PHYLLOXERA STEPHEN J. KREBS PHYLLOXERA BIOLOGY AND LIFE CYCLE The grape phylloxera, Daktulosphaira vitifoliae (Fitch), (Hemiptera: Homoptera: Phylloxeridae), is an aphid-like insect that attacks the roots and the leaves of plants in the genus Vitis. It was first described in 1854 from vines in New York State by Asa Fitch, who named the insect Pemphigus vitifolii. It was then reclassified into the genus Phylloxera (Mayet, 1894) but because the grape phylloxera differs morphologically from other phylloxera species it was re-assigned to its own genus. Outside the United States, Viteus is an accepted synonym for the older term Daktulosphaira. Numerous other names appear in the literature (Russell, 1974). The basic biology of phylloxera was established in the 1870s by C. V. Riley, State Entomologist in Missouri (Riley, 1871, 1872, 1873, 1874, 1876). He found that in its native North American range and in other summer-humid climate areas, phylloxera has a complex life cycle, feeding on both the root system and the aerial portion of the vine (Figure 1). The root feeding forms are all oviparous parthenogenic females. Some of the eggs these females produce are pre-destined to become winged adults. In their fourth instar the alates emerge from the soil and molt to the winged type. In this form they are highly mobile (Riley, 1876). The winged adult, which does not feed, lays eggs that hatch into male and female insects. These males and females, which also do not feed, molt four times, mate and produce the so-called winter egg. Only fundatrix females hatch from the winter eggs, their feeding inducing galls to form on the vine leaves. They develop and lay eggs which will produce females. The offspring of the fundatrix females eventually exit from the galls to form new galls. Some may return to the soil to live on the roots. Infestations are spread by both the movement of the winged form above ground in regions where they are fertile, and by the crawler form, a first instar female that can move short distances above or below ground (Riley, 1874) or, when they are above ground, short or long distances in wind (Granett, personal communication, 1995). Riley confirmed that the insect damaging vines in France and California was the same phylloxera native to the eastern United States (Riley, 1872; Appleton, 1880; Ordish, 1987). He also confirmed that American Vitis species were resistant to phylloxera and were seldom killed by the insect (Riley, 1880). In California and other dry-summer climates, the phylloxera life cycle is truncated. The insect is found on the roots as an oviparous parthenogenic female. The development of the winged form is often observed under these growing conditions, but it is not known to be fertile and therefore no sexual forms or winter egg is produced and there is no leaf-galling. The lack of the sexual cycle is thought to limit the genetic diversity of the phylloxera population (Davidson and Nougaret, 1921). 2 S- PHYLLOXERA Daktulosphaira vitifoliae (Fitch) WINTER EGG SEXUAL FORMS 2/ TO LEAVES LEAF WINGED GALLIN FORM C WLER DISPERSAL TO OTHE DI SPERSAL TO OTHER LEAVES AND TO ROOTS NYMPH 41 WITH FORMING ROOT WINGPADS SWELLING CYCLE CRAWLER D SPERSAL TO OTHER ROOTS Phylloxera is the most serious insect pest of the grapevine. The active root stage of the insect is known as the radicole and its feeding results in the formation of nodosity and tuberosity root swellings. Several parthenogenic female radicole generations are produced during the active growth of the vine. Crawlers of the radicole form migrate above and below ground to the roots of other vines. The overwintering root form is called a hibernant and does not feed. The emerging nymph with forming wingpads becomes the winged migratory adult female, called an elate. The sexual forms develop from eggs laid by the alate. Mating of the sexual forms produces the winter egg, which hatches into the fundatrix female. The fundatrix migrates to new leaves in the spring and feeds on the leaf tissue, causing leaf galls to form. The egg of the fundatrix hatches into the gallicole female, which forms additional galls and several more parthenogenic generations are produced during the active growth of the vine. The gallicole may migrate to other leaves, or to roots where a new radicole cycle is initiated. (Illustration © 1994 by R. Krebs James. Text ° 1994 by S. Krebs.) 3 Phylloxera may damage grapevine roots by feeding on either new root tips or on older root tissue. Feeding on new root tips causes a small gall called a nodosity to develop at the feeding site. Feeding on older roots causes the formation of an abnormal roughened swelling called a tuberosity. The formation of tuberosities is more serious because it leads to the decomposition and death of the damaged root (Millardet, 1892). Phylloxera damage to the roots of the grapevine results in a general weakening and the eventual death of susceptible plants. Vegetative symptoms include reduced cane growth, short internode length, an absence of actively growing shoot tips in the spring and premature leaf fall. Crop yield is reduced because the berries are small and few clusters are produced. The symptoms become increasingly severe over several seasons. In the field, a circular pattern of decline radiating from the point of first infestation may occur (Riley, 1874; Bioletti, 1901; Davidson and Nougaret, 1921; Husmann, 1910). In North America phylloxera coevolved with the indigenous Vitis species. The resistance developed by some American Vitis species limits the root damage caused by the insect. Different levels of resistance to both leaf and root damage are found among the Vitis species (Riley, 1874; Millardet, 1892; Viala and Ravaz, 1903; Boubals, 1966). Vitis vinifera has susceptible roots but is resistant to leaf galling (Wapshere and Helm, 1987). It is the species from which most commercial grape cultivars have been selected. Accidental importation of phylloxera led to the catastrophic destruction of V. vinifera vineyards throughout Europe, California and most other world viticultural regions in the late nineteenth century (Stevenson, 1985; Ordish, 1987). It is the most important insect enemy of the grapevine worldwide. PHYLLOXERA INTRODUCTION INTO EUROPE AND ELSEWHERE The introduction of phylloxera into Europe probably occurred on American vines used in grafting and hybridizing experiments for the control of powdery mildew (oidium), Uncinula necator, which had been accidentally brought into Europe in the mid-1800s from North America (Hewitt, 1988). The knowledge gained from this work was later applied to the control of phylloxera (Ordish, 1987). Phylloxera was found on the roots of grapevines in southern France in 1868 (Planchon, et al., 1868). Based on vine decline symptoms that had been previously noted there, the actual introduction into France probably occurred in the Rhone Valley around 1862. The insect spread very rapidly and soon had devastated the viticulture industry in much of the country (Stevenson, 1980). 4 In other European countries, phylloxera was found at about the same time. In Portugal, the first discovery of the pest occurred in 1862. It had spread through the Douro region by 1872 and was found in most other districts by 1880 (Bleasdale, 1880; Morrow, 1973). In Spain, the discovery of phylloxera occurred in 1876 in the Mediterranean district of Malaga and infestation had become general in the country by 1888. In Italy, phylloxera was probably present by 1870. In Germany, the first damage occurred in 1875 (Ordish, 1987). In Great Britain, phylloxera was discovered in 1867 (Stevenson, 1985). Other European countries infested with phylloxera include Turkey, Austria, Hungary, Switzerland, Algeria, Greece, Cyprus and Yugoslavia (Branas, 1962; Daris, 1970; Ordish, 1987). In Asia, phylloxera is present in Korea and in Japan. In Central America, the insect is found in Mexico (Anonymous, 1975). Phylloxera was also introduced into viticultural regions of the Southern Hemisphere in the nineteenth century. The insect was first detected in Australia in 1875 (Adcock, 1914; Buchanan, 1987). The introduction into New Zealand occurred in 1885 (Dry and Smart, 1982a, 1982b; Smart and King, 1983). In South Africa, phylloxera was discovered in 1886 and is now widely distributed throughout the grape growing regions of that country (De Klerk, 1972). In South America, phylloxera is present in Peru, Brazil and Argentina (Anonymous, 1975). Olmo (19xx) believes it to be native to Venezuela. Phylloxera created severe economic and social displacement as wine production declined (Eichel, 1975; Stevenson, 1980; de Blij, 1983; Ordish, 1987; Unwin, 1991). Expensive insecticide applications were devised to control the insect. Carbon bisulfide was the most effective material tested, but its application was labor-intensive and the effects were short-lived. Repeated treatments were therefore required. Many other purportedly insecticidal materials were also recommended, including coal tars, manures, and various fanciful decoctions. None of these were successful in the control of the insect (Bleasdale, 1880). Quarantine methods were generally ineffective in controlling the spread of phylloxera. Growers were warned to practice careful sanitation whenever moving from one vineyard to another, because the insect is readily transported on harvesting bins, on nursery stock and in contaminated soil that becomes attached to vineyard equipment and workers' clothing. The small size of the pest makes detection difficult (Fodx, 1902; Viala and Ravaz, 1903). PHYLLOXERA INTRODUCTION INTO CALIFORNIA Phylloxera was first found on the roots of grapevines in the Sonoma Valley in 1873, at the center of the young California wine industry. It was to this location that many Vitis cultivars had been introduced before being taken to other growing regions in the state (Pinney, 1984). As early as 1860, growers had noted vines with symptoms of phylloxera injury (Appleton, 1880). University of California reports proposed an introduction date of 1858 (Davidson 2 5 and Nougaret, 1921) or 1852 (Smith and Stafford, 1955).