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Grape phylloxera is an insect pest of commercial
grapevine ''Vitis'' (grapevine) is a genus of 79 accepted species of vining plants in the flowering plant family Vitaceae. The genus is made up of species predominantly from the Northern Hemisphere. It is economically important as the source of grapes, b ...
s worldwide, originally native to eastern North America. Grape phylloxera (''Daktulosphaira vitifoliae'' (Fitch 1855) belong to the family Phylloxeridae, within the order Hemiptera, bugs); originally described in France as ''Phylloxera vastatrix''; equated to the previously described ''Daktulosphaera vitifoliae'', ''Phylloxera vitifoliae''. The insect is commonly just called phylloxera (; from grc, φύλλον, leaf, and , dry). These almost microscopic, pale yellow sap-sucking
insect Insects (from Latin ') are pancrustacean hexapod invertebrates of the class Insecta. They are the largest group within the arthropod phylum. Insects have a chitinous exoskeleton, a three-part body (head, thorax and abdomen), three pairs ...
s, related to
aphid Aphids are small sap-sucking insects and members of the superfamily Aphidoidea. Common names include greenfly and blackfly, although individuals within a species can vary widely in color. The group includes the fluffy white woolly aphids. A ...
s, feed on the roots and leaves of grapevines (depending on the phylloxera genetic strain). On ''
Vitis vinifera ''Vitis vinifera'', the common grape vine, is a species of flowering plant, native to the Mediterranean Basin, Mediterranean region, Central Europe, and southwestern Asia, from Morocco and Portugal north to southern Germany and east to northern ...
'', the resulting deformations on roots ("nodosities" and "tuberosities") and secondary fungal infections can
girdle A belt, especially if a cord or rope, is called a girdle if it is worn as part of Christian liturgical vestments, or in certain historical, literary or sports contexts. Girdles are used to close a cassock in Christian denominations, including ...
roots, gradually cutting off the flow of nutrients and water to the vine.Wine & Spirits Education Trust ''"Wine and Spirits: Understanding Wine Quality"'' pgs 2-5, Second Revised Edition (2012), London,
Nymphs A nymph ( grc, νύμφη, nýmphē, el, script=Latn, nímfi, label=Modern Greek; , ) in ancient Greek folklore is a minor female nature deity. Different from Greek goddesses, nymphs are generally regarded as personifications of nature, are ty ...
also form protective
gall Galls (from the Latin , 'oak-apple') or ''cecidia'' (from the Greek , anything gushing out) are a kind of swelling growth on the external Tissue (biology), tissues of plants, fungi, or animals. Plant galls are abnormal outgrowths of plant tissu ...
s on the undersides of grapevine leaves of some ''Vitis'' species and overwinter under the bark or on the vine roots; these leaf galls are typically only found on the leaves of American vines. American vine species (such as ''
Vitis labrusca ''Vitis labrusca'', the fox grape, is a species of grapevines belonging to the '' Vitis'' genus in the flowering plant family Vitaceae. The vines are native to eastern North America and are the source of many grape cultivars, including Catawb ...
'') have evolved to have several natural defenses against phylloxera. The roots of the American vines exude a sticky sap that repels the nymph form by clogging its mouth when it tries to feed from the vine. If the nymph is successful in creating a feeding wound on the root, American vines respond by forming a protective layer of tissue to cover the wound and protect it from secondary bacterial or fungal infections. Currently there is no cure for phylloxera and unlike other
grape diseases This is a list of diseases of grapes (''Vitis'' spp.). Bacterial diseases Fungal diseases Miscellaneous diseases and disorders Nematodes, parasitic Phytoplasma, virus and viruslike diseases See also *''Ampeloglypter ater'' *''Amp ...
such as powdery or
downy mildew Downy mildew refers to any of several types of oomycete microbes that are obligate parasites of plants. Downy mildews exclusively belong to the Peronosporaceae family. In commercial agriculture, they are a particular problem for growers of c ...
, there is no chemical control or response. The only successful means of controlling phylloxera has been the
grafting Grafting or graftage is a horticultural technique whereby tissues of plants are joined so as to continue their growth together. The upper part of the combined plant is called the scion () while the lower part is called the rootstock. The succ ...
of phylloxera-resistant American rootstock (usually hybrid varieties created from the '' Vitis berlandieri'', '' Vitis riparia'' and ''
Vitis rupestris ''Vitis rupestris'' is a species of grape native to the United States that is known by many common names including July, Coon, sand, sugar, beach, bush, currant, ingar, rock, and mountain grape. It is used for breeding several French-American hy ...
'' species) to more susceptible European ''vinifera'' vines.


Biology

Phylloxera has a complex life-cycle of up to 18 stages, that can be divided into four principal forms: sexual form, leaf form, root form, and winged form. The ''sexual form'' begins with male and female eggs laid on the underside of young grape leaves. The male and female at this stage lack a digestive system, and once hatched, they mate and then die. Before the female dies, she lays one winter egg in the bark of the vine's trunk. This egg develops into the ''leaf form''. This nymph, the fundatrix (stem mother), climbs onto a leaf and lays eggs
parthenogenetic Parthenogenesis (; from the Greek grc, παρθένος, translit=parthénos, lit=virgin, label=none + grc, γένεσις, translit=génesis, lit=creation, label=none) is a natural form of asexual reproduction in which growth and developmen ...
ally in a leaf gall that she creates by injecting saliva into the leaf. The nymphs that hatch from these eggs may move to other leaves, or move to the roots where they begin new infections in the ''root form''. In this form they perforate the root to find nourishment, infecting the root with a poisonous secretion that stops it from healing. This poison eventually kills the vine. This nymph reproduces by laying eggs for up to seven more generations (which also can reproduce parthenogenetically) each summer. These offspring spread to other roots of the vine, or to the roots of other vines through cracks in the soil. The generation of nymphs that hatch in the autumn hibernate in the roots and emerge next spring when the sap begins to rise. In humid areas, the nymphs develop into the ''winged form'', else they perform the same role without wings. These nymphs start the cycle again by either staying on the vine to lay male and female eggs on the bottom side of young grape leaves, or flying to an uninfected vine to do the same. Many attempts have been made to interrupt this life cycle to eradicate phylloxera, but it has proven to be extremely adaptable, as no one stage of the life cycle is solely dependent upon another for the propagation of the species.


Fighting the "phylloxera plague"

In the late 19th century the phylloxera epidemic destroyed most of the vineyards for
wine Wine is an alcoholic drink typically made from fermented grapes. Yeast consumes the sugar in the grapes and converts it to ethanol and carbon dioxide, releasing heat in the process. Different varieties of grapes and strains of yeasts are ...
grape A grape is a fruit, botanically a berry (botany), berry, of the deciduous woody vines of the flowering plant genus ''Vitis''. Grapes are a non-Climacteric (botany), climacteric type of fruit, generally occurring in clusters. The cultivation of ...
s in Europe, most notably in France. Phylloxera was introduced to
Europe Europe is a large peninsula conventionally considered a continent in its own right because of its great physical size and the weight of its history and traditions. Europe is also considered a subcontinent of Eurasia and it is located enti ...
when avid botanists in Victorian England collected specimens of American vines in the 1850s. Because phylloxera is native to North America, the native grape species are at least partially resistant. By contrast, the European wine grape ''
Vitis vinifera ''Vitis vinifera'', the common grape vine, is a species of flowering plant, native to the Mediterranean Basin, Mediterranean region, Central Europe, and southwestern Asia, from Morocco and Portugal north to southern Germany and east to northern ...
'' is very susceptible to the insect. The epidemic devastated vineyards in Britain and then moved to the European mainland, destroying most of the European grape growing industry. In 1863, the first vines began to deteriorate inexplicably in the southern Rhône region of France. The problem spread rapidly across the continent. In France alone, total wine production fell from 84.5 million
hectolitre The litre (international spelling) or liter (American English spelling) (SI symbols L and l, other symbol used: ℓ) is a metric unit of volume. It is equal to 1 cubic decimetre (dm3), 1000 cubic centimetres (cm3) or 0.001 cubic metre (m3). ...
s in 1875 to only 23.4 million hectolitres in 1889.winepros.com.au Some estimates hold that between two-thirds and nine-tenths of all European vineyards were destroyed. In France, one of the desperate measures of grape growers was to bury a live
toad Toad is a common name for certain frogs, especially of the family Bufonidae, that are characterized by dry, leathery skin, short legs, and large bumps covering the parotoid glands. A distinction between frogs and toads is not made in scient ...
under each vine to draw out the "poison". Areas with
soil Soil, also commonly referred to as earth or dirt, is a mixture of organic matter, minerals, gases, liquids, and organisms that together support life. Some scientific definitions distinguish ''dirt'' from ''soil'' by restricting the former ...
s composed principally of sand or
schist Schist ( ) is a medium-grained metamorphic rock showing pronounced schistosity. This means that the rock is composed of mineral grains easily seen with a low-power hand lens, oriented in such a way that the rock is easily split into thin flakes ...
were spared, and the spread was slowed in dry climates, but gradually phylloxera spread across the continent. A significant amount of research was devoted to finding a solution to the phylloxera problem, and two major solutions gradually emerged: grafting cuttings onto resistant rootstocks and hybridization.


Response

By the end of the 19th century, hybridization became a popular avenue of research for stopping phylloxera. Hybridization is the breeding of ''
Vitis vinifera ''Vitis vinifera'', the common grape vine, is a species of flowering plant, native to the Mediterranean Basin, Mediterranean region, Central Europe, and southwestern Asia, from Morocco and Portugal north to southern Germany and east to northern ...
'' with resistant species. Most native American grapes are naturally phylloxera resistant ('' Vitis aestivalis'', ''rupestris'', and ''riparia'' are particularly so, while ''
Vitis labrusca ''Vitis labrusca'', the fox grape, is a species of grapevines belonging to the '' Vitis'' genus in the flowering plant family Vitaceae. The vines are native to eastern North America and are the source of many grape cultivars, including Catawb ...
'' has a somewhat weak resistance to it) but have aromas that are off-putting to palates accustomed to European grapes. The intent of the cross was to generate a hybrid vine that was resistant to phylloxera but produced wine that did not taste like the American grape. The hybrids tend not to be especially resistant to phylloxera, although they are much hardier with respect to climate and other vine diseases. The new hybrid varieties have never gained the popularity of the traditional ones. In the EU they are generally banned or at least strongly discouraged from use in
quality wine Quality wines produced in specified regions (often abbreviated to quality wines psr, QWpsr or simply "quality wines") is a quality indicator used within European Union wine regulations. The QWpsr category identifies wines with protected geograph ...
, although they are still in widespread use in much of North America, such as Missouri, Ontario, and upstate New York.


Grafting with resistant rootstock

Use of a resistant, or tolerant, rootstock, developed by Charles Valentine Riley in collaboration with J. E. Planchon and promoted by T. V. Munson, involved grafting a ''
Vitis vinifera ''Vitis vinifera'', the common grape vine, is a species of flowering plant, native to the Mediterranean Basin, Mediterranean region, Central Europe, and southwestern Asia, from Morocco and Portugal north to southern Germany and east to northern ...
'' scion onto the roots of a resistant '' Vitis aestivalis'' or other American native species. This is the preferred method today, because the rootstock does not interfere with the development of the wine grapes (more technically, the
genes In biology, the word gene (from , ; "... Wilhelm Johannsen coined the word gene to describe the Mendelian units of heredity..." meaning ''generation'' or ''birth'' or ''gender'') can have several different meanings. The Mendelian gene is a b ...
responsible for the grapes are not in the rootstock but in the scion), and it furthermore allows the customization of the rootstock to soil and weather conditions, as well as desired vigor. Not all rootstocks are equally resistant. Between the 1960s and the 1980s in
California California is a state in the Western United States, located along the Pacific Coast. With nearly 39.2million residents across a total area of approximately , it is the most populous U.S. state and the 3rd largest by area. It is also the ...
, many growers used a rootstock called AxR1. Even though it had already failed in many parts of the world by the early twentieth century, it was thought to be resistant by growers in California. Although phylloxera initially did not feed heavily on AxR1 roots, within twenty years, mutation and selective pressures within the phylloxera population began to overcome this rootstock, resulting in the eventual failure of most vineyards planted on AxR1. The replanting of afflicted vineyards continues today. Many have suggested that this failure was predictable, as one parent of AxR1 is in fact a susceptible ''V. vinifera'' cultivar. But the transmission of phylloxera tolerance is more complex, as is demonstrated by the continued success of 41B, an
F1 hybrid An F1 hybrid (also known as filial 1 hybrid) is the first filial generation of offspring of distinctly different parental types. F1 hybrids are used in genetics, and in selective breeding, where the term F1 crossbreed may be used. The term is somet ...
of '' Vitis berlandieri'' and ''
Vitis vinifera ''Vitis vinifera'', the common grape vine, is a species of flowering plant, native to the Mediterranean Basin, Mediterranean region, Central Europe, and southwestern Asia, from Morocco and Portugal north to southern Germany and east to northern ...
''. Modern phylloxera infestation also occurs when wineries are in need of fruit immediately, and choose to plant ungrafted vines rather than wait for grafted vines to be available. The use of resistant American rootstock to guard against phylloxera also brought about a debate that remains unsettled to this day: whether self-rooted vines produce better wine than those that are grafted. Of course, the argument is essentially irrelevant wherever phylloxera exists. Had American rootstock not been available and used, there would be no ''V. vinifera'' wine industry in Europe or most places other than Chile, Washington State, and most of Australia.
Cyprus Cyprus ; tr, Kıbrıs (), officially the Republic of Cyprus,, , lit: Republic of Cyprus is an island country located south of the Anatolian Peninsula in the eastern Mediterranean Sea. Its continental position is disputed; while it is ...
was spared by the phylloxera plague, and thus its wine stock has not been grafted for phylloxera resistant purposes.


Aftermath

The only European grapes that are natively resistant to phylloxera are the Assyrtiko grape which grows on the volcanic island of
Santorini Santorini ( el, Σαντορίνη, ), officially Thira (Greek: Θήρα ) and classical Greek Thera ( English pronunciation ), is an island in the southern Aegean Sea, about 200 km (120 mi) southeast from the Greek mainland. It is th ...
, Greece, although it is not clear whether the resistance is due to the rootstock itself or the volcanic ash on which it grows; and the Juan Garcia grape variety, autochthonous to the medieval village of Fermoselle in
Spain , image_flag = Bandera de España.svg , image_coat = Escudo de España (mazonado).svg , national_motto = '' Plus ultra'' ( Latin)(English: "Further Beyond") , national_anthem = (English: "Royal March") , ...
. The Juan Garcia variety remained—untouched by phylloxera—sheltered on the vineyards planted on the man-made land terraces along the mountainous skirts on the gigantic and steep Duero Arribes / Douro River Canyon, where the microclimatic conditions discourage the growth of phylloxera. To escape the threat of phylloxera, wines have been produced since 1979 on the sandy beaches of Provence’s
Bouches-du-Rhône Bouches-du-Rhône ( , , ; oc, Bocas de Ròse ; "Mouths of the Rhône") is a department in Southern France. It borders Vaucluse to the north, Gard to the west and Var to the east. The Mediterranean Sea lies to the south. Its prefecture and l ...
, which extends from the coastline of the Gard region to the waterfront village of
Saintes Maries de la Mer Saintes-Maries-de-la-Mer (, lit.: "Saint Marys of the Sea"; Provençal Occitan: ''Li Santi Mario de la Mar'') is the capital of the Camargue (Provençal Occitan ''Camarga'') in the south of France. It is a commune in the Bouches-du-Rhône ...
. The sand, sun and wind in this area has been a major deterrent to phylloxera. The wine produced here is called "Vins des Sables" or "wines of the sands". In the same department, where the canal irrigation system built by the Romans still partly persists to this day, winter flooding is also practiced where possible, for instance south of the city of
Tarascon Tarascon (; ), sometimes referred to as Tarascon-sur-Rhône, is a commune situated at the extreme west of the Bouches-du-Rhône department of France in the Provence-Alpes-Côte d'Azur region. Inhabitants are referred to as Tarasconnais or Tara ...
. Flooding the vineyards for 50 days kills all the nymphs that overwinter in the roots or the bark at the bottom of the plant. Some regions were so blighted by phylloxera that they never recovered, and instead the producers switched crops entirely. The island of
Mallorca Mallorca, or Majorca, is the largest island in the Balearic Islands, which are part of Spain and located in the Mediterranean. The capital of the island, Palma, is also the capital of the autonomous community of the Balearic Islands. The Bale ...
is one example, where almonds now substitute for vines.


Vines that survived phylloxera

According to wine critic and author Kerin O'Keefe, thanks to tiny parcels of vineyards throughout Europe which were inexplicably unscathed, some vineyards still exist as they were before the phylloxera devastation. So far, most Chilean wine has remained phylloxera free. It is isolated from the rest of the world by the
Atacama Desert The Atacama Desert ( es, Desierto de Atacama) is a desert plateau in South America covering a 1,600 km (990 mi) strip of land on the Pacific coast, west of the Andes Mountains. The Atacama Desert is the driest nonpolar desert in the ...
to the north, the Pacific Ocean to the west, and the Andes Mountains to the east. Phylloxera has also never been found in several wine-growing regions of Australia, including Tasmania, Western Australia and South Australia. Australia has strong internal biosecurity controls to minimise the risk of phylloxera spreading beyond 'Phylloxera Infested Zones' in parts of Victoria and New South Wales. The
Riesling Riesling (, ; ) is a white grape variety that originated in the Rhine region. Riesling is an aromatic grape variety displaying flowery, almost perfumed, aromas as well as high acidity. It is used to make dry, semi-sweet, sweet, and sparkling ...
of the Mosel region has also remained untouched by phylloxera; the parasite is unable to survive in the slate soil. Until 2005, three tiny parcels of ungrafted
Pinot noir Pinot Noir () is a red-wine grape variety of the species ''Vitis vinifera''. The name may also refer to wines created predominantly from pinot noir grapes. The name is derived from the French language, French words for ''pine'' and ''black.' ...
that escaped phylloxera were used to produce Bollinger Vieilles Vignes Françaises, one of the rarest and most expensive Champagnes available. In 2004, one of the parcels, Croix Rouge in Bouzy, finally succumbed to phylloxera and was replanted with grafted rootstock. A rare vintage
port A port is a maritime facility comprising one or more wharves or loading areas, where ships load and discharge cargo and passengers. Although usually situated on a sea coast or estuary, ports can also be found far inland, such as ...
is made from ungrafted vines grown on a small parcel, called Nacional, in the heart of the Quinta do Noval estate. No explanation has been found as to why this plot survived while others succumbed. Another vineyard unaffected by the phylloxera is the Lisini estate in Montalcino in Italy, a half-hectare vineyard of Sangiovese with vines dating back to the mid-1800s. Since 1985, the winery has produced a few bottles of Prefillossero (Italian for "before the phylloxera"). The wine has a following, including Italian wine critic Luigi Veronelli who inscribed on a bottle of the 1987 at the winery that drinking Prefillossero was like listening to ‘the earth singing to the sky’. Jumilla in southeastern Spain is an important area of ungrafted vineyards, mainly from Monastrell grapes. Those vineyards, however, are not immune to the insect, which is slowly advancing and destroying the Pie Franco vineyard of the Casa Castillo estate, planted in 1942, i.e., when phylloxera had already been in the region for five decades. Large swaths of vineyards on the slopes of Sicily's volcano
Mount Etna Mount Etna, or simply Etna ( it, Etna or ; scn, Muncibbeḍḍu or ; la, Aetna; grc, Αἴτνα and ), is an active stratovolcano on the east coast of Sicily, Italy, in the Metropolitan City of Catania, between the cities of Messina a ...
also remain free of phylloxera. Some vines are more than one-hundred-fifty years old, predating the phylloxera infestation in
Sicily (man) it, Siciliana (woman) , population_note = , population_blank1_title = , population_blank1 = , demographics_type1 = Ethnicity , demographics1_footnotes = , demographi ...
(1879–1880). Part of the reason for this is the high concentration of silica sand and very low (less than 3%) concentration of clay in the
volcanic soils The soil composition of vineyards is one of the most important viticultural considerations when planting grape vines. The soil supports the root structure of the vine and influences the drainage levels and amount of minerals and nutrients that ...
. In this environment (> 400m AMSL), the surface water from heavy bouts of rain seals the soil so perfectly that it imprisons the insects, effectively drowning them before they are able to thrive.Campbell, Christy. "Phylloxera: How Wine Was Saved For the World." Harper Perennial, 2004, p. 129-130
Bien Nacido Vineyard Bien Nacido Vineyards is cool-climate vineyard on the central coast of California. Located midway up the Santa Maria Valley, it is known for growing Burgundian and Rhone varieties of wine grapes. Bien Nacido has the distinction of being one of th ...
in Santa Maria Valley AVA of Santa Barbara, CA is a phylloxera-free vineyard. Despite being planted on its own roots, with UC Davis virus-free clones, the vineyard has never been affected by phylloxera. The high percentage of sand in the soil creates a mostly uninhabitable substrate for phylloxera. While Bien Nacido has not been affected, there is a potential, as all of the vines are true ''Vitis vinifera'' without scions or grafting. Many of the old vines were planted in 1973 and fall within the blocks G, N, Q and W. The wines of Bien Nacido Estate have a high percentage of these ungrafted and phylloxera-free vines within the cuvée. Colares vineyards, native to the Portuguese region of
Sintra Sintra (, ) is a town and municipality in the Greater Lisbon region of Portugal, located on the Portuguese Riviera. The population of the municipality in 2011 was 377,835, in an area of . Sintra is one of the most urbanized and densely populat ...
are grown on 3-4 metres of sand, and are therefore unaffected by Phylloxera.


References


Further reading

* Boubals, Denis, "Sur les attaques de Phylloxera des racines dans le monde", Progres Agricole et Viticole, Montpellier, 110:416-421, 1993. * Campbell, Christy, "The Botanist and the Vintner: How Wine Was Saved for the World", Algonquin Books, 2005. * Ordish, George, "The Great Wine Blight", Pan Macmillan, 1987. * Powell, Kevin, "Grape phylloxera: An Overview". In Root feeders An Ecosystem perspective (Eds S.N. Johnson & P.J. Murray) CAB International 2008. * Benheim, Devin et al., "Grape phylloxera (Daktulosphaira vitifoliae) – a review of potential detection and alternative management options", Annals of Applied Biology, Volume 161, Issue 2, pages 91–115, September 2012


External links

* *
Web page of the Phylloxera and Grape Industry Board of South Australia

The Vine's Enemy
A profile of phylloxera drawn from the 2nd edition of ''The Oxford Companion to Wine'' {{Taxonbar, from=Q367315 Phylloxeridae Grape pest insects Insects in culture