybrids vs grafted vines
Transatlantic cooperation (led by Planchon and Riley) meant that 700,000 vine cuttings were imported to France from St Louis over 1872-73. But knowledge of the American vines was non-existent in France, and very limited in the US, too. Bets were hedged whether rootstocks or direct-producing vines would be more effective, and initial efforts focused, at great cost, on the least effective American species.
However these have a high percentage of Vitis labrusca, which originates in cooler northern forests of the US. The vines struggled in the French heat and, when used as rootstock material or cultivated as whole plants, were less phylloxera-resistant in the new conditions.
Even worse, the wines tasted unpleasant, carrying the musty, foxy hallmarks of labrusca. Many of those growers who placed their faith in these early imports went out of business forever.
Work on grafted vines was hardly less difficult. A successful rootstock would need to graft easily, show longer-term affinity to the French vinifera variety, and have resistance to phylloxera.
The American vines needed to be properly classified, as research led to new species being discovered, most importantly Vitis riparia and Vitis rupestris. Different species have different traits and preferences based on the conditions in which they evolved. And not all wild vines from each species perform the same way.
Careful selection among the various cuttings collected at the University of Montepellier through the 1870s led to focus on the propagation and distribution of around one dozen rootstocks. Riparia Gloire de Montpellier and Rupestris du Lot were among the most successful. By the 1890s further work resulted in a new generation of hybrid rootstocks better suited to French conditions.
In competition to the program at Montpellier, attempts were made – led by the University of Bordeaux – to breed new hybrid varieties which would not need a graft (direct producers). This was based around an optimistic view of genetic inheritance which suggested the rootstock traits of American species could be combined with the fruit systems of French vine parents.
This duality was vigorous until around 1900 and continued less vehemently around the world well into the next century. The hybrids never captured the taste of their vinifera parent, but did prove more hardy in colder climate and for resisting other diseases. Though generally banned for quality wine in the EU, many of these varieties remain stalwarts of the North American wine industry outside California, Oregon and Washington.
Other attempts to combat phylloxera
The idea of using American vine species to fight back caused great conflict in France. They were viewed by many as the villain of the story. But, more powerfully, many figures within the French wine industry did not wish, at any price, to compromise the integrity of French vineyards, grape varieties and wine by introducing alien plant material. These groups instituted a phase of non-biological countermeasures known as La Défense based on sand and water.
Flooding techniques require a great deal of infrastructure, and the government was slow to plan the necessary canals. (War with Prussia ended in 1871. The conflict and its aftermath limited the effectiveness of French government throughout this period.) Nevertheless as many as 40,000 hectares (100,000 acres) were flooded.
Total plantings in sand topped out at around 20,000ha (50,000 acres). Even today there are still vineyards dotted around the dunes of Aigues-Mortes in the Carmargue Gardoise. However, in sand almost all vine nutrition must be supplied via fertilizers. Attempts to pump river silt onto the plots only served to reintroduce the pest. Coastal winds in these sandy sites were often also problematic as they carried away the sand. The wines tasted very different to those previously made further inland, if still drinkable.
Insecticide trials in the 1870s were championed by the government and the Academie Française. Most were laughable, all were ineffective and only served to shift emphasis away from rootstock-based strategies.
Treatments using the volatile chemical solvent carbon disulfide, as developed by Baron Paul Thenard, proved the most effective. This oily liquid settles in the soil and asphyxiates bugs; it proved particularly effective on phylloxera, but did not kill all of them. This meant annual treatments were necessary, which gradually weakened the vine. In addition, skilled workers were needed, it was only effective in the best, most aerated and fertile soils, and cost more than most growers could afford.
The Champagne region, far to the north, avoided the worst effects of the pest until the early 1890s. As late as 1890 the local trade journal was recommending the planting of alfalfa, lupins and sainfoin in the vineyards to keep phylloxera at bay.
But eventually, all the blind alleys were abandoned. A greater focus on replanting with hybrid rootstocks became known as La Reconstitution. By 1900, France had the pest under some semblance of control.
Global spread of phylloxera
Phylloxera spread to other European countries either via American or French cuttings, or by both. Italy and Spain's wine industries were hit from the 1870s, along with Portugal Germany and Switzerland. Phylloxera was found in California in 1874 near the city of Sonoma. By 1900, 12,000ha (30,000 acres) had been destroyed across the state.
The Balkans and Greece suffered from around the turn of the century. Around the same time, in Australia, Victoria and New South Wales were affected. However, strict quarantines and restrictions on transporting plant matter protected other regions, including those in the state of South Australia.
Many French firms planted heavily in what is now Croatia and Slovenia. These vines were ravaged between 1902 and 1905, prompting emigration that would energise wine industries in North America and Australasia.
In the early 20th Century, the global industry could at least draw on conclusions reached the 30 years of debate in France. Use of carefully selected grafted rootstocks on vinifera scions (and to a lesser extent, resistant hybrid varieties) seemed to stabilize the situation for much of the 20th Century.
Rootstocks vs phylloxera in the 20th Century
Not all rootstocks are equally resistant. And the resistance that any rootstock offers can diminish with time. One main reason is that Phylloxera mutates when faced with resistant vines. There are now several hundred genetic strains of phylloxera documented worldwide.
In the 1990s in California, many vines grafted to the widely used AXr1 (Aramon Rupestris Ganzin No.1) were found to be infested. Some commentators suggested this was inevitable as Aramon is a vinifera variety. But other such hybrids such as 41B have continued to be more effective.
Investigations showed that phylloxera had mutated into "Biotype B", which could overcome the rootstocks resistance. Around two-thirds of the vineyards in Napa had to be replanted. It was the cost of replacing phylloxera-ravaged vineyards that obliged the Mondavi family to take their company into public ownership.
Another important point is that only some rootstocks have such resistance that the insect does not lay eggs. In many grafted vineyards, phylloxera can still survive and reproduce, just with less devastating consequences. As happened with transatlantic cuttings in the late 19th Century, this population can spread to ungrafted vines at a later date.
Similarly, sandy soils are not infallible. The famous Bien Nacido Vineyard in the Santa Maria Valley AVA is is planted with own root vines, which have stayed phylloxera-free thus far. But in Jumilla, Spain, Casa Castillo's Pie Franco (French Foot) red comes from a plot of own-root Monastrell vines, planted in 1942 in sandy soils. However, the pest took hold after a number of decades; every year another few vines die and volumes of the wine diminish. In Champagne in 2004, Bollinger lost one of the ungrafted parcels that went into its Vieilles Vignes cuvée. Phylloxera had been discovered six years before.
In fact, many growing regions have given insufficient consideration (with the benefit of hindsight) to rootstock choice. This is not necessarily due to trust in soil types or other mitigating factors. Many of these regions have developed since the 1960s and were more focused on expansion. Grafted vines cost three times as much as ungrafted vines, sometimes more.
Phylloxera has been present in some form in the state of Washington since the 1910s. But this year it made its presence in the important Walla Walla region was reported for the first time. This area is particularly at risk because many growers here chose to plant own-rooted vines.
The reasoning was that the harsh winters slowed down phylloxera reproduction. Added to this, grated vines are reported to recover more slowly from frost. Moreover there are plenty of dry sandy soils here. But climate change means that luck has run out, as the hard freezes are becoming rarer.
On New Zealand's South Island, phylloxera was discovered in the Central Otago wine region in 2002. Rapid expansion meant that it was estimated at that time that only 55 percent of vines were on resistant rootstock. This was well below the figure for other regions in the country. Harsh winters were an insufficient safeguard here.
Phylloxera: present and future
There is still no "cure" for vines that have been attacked by phylloxera. Neither are there chemical or biological controls to prevent it taking hold. Flooding the vines is rarely even a last resort. Currently, the best solution remains to rip out a vineyard and plant on more suitable rootstocks. One possible silver lining is that the grower can choose a more suitable clone, or change the grape variety, but the financial implications can be huge.
Choice of (currently commercially available) rootstock remains complicated. Aside from suitability for local soil and macroclimate, viticulturalists also have to be aware which particular strain(s) of phylloxera they are up against. Vinehealth Australia (formerly the Phylloxera and Grape Industry Board of South Australia) tests rootstocks against at least seven strains.
Around the world protocols continue to be introduced to control the movement of machinery and people between vineyards. The machinery might be steam cleaned, and staff may have footwear specific to each site they must visit.
Allied to this, passes through the vineyard, mechanized or manual, may be kept to a minimum. This would seem to make sense in an affected vineyard, but otherwise growers (especially biodynamic practitioners) will want or need to have a high degree of vigilance. Often these measures are voluntary, however.
Research is underway to introduce new, more resistant rootstocks to combat phylloxera's ability to develop new biotypes to overcome specific rootstocks' defences. A 2018 study (Smith et al, BMC Plant Biology) examining the genetic factors of phylloxera resistance in rootstocks identified a single allele (RDV2) that confers that trait.
Also in 2018, Vinehealth Australia reported that it had successfully trialled DNA profiling techniques to detect genetic material of phylloxera in vineyard soil cores. Though sample taking is easy, the storage and transport conditions are crucial (as is laboratory availability). Therefore it may take some time for this become common practice. But together with use of drones to provide cost effective aerial imagery, at least Australian wine producers may soon have a viable early warning system toolkit.