Grapevine phylloxera Phylloxera vastatrix (Planchon) Hemiptera: Phylloxeridae

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1 Islamic Republic Of Iran Ministry of Jihad-e-Agriculture Plant Protection Organization A Guide for Diagnosis & Detection Of Quarantine Pests Grapevine phylloxera Phylloxera vastatrix (Planchon) Hemiptera: Phylloxeridae Edited by: Ahmad cheraghian Bureau of Plant Pest Surveillance and Pest Risk Analysis 2016

2 Phylloxera vastatrix (Planchon) Hemiptera: Phylloxeridae Common name: grapevine phylloxera, grape phylloxera, vine louse, grape leaf louse Synonyms: Viteus vitifoliae (Fitch), Daktylosphaera vitifoliae Fitch Phylloxera vitifoliae (Fitch), Dactylosphaera vastatrix (Planchon), Peritymbia vastatrix Fitch, Peritymbia vitifoliae (Planchon) Phylloxera pervastatrix B rner, Phylloxera vitifolii (Fitch) Viteus vastatrix (Planchon), Dactylosphaera vitifoliae (Shimer) Daktulosphaira vitifoliae Fitch, Pemphigus vitifoliae Fitch Peritymbia vitisana Westwood, Rhizaphis vastatrix (Planchon) Economic impact: V. vitifoliae is the most destructive pest of grapevines known in Europe and the western USA and has become an important pest of wine grapes in Pennsylvania. Within 25 years of its introduction into France from America (in about 1860) it had destroyed nearly one-third of the vineyards in the country - more than 100,000 ha - with incalculable economic and social consequences. This was because the European grapevine cultivars then grown were highly susceptible. The solution found was to replant with European cultivars grafted onto American rootstocks, a practice which is now almost universal wherever V. vitifoliae occurs. The pest still represents a serious threat to the few regions where susceptible grape cultivars are still cultivated on their own roots (rather than on resistant rootstocks). It is also more damaging in recently planted vineyards, and damage is less significant on vigorous vines over 10 years old. Leaf infestation is reported to have no economic effect on wine grapes, or on the quality and quantity of wine made from them (Strapazzon and Girolami, 1985b; Strapazzon et al., 1986). In California in the early 1980s, large populations of V. vitifoliae were detected in grapevines grafted on 'AxR#1' (a hybrid between V. vinifera and V. rupestris). The existence of a different biotype (biotype B), having a greater parasitic ability on this rootstock, was demonstrated (Granett et al., 1985). These susceptible vineyards had to be uprooted, fumigated and replanted at a cost of over US$500 million (Chiarappa and Buddenhagen, 1994). In general, rootstocks with no vinifera parentage have retained their resistance remarkably, for over 120 years (Grannet et al., 2001a). Problems are more likely on rootstocks like AXR#1, with vinifera, parentage, which are now best avoided. For more information, see Balachowsky and Mesnil (1935), Dominguez Garcia- Tejero (1957) and Rilling (1964). Environmental impact V. vitifoliae is only a pest of viticulture, attacking species, especially Vitis vinifera, which have been widely planted outside their native range. Although it had the immediate effect of destroying vineyards, the areas concerned have in general been replanted with grapevines on resistant rootstocks, so there has been llittle long-term effect on land use. Social impact V. vitifoliae had catastrophic social effects when it was first introduced into Europe. Numerous small vine growers lost their livelihood altogether, and flocked to the cities to join an increasing pool of unemployed labourers. Local politics were radicalized, strengthening socialist and communist support in the agricultural population.

3 Hosts: Major hosts:) Vitis vinifera (grapevine). Minor hosts):vitis (grape), Vitis aestivalis (Summer grape), Vitis labrusca (fox grape), Vitis riparia (riverbank grape (USA). Geographic distribution: Europe: Austria,Bosnia and Herzegovina, Bulgaria, Croatia, Cyprus, Czechoslovakia, France, Germany, Greece, Hungary, Italy, Luxembourg,, Macedonia, Malta, Moldova, Poland, Portugal, Romania, Russian Federation, Serbia and Montenegro, Slovakia,Slovenia, Spain, Switzerland, Ukraine, United Kingdom. Asia: Armenia, Azerbaijan, China, India, Indonesia, Israel, Japan, Jordan, Korea, DPR, Korea, Republic of, Lebanon, Syria, Turkey. Africa: Algeria, Morocco, South Africa, Tunisia, Zimbabwe Central America & Caribbean: Bermuda, Panama North America: Canada, Mexico, USA South America: Argentina, Bolivia, Brazil, Colombia, Peru, Uruguay, Venezuela. Oceania: Australia, New Zealand World distribution map of Phylloxera vastatrix (Planchon) Morphology: Gallicolae form Adult Globular aphid, mm long and mm wide; cephalothorax widened and its dorsal face rounded off; abdomen tapers off and is slightly frayed posteriorly; antennae composed of three segments, the third one being the most developed and provided with a large primary latero-external sensorium; the processus terminalis is short and broad, little differentiated at its base, having a length which is one-third in excess of that of the third segment (dimension taken from the base of the sensorium to the tip of the antenna, excluding the apiales); dorsal cuticle is rough, but entirely free from tubercles. The rostrum reaches the femora of the foremost legs. Radicicolae form Eggs The eggs measure x µm. Larva The four larval stages have the same general external morphology as the adult. In the later stages, the width of the body increases more rapidly than the length, and the body thus becomes rounder in outline. Similarly, the size of the legs and antennae does not increase at the same rate as that of the body; they therefore appear smaller in the later stages. From the second stage onwards, the tubercles on the dorsal surface become more obvious.

4 Adult General appearance similar to gallicolae form, but smaller, being about 1 mm in length. It is distinguished from gallicolae by the presence of tubercles on the dorsal surface - 12 on the head, 28 on the thorax and 30 on the abdomen. On the antenna, the processus terminalis is well differentiated and much finer than that of the gallicolae form.

5 Type Radicicola a. Healthy root. b. Root on which the lice are working, showing1 the knots and swellings caused by their punctures. c.root deserted by them, on which the rootlets have begun to decay, d d d. Lice on the larger roots, natural size. e. Female pupa, dorsal view. f. Winged female, dorsal view, greatly enlarged. Type Gallicola a. Egg. b.section of gall c.swelling of tendril., a, b. Newly hatched larva, ventral and dorsal. view. Natural sizes in circles at sides

6 Biology and ecology: The full life-cycle of V. vitifoliae on American grapevines is a complex alternation between an aerial, leaf-feeding form and the root-feeding form (gallicolae and radicicolae, respectively). However, V. vitifoliae can also persist parthenogenetically as the root-feeding form, without the leaf-feeding stage of the cycle. The occurrence or non-occurrence of the gallicolae form depends on several factors, including vine species, cultivar and environment (Stevenson and Jubb, 1976). On American grapevine species, V. vitifoliae lives on the roots and leaves, and exhibits a full cycle of development with the presence of all forms of the aphid. This full life-cycle involves migration from the roots to the leaves and back to the roots, and also an alternation of parthenogenetic and sexual reproduction. On cultivars of the European grapevine (V. vinifera) grafted onto American rootstocks, the aphid normally infests only the underground parts of the plant and undergoes an incomplete cycle of seasonal development, with no change of feeding site. European grapevines grown on their own roots are so susceptible that plants are killed by radicicolae (except in very particular conditions, for example, in isolated places in France where vineyards are naturally flooded in winter). The winter is passed as eggs attached to the grapevine stems (American grapevines) and in the form of first- and second-instar nymphs on the nodules or galls on vine roots (European grapevines). The survival of eggs on stems is dependent on temperature: optimal temperatures for survival are between 21 and 36 C (Granett and Timper, 1987). In the full life-cycle, eggs on the stems hatch in spring, after the foliage has appeared, and the yellow gallicolae aphids developing from these eggs migrate to the leaves, where they begin feeding, so causing the formation of galls. As soon as the aphids mature, they lay eggs inside each gall. Four to six generations of the gallicolae are usually produced. Individuals of the final generation of these leafinhabiting aphids drop to the ground and burrow beneath the soil to the roots, as deep as 1.2 m, where they can live for a number of parthenogenetic generations. Towards autumn, winged, sexuparous forms are produced on the grapevine roots; they leave the ground and fly to grapevine leaves. After 24 h, two kinds of eggs are laid; larger ones give rise to females and smaller ones to males. This sexual generation mates, producing the winter eggs, thus completing the life-cycle. Even very severe winter conditions do not kill the eggs. On European cultivars of V. vinifera grafted onto American rootstocks, radicicolae become active, feeding on the roots, as soon as growth starts in the spring. They continue to multiply parthenogenetically through the summer. Sexuparous forms appear, but the gallicolous aphids do not normally develop on the leaves, and the aerial life-cycle is therefore not completed. Corrie et al. (2002) confirm that, in an equivalent situation in Australia, "the majority of vineyards are infested by functionally parthenogenetic lineages". Occasionally, galls do appear on V.vinifera leaves, according to cultivar, local conditions, possibly migration from naturalized American vine rootstocks. Insecticides can be used to control them (Yvon and Leclant, 2001). V. vitifoliae can survive under virtually all climatic conditions tolerated by its host plant. It appears not to be influenced by temperature, rainfall or humidity within that range (de Klerk, 1974). In South Africa it has been shown to be influenced by soil type, with infestations decreasing as the percentage of fine and medium sand content of a soil increases.

7 V. vitifoliae does not occur in soils with a medium to fine sand content of more than 65% (de Klerk, 1974). Development from egg to adult female takes about 22 days and the annual active reproductive period is 7.5 months. Recently, Downie and Granett (1998) described another life-cycle variant in southwestern USA, in which sexuparous forms appear directly on the leaf galls, and the root phase is absent. In conclusion, it may be said that the survival of V. vitifoliae on a particular scion/rootstock combination, and the severity of symptoms on roots and leaves, depends on a complex interaction of the tolerance or resistance of the roots or leaves to the radicicolous or gallicolous forms, which varies further according to the strain of the pest and the variant of the life-cycle which it follows. These interactions are currently the subject of much research, stimulated by the apparent resurgence of V. vitifoliae as a pest in the 1990s (see, for example, Omer et al., 1999; Forneck et al., 2001; Granett et al. 2001a,b). For more information, see Dominguez Garcia-Tejero (1957), Maillet (1957), Rilling (1964), Daris (1970), Bovey (1972), Gorkavenko (1975) and Gorkavenko and Gorkavenko (1977).

8 Symptoms: V. vitifoliae damage can appear initially as a few dead or declining contiguous vines in a vineyard. Gallicolae form Small galls, about the size of half a pea, develop on the leaf surface, sometimes so numerous as to cover practically the entire leaf. The galls are open on the underside of the leaf. Although leaf galling by V. vitifoliae does not normally cause significant losses in grape production, severe infestations do cause considerable distortion and dropping of affected leaves late in the season. Radicicolae form Numerous knots or galls form on grapevine roots, with rotting of the roots, yellowing of the foliage and general decrease in vigour of the vines. Death of susceptible vines may result within 3-10 years. Symptoms by affected plant part Leaves: abnormal forms; abnormal leaf fall. Roots: galls; reduced root system; swollen roots. Whole plant: plant dead; dieback..

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11 Means of movement and dispersal: Plant parts liable to carry the pest in trade/transport - Growing Medium Accompanying Plants: Nymphs, Adults. - Leaves: Eggs, Nymphs, Adults; borne internally; visible to naked eye. - Roots: Eggs, Nymphs, Adults; borne internally; visible to naked eye. - Stems (above Ground)/Shoots/Trunks/Branches: Eggs, Nymphs, Adults; borne internally; visible to naked eye. Plant parts not known to carry the pest in trade/transport - Bark - Bulbs/Tubers/Corms/Rhizomes - Fruits (inc. Pods) - Flowers/Inflorescences/Cones/Calyx - Seedlings/Micropropagated Plants - True Seeds (inc. Grain) - Wood. Phytosanitary significance: The dispersal of V.vitifoliae into such areas must have occurred by humane to other countries, whereas the transportation of the eggs / nymphe and adult is only possible if the planting of the young trees had leaves and roots, V.vitifoliae is quarantine pests for some countries and Iran. Detection and inspection: Vines that fail to thrive and become chlorotic and unproductive should be inspected for the presence of phylloxera. Galls on leaves are an obvious indication of phylloxera on hybrid varieties, but damage confined to roots of vinifera wine grapes can be confused with damage from nematodes or root diseases. Carefully expose the roots and search for the typical swellings and dying roots. A hand lens or dissecting microscope will help verify the presence of phylloxera.

12 References: Abai, M. (1984).List of forest trees and shrubs of Iran. Plant pests and Diseases Rech. Inst.,Tehran, 147p. Barouti,S.,A.alavi,2004,Plant Nematology,Principles, Parasitic and Quarantine Nematode in Iran., p. Behdad,E.,1984.Pests of Fruit Crops in Iran,Sepehr pub,tehran,822p. Esmaile,M.1983, Pests of Fruit Crops in Iran, Sepehr pub,tehran,366p. CAB International Crop Protection Compendium Edition. CAB International. Wallingford, Oxon, UK. Modarres Awal, M.2012.List of Agricultural pests and Their Natural Enemies in Iran. Revised Edition, Ferdowsi university Prss,877p. Salavatean, Mer.1996, Plant quarantine in Iran, Research Institute,Ministey of Agriculture pub,279p /