Nicol, Stirling, Rose, May and Van Heeswijck Nematodes in viticulture 109 Impact of nematodes on grapevine growth and productivity: current knowledge and future directions, with special reference to Australian viticulture J.M. NICOL1,2, G.R. STIRLING3, B.J. ROSE4,P.MAY1 and R. VAN HEESWIJCK1,5 1 Department of Horticulture,Viticulture and Oenology, University of Adelaide, Glen Osmond, SA 5064, Australia 2 Present address: CIMMYT International, 06600 Mexico, D.F. Mexico 3 Biological Crop Protection, Moggill, Qld 4070,Australia 4 Performance Viticulture, St Andrews, Vic. 3761,Australia 5 Corresponding author: Dr Robyn van Heeswijck , facsimile +61 8 83037116, e-mail [email protected] Abstract Grapevines, like most other crops and especially horticultural crops, suffer from attacks by plant- pathogenic nematodes. The types of nematodes found in vineyards and their distribution in Australia and other regions of the world are described, together with an assessment of their impact on vineyard productivity. Relationships between nematode population density and potential damage to grapevines is tabulated, based on published data. Information on reducing nematode impact by means of rootstocks is summarised and also tabulated. Control by other means is discussed, including soil fumigants and nematicides, biological control agents and plants with nematicidal properties. Special attention is paid to improving nematode resistance in rootstocks or even own-rooted Vitis vinifera cultivars by conventional breeding and by genetic engineering. Areas for future research are identified, and we provide conceptual tools plus information for long term control of nematodes in vineyards. Keywords: nematodes, grapevine, Australian viticulture, rootstocks, resistance, plant breeding 1 Introduction reproduction, which can be both heterosexual and Grape production in Australia, in contrast to most other parthenogenetic. viticultural regions, is predominantly based on own-root- In this review we describe which nematodes are most ed Vitis vinifera, a species of grapevine highly susceptible likely to cause damage to grapevines in Australia. We to two soil-borne pests, the aphid-like insect phylloxera also present current information on control measures (Daktulosphaira vitifoliae) and microscopic roundworms, that might be used to reduce the damage they cause, and nematodes. Only about 2% of the total vineyard area of make suggestions for future research. Australia is infested with phylloxera and strict quarantine regulations control the export of all living grapevine material from infested areas. By contrast, plant-patho- 2 Nematodes found in vineyards genic nematodes are found in all viticultural regions. World-wide, 162 species of plant-parasitic nematodes, However, much less attention is given to nematodes, and belonging to 35 genera, have been found on grapevines fewer legal requirements exist to control the movement (Lamberti 1988). However, not all of these species have of nematode-infested material from one vineyard to been recognised as causing economically significant dam- another. Due to their widespread distribution, nematodes age. Those nematodes which are thought to be most present a serious challenge to productivity in Australian important in vineyards are described below. viticulture. At least 2000 species of plant-parasitic nematodes 2.1 ROOT-KNOT NEMATODES (MELOIDOGYNE SPP.) have been described and they are characterised by a stylet Meloidogyne spp. are sedentary endoparasites whose bio- which is used for penetration of root tissue and sub- logy and life cycle have been described in detail in many sequent feeding. Some species are endoparasitic, entering standard texts such as Eisenback and Triantaphyllou host root tissue and feeding within it, others are ectopar- (1991) and Brown et al. (1993). These nematodes hatch asitic, living outside the plant and feeding on cells near from their eggs as second-stage juveniles and migrate the root surface. Nematode biology is thus diverse, not through soil to find a host plant root. After entering a only with respect to feeding but also with respect to root they establish a feeding site by inducing the forma- 110 Nematodes in viticulture Australian Journal of Grape and Wine Research 5, 109–127, 1999 tion of ‘giant’ cells. The infested root cortex swells to form 2.2 DAGGER NEMATODES (XIPHINEMA SPP.) a characteristic gall. A further three moults occur within Detailed information on the life cycle and biology of the root as the second stage juvenile develops into an dagger nematodes can be found in Siddiqi (1974a). adult. These moults are superimposed so that no feeding Dagger nematodes are widely dispersed in vineyard soils or growth takes place until their completion (Bird 1978). but congregate at vine root tips where they feed ecto- Many of the adults are female, but some develop into parasitically. Their feeding retards root extension, causing males which then discontinue their feeding, leave the swelling and gall formation. Cells within gall tissue are roots and move freely within the soil. In grapevine roots, enlarged and sometimes multinucleate (Cohn 1975, one gall may contain one or several females, each of Boubals and Pistre 1978, Raski and Krusberg 1984, which may lay up to 1500 eggs in a gelatinous matrix on Brown et al. 1993). Radewald (1962) found that in the root surface. Each life cycle takes just over a month California the life cycle of X. index takes 22–27 d at 24°C. under optimal conditions (Bird 1978) and several gener- However, studies in Israel have indicated that a much ations may be produced per season (McKenry 1992, longer period (up to nine months at 20–23°C) may be Brown et al. 1993). Thus, with adequate food and no required (Cohn and Mordechai 1969). competition or predators, a single juvenile (assuming an At least 28 species of this genus have been reported to egg mass of 500) can give rise to more than 125 million occur on grapevines. The species of greatest importance is progeny in a season lasting 3–4 months. X. index which is the vector of the destructive Grapevine Root-knot nematodes have a broad host range, and Fanleaf Virus (GFLV). Xiphinema index can also cause are known to parasitise almost every cultivated crop as direct injury to the roots and in this respect populations well as those of many other plant species, among them derived from Italy, California, Israel and France have those classified as weeds. More than 50 Meloidogyne been shown to differ in their virulence on grapevines species have been described and are known to differ in (Coiro et al. 1990). Xiphinema species other than X. index their pathogenicity on different host plants. At least four can be vectors for transmission of nepoviruses such as species, M. incognita, M. javanica, M. hapla and M. arenaria tobacco and tomato ringspot, and arabis mosaic virus are considered to be important pests of grapevines. Two (Krake et al. 1999 p. 43). Xiphinema americanum, one of other species have also been found on grapevines in the more common species, affects grapevine growth and Australia, namely M. thamesi (McLeod and Khair 1973) yields in California (Ferris and McKenry 1975). and M. hispanica (Hugall et al. 1994), but their impor- tance is unknown. M. incognita is considered the most 2.3 CITRUS NEMATODE (TYLENCHULUS SEMIPENETRANS) virulent on grapevines under South Australian (Stirling Tylenchulus semipenetrans has a sedentary, semi-endopara- and Cirami 1984, Walker 1997a) and South African sitic life cycle (Dalmasso et al. 1972). This nematode conditions (Loubser 1988). However due to the limited hatches from eggs as second-stage juveniles, and then number of studies and the difficulties in identifying feeds ectoparasitically on root epidermal cells. After a Meloidogyne species (see below), this needs to be con- further moult, the nematodes bury their head within the firmed. Within the Meloidogyne species, differences in root tissue, leaving their body outside, and develop into virulence between populations have been identified. For females. Eggs are laid in a gelatinous matrix on the root example, nine populations of M.hapla in France were surface, and subsequently become dispersed within the found to vary considerably in their virulence when tested soil. Their life cycle is completed within 2–3 months. against six rootstocks (Dalmasso and Cuani 1976). Optimum temperature for development and reproduc- Variation in the virulence of populations of M. incognita tion is 25°C (reviewed by Siddiqi 1974b). Males develop and M. arenaria has also been reported (Lider 1954, from eggs to maturity within 7 d without feeding, appar- McKenry 1992, Cain et al. 1984, McKenry and Kretsch ently causing no damage to the plant host (Brown et al. 1995, Walker 1997b). 1993). Root-knot nematodes have been traditionally identi- The host range of T. semipenetrans is restricted to only a fied using perineal patterns, but because a certain amount few plant genera: various grapevine and citrus species, of variability occurs within all Meloidogyne populations, lilac, persimmon, loquat, olive and pear, according to such identification may not be reliable. Other methods, reports summarised by Siddiqi (1974b). such as the differential host range test (Hartman and Races and pathotypes of T. semipenetrans have been Sasser 1985) can be used to confirm a tentative diagnosis detected which differ in their host specificity. Some but recent results indicate that they too are imperfect and populations collected from citrus or olive fail to infect can lead to mis-identification (Stanton and O’Donnell grapevines (Gottlieb et al. 1986, Scotto La Massese, 1998). The most accurate method of identification is quoted by Brown et al. 1993). In California, at least based on true genetic groupings as determined by DNA- five different races have been identified on grapevines based tests such as mitochondrial DNA patterns (Stanton (McKenry 1992). et al. 1997) or ribosomal DNA sequences (Zijlstra et al. 1997). Use of these methods will enable a more definitive 2.4 ROOT-LESION NEMATODES (PRATYLENCHUS SPP.) identification of and differentiation between Meloidogyne A detailed description of the life cycle and biology of species.