Daktulosphaira vitifoliae (Fitch)
{Also known as Viteus vitifoliae (Fitch)}
Taxonomic placing: Insecta, Hemimetabola, Hemiptera, Sternorrhyncha, Aphidoidea, Phylloxeridae.
Common name: Grape phylloxera.
Geographical distribution: A North American species that now occurs in the majority of grapevine-growing regions. CIE Map #339, 1975.
Host plants: Various species of Vitis
Morphology: Three forms of this pest occur in the Middle East. The body of the root-infesting apterous females (“radicoles”) is green to yellow, about 1.0 mm long and with many hair-bearing dorsal tubercles. The leaf-infesting form (“gallicoles”) has a similar color but without dorsal tubercles. The alate form (“sexupara”) is orange-yellow with a darker thorax, body length about 1.2 mm.
Life history: In the Middle East the grape phylloxera lives throughout the year on the roots of grapevines, reproducing by viviparous parthenogenesis. Completing a generation on susceptible cultivars requires 16 days at 24ºC, whereas on resistant (American) rootstocks it takes about 35 days. The threshold for development was calculated to be at 9.3ºC. Generation time could require one month, and each female produces about 50-70 eggs, depending on temperature and root size; feeding on smaller roots results in more eggs. In North America this aphid also occurs on the leaves of species of Vitis. The pest has several biotypes that differ in their level of aggressiveness, expressed in the ability to form leaf galls in certain cultivars, in the degree of root damage, and in their propensity to form sexual or winged forms.
Economic importance: The grape phylloxera is a major pest of grapevines, listed as an A2 quarantine pest for EPPO and considered one of the most destructive pests of grapes in Europe and the western USA. Infestation of European grapevines (Vitis vinifera Linnaeus) began in the 1860’s after the pest was introduced into France on American rootstocks, such as Vitis riparia Michaux and others. The legal and illegal movement of planting material then caused the pest to spread around the world, almost destroying the vine industries of France and other regions, including the Middle East. Most damage is caused by the radicole nymphs, whose sucking on grape roots induces the formation of two types of galls. Tuberosities, localized enlargements of phloem cells, occur on thin roots. Nodules (often called (nodosities), fleshy outgrowths that cause the roots to bend at the point of feeding, are induced in elderly roots. These galls disrupt the vascular system, affect nutrient and the water transportation and absorption, and are later invaded and infected by soil-borne pathogenic rot fungi, leading to further reductions in vine biomass and even death. Vine vigor and infestation size, as well as the specific phylloxera biotype, affect the rate of decline. It may take years, the plants slowly become stressed and chlorotic, or they may die rapidly. Soil type also affects pest infestations. Grapes growing in heavy soils are at greater risk because the nymphs can move through the cracks to reach new hosts. In sandy soils there are no cracks, pest spread is thus restricted limiting further infestations.
The pest also forms leaf galls, in the form of invaginations on the upper leaf surfaces of American vines. Although this galling is of minor economic importance, severe infestations may reduce photosynthetic rates and cause considerable distortion and leaf drop, leading to delayed ripening and reduced grape quality. In the Middle East local and imported resistant rootstocks are routinely used. As a result the pest seldom occurs except on American rootstocks when grown for rootstocks, or when suckers of such rootstocks are allowed to emerge.
The grape phylloxera has been a classic object of phytosanitary regulations, leading to the first international measures and agreements formulated for phytosanitary purposes in Europe. The world-wide concern about this pest is reflected in convening the International Phylloxera Symposiums, of which the most recent (the sixth) met in 2014 (http://www.ishs.org/ishs-book/1045).
Management
Monitoring: The roots of vines that fail to thrive, become chlorotic and unproductive and show stunting of lateral shoot growth are to be inspected for the typical swellings and dying roots. Young emerging aphids can be monitored by sticky traps that are placed on the ground around vine trunks.
A diagnostic assay for detecting the pest in soil samples was described in Australia. Specific primers were developed for phylloxera and their specificity confirmed using various soil types with known pest numbers. The assay was more sensitive for detecting pest nymphs than a standard method for establishing phylloxera presence on roots.
Horticultural control: Planting vines in light or sandy soils. Disinfestation of farm machinery in order to prevent aphid movement from infested to clean areas. Providing enough irrigation and nutrients to delay the rate of vine decline. Preventing stresses by aggressive cropping and efficient pest and disease control. Immersing dormant vine cuttings in hot (43 to 52°C) water baths.
Plant resistance: North American grapevines are resistant to the pest. This has led to the worldwide practice of grafting scions of European varieties (as well as various hybrids) onto American rootstocks (such as V. riparia and Vitis aestivalis Michaux). The obtained resistance is however not durable, because pest biotypes have emerged that surmount this resistance in different parts of the world, and there is concern that future climate changes could affect the resistance. Although such biotypes have not yet been reported in the Middle East, their appearance in this region may be only a matter of time. Grafting with resistant rootstocks ensures that the production of fruit is rarely affected by pest infestations and, if so, only at a limited level.
Radiation: Exposing phylloxera eggs to gamma radiation reduced their hatching, and females radiated as nymphs had fewer progeny. In addition, females reared on irradiated vine roots laid fewer eggs.
Chemical control: Applications of imidacloprid killed 85% phylloxera nymphs in a glasshouse pot experiment. Vines treated with spirotetramat, applied in the field as a foliar spray, were stronger and the size of phylloxera colonies was reduced. Fumigation of dormant vine cuttings with phosphine and carbon dioxide killed almost all pest nymphs.
Biological control: Many biological control agents (like entomopathogenic nematodes were tried within the context of IPM projects and contributed to pest reduction. A field trial with a commercial formulations of the entomopathogenic fungus Metarhizium anisopliae (Metchnikoff) Sorokin reduced pest abundance for 2 years post-application, but such control did not persist. At present there are no biological (or chemical) control agents registered against phylloxera in Europe.
References
Benheim, D., Rochfort, S., Robertson, E., Potter, I.D. and Powell, K.S. 2012. Grape phylloxera (Daktulosphaira vitifoliae) - a review of potential detection and alternative management options. Annals of Applied Biology 161: 91–115.
English-Loeb, G., Villani, M., Martinson, T., Forsline, A. and Consolie, N, 1999. Use of entomophagic nematodes for control of grape phylloxera (Homoptera: Phylloxeridae): a laboratory evaluation. Biological Control 28: 890–894.
EPPO (European and Mediterranean Plant Protection Organization). 2009. PM 10⁄16: Hot water treatment of grapevine to control Viteus vitifoliae. OEPP/EPPO Bulletin 39: 484–485.
EPPO (European and Mediterranean Plant Protection Organization). 2012. Phosphine fumigation of grapevine to control Viteus vitifoliae. OEPP/EPPO Bulletin 42: 496–497.
EFSA PLH Panel 2014. Scientific Opinion on the risk to plant health posed by Daktulosphaira vitifoliae (Fitch), in the EU territory, with the identification and evaluation of risk reduction options. EFSA Journal 12: 3678, 67 pp.
Herbert, K. (and 6 co-authors). 2008. Developing and testing a diagnostic probe for grape phylloxera applicable to soil samples. Journal of Economic Entomology 101: 1934-1943.
Herbert, K.S., Hoffmann, A. A. and Powell, K.S. 2008. Assaying the potential benefits of thiamethoxam and imidacloprid for phylloxera suppression and improvements to grapevine vigour. Crop Protection 27 1229–1236.
Kirchmair, M., Neuhauser, S., Strasser, H., Voloshchuk, N. Hoffmann, M. and Huber, L. 2009. Biological control of grape phylloxera – a historical review and future prospects. Acta Horticulturae 816: 13–18.
Kocsis, L. and Andor, R. 2014. Efficacy of pesticides on grape phylloxera populations in vitro and in situ. Acta Horticulturae 1045: 33-36.
Makee, H. 2004. Factors influencing mortality, fecundity and fertility of grape phylloxera (Daktulosphaira vitifoliae (Fitch)). Vitis 43: 49–50.
Makee, H., Charbaji, T., Idris, I. and Ayyoubi, Z. 2008. Effect of gamma irradiation on survival and reproduction of grape phylloxera Daktulosphaira vitifoliae (Fitch). Advances in Horticultural Science 22:182-186.
Omer, A.D., Granett, J., De Benedictis, J.A. and Walker, M.A. 1995. Effects of fungal root infections on the vigor of grapevines infested by root-feeding grape phylloxera. Vitis 34: 165-170.
Powell, K.S., Cooper†, P.D. and Forneck, A. 2013. The biology, physiology and host–plant interactions of grape pylloxera Daktulosphaira vitifoliae. Advances in Insect Physiology 45: 159-218.
Swirski, E. and Amitai, S. 1999. Annotated list of aphids (Aphidoidea) in Israel. Israel Journal of Entomology 33: 1-120.