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Xiphinema index
(fan-leaf virus nematode)

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Datasheet

Xiphinema index (fan-leaf virus nematode)

Summary

  • Last modified
  • 14 July 2018
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Vector of Plant Pest
  • Preferred Scientific Name
  • Xiphinema index
  • Preferred Common Name
  • fan-leaf virus nematode
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Nematoda
  •       Class: Adenophorea
  •         Order: Dorylaimida

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Pictures

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PictureTitleCaptionCopyright
X. index feeding from cortex cells deep inside of roots of host plant, a Ficus sp.
TitleNematode feeding
CaptionX. index feeding from cortex cells deep inside of roots of host plant, a Ficus sp.
Copyright©U. Zunke/Nemapix Vol. 1
X. index feeding from cortex cells deep inside of roots of host plant, a Ficus sp.
Nematode feedingX. index feeding from cortex cells deep inside of roots of host plant, a Ficus sp. ©U. Zunke/Nemapix Vol. 1

Identity

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Preferred Scientific Name

  • Xiphinema index Thorne & Allen, 1950

Preferred Common Name

  • fan-leaf virus nematode

Other Scientific Names

  • Diversiphinema index Thorne & Allen (Cohn & Sher, 1972)

International Common Names

  • English: dagger nematode
  • Spanish: vector virus en vinedos

EPPO code

  • XIPHIN (Xiphinema index)

Taxonomic Tree

Top of page
  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Nematoda
  •             Class: Adenophorea
  •                 Order: Dorylaimida
  •                     Family: Xiphinematidae
  •                         Genus: Xiphinema
  •                             Species: Xiphinema index

Notes on Taxonomy and Nomenclature

Top of page Cohn and Sher (1972) proposed the subgenus Diversiphinema under Xiphinema Cobb, 1913 and assigned X. index to it. The subdivision of Xiphinema under subgenera has not been recognized as a sound proposal.

Description

Top of page Measurements

Female: body length=2.9-3.6 mm; a=54-61; b=6.0-7.7; c=72-98; c'=0.9-1.3; V=38-42%; odontostyle=119-130 µm; odontophore=65-78 µm.

Male (rare; after Thorne and Allen, 1951): body length=3.6 mm; a=63; b=7.3; c=88; T=49.

Female: body forms an open spiral on death. Cephalic region continuous with body contour. Amphidial slits almost as long as cephalic region width. Odontostyle needle-like, averaging 126 µm long. Odontophore with three large basal flanges, average length 70 µm. Basal stylet guiding ring 100-114 (108) µm from anterior end. A short mucro resembling spear tip present about 30 µm behind odontophore. Oesophagus in two parts - anterior slender and posterior bulbar part. The dorsal oesophageal gland cell extends along the length of the basal oesophageal bulb on the dorsal side and the anterior half of the ventral side. The cell has a system of six ducts formed by deep infolds of the limiting cell membrane. Two ducts extend almost the entire length of the bulb on the dorsal side and four extend half-way on the ventral side (Robertson and Wyss, 1979). Ovaries paired, opposed, reflexed. Z-organ absent. Prerectum 320-390 µm long. Tail mammiform, about as long as anal body width, usually with a digitate ventral or terminal peg 9-13 µm long; females with pegless tail sometimes occur (Heyns, 1971).

Male: extremely rare, reported by Thorne and Allen (1951) from USA; Harris (1977) from Victoria, Australia; and Luc and Cohn (1982) from Israel; not essential for reproduction. Spicules strong, 63 µm long measured along medial line; lateral guiding pieces of spicules 12 µm long. A ventromedian series of seven supplementary papillae present.

Juveniles: four different juvenile stages recognized by the relative body length and the length of the odontostyle. The length of the replacement odontostyle of one stage corresponds to the length of the functional odontostyle of the next stage. Odontostyle length increased from 49±4.6 (38-55) µm for the first stage juveniles to 135±2.8 (128-138) µm for the female and male, with a growth rate of 61, 35, 30 and 13% compared to the previous stage for J2, J3, J4 and adults, respectively (Vovlas and Larizza, 1994).

Bleve Zacheo et al. (1976) described the ultrastructure of the female reproductive system of X. index and Xiphinema mediterraneum.

Morphology and taxonomy of X. index have been given by Thorne and Allen (1951), Heyns (1971) and Siddiqi (1974). A key to Xiphinema species occurring in the UK, including X. index, is given by Southey (1973).

Distribution

Top of page The distribution of X. index is closely related to that of its most important host, grapevine. X. index is widespread on grapevines with grapevine fanleaf nepovirus.

Distribution Table

Top of page

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

ArmeniaPresentAkopyan et al., 1987; CABI/EPPO, 2000; EPPO, 2014
AzerbaijanPresentChumakova, 1982; Treskova and Venetskaya, 1982; CABI/EPPO, 2000; EPPO, 2014
Georgia (Republic of)PresentCABI/EPPO, 2000; EPPO, 2014
IndiaPresentCABI/EPPO, 2000; EPPO, 2014
-HaryanaPresentCABI/EPPO, 2000; EPPO, 2014
-Tamil NaduPresentSivakumar et al., 2003
-Uttar PradeshPresentCABI/EPPO, 2000; EPPO, 2014
-West BengalPresentCABI/EPPO, 2000; EPPO, 2014
IranPresentMojtahedi et al., 1980; CABI/EPPO, 2000; EPPO, 2014
IraqPresentKatcho and Allow, 1968; CABI/EPPO, 2000; EPPO, 2014
IsraelPresentCohn, 1975; Luc and Cohn, 1982; CABI/EPPO, 2000; EPPO, 2014
LebanonPresentJawhar et al., 2006
PakistanPresentQasim et al., 1988; CABI/EPPO, 2000; EPPO, 2014
TajikistanPresentIvanova, 1972; Kankina, 1976; Kankina, 1977; CABI/EPPO, 2000; EPPO, 2014
TurkeyPresentTekinel et al., 1971; CABI/EPPO, 2000; EPPO, 2014
TurkmenistanPresentCABI/EPPO, 2000; EPPO, 2014
UzbekistanPresentAzizova, 1970; Azizova, 1972; CABI/EPPO, 2000; EPPO, 2014

Africa

AlgeriaPresentDalmasso and Cuany, 1969; CABI/EPPO, 2000; EPPO, 2014
South AfricaPresentHeyns, 1971; Orffer, 1977; CABI/EPPO, 2000; EPPO, 2014
Spain
-Canary IslandsPresentArias et al., 1994; CABI/EPPO, 2000; EPPO, 2014
TunisiaPresentCABI/EPPO, 2000; EPPO, 2014

North America

USARestricted distributionCABI/EPPO, 2000; EPPO, 2014
-CaliforniaPresentRaski et al., 1971; Raski and Schmitt, 1972; CABI/EPPO, 2000; EPPO, 2014

South America

ArgentinaPresentLa Red & Vega, 1968; Vega, 1978; CABI/EPPO, 2000; EPPO, 2014
BrazilPresentAndrade et al., 1993; CABI/EPPO, 2000; EPPO, 2014
-CearaPresentCABI/EPPO, 2000; EPPO, 2014
ChilePresentGonzález, 1970; Auger et al., 1992; CABI/EPPO, 2000; EPPO, 2014
PeruPresentLamberti et al., 1987; Alkemade and Loof, 1990; CABI/EPPO, 2000; EPPO, 2014

Europe

AlbaniaPresentMerkuri et al., 1994; CABI/EPPO, 2000; EPPO, 2014
AustriaPresentCABI/EPPO, 2000; EPPO, 2014
BulgariaPresentStoyanov, 1974; CABI/EPPO, 2000; EPPO, 2014
CroatiaPresentCABI/EPPO, 2000; EPPO, 2014
CyprusRestricted distributionCABI/EPPO, 2000; EPPO, 2014
Czech RepublicPresentCABI/EPPO, 2000; EPPO, 2014
FrancePresentDalmasso, 1969; Dalmasso et al., 1972; Esmenjaud et al., 1992; Walter and Demangeat, 1995; CABI/EPPO, 2000; EPPO, 2014
GermanyPresentWeischer and Wyss, 1976; Bercks et al., 1977; CABI/EPPO, 2000; EPPO, 2014
GreecePresentVovlas and Avgelis, 1988; Avgelis et al., 1993; Lamberti et al., 1996; CABI/EPPO, 2000; EPPO, 2014
-CretePresentCABI/EPPO, 2000; EPPO, 2014
HungaryPresent, few occurrences1967Vanek et al., 1973; Mali et al., 1975; CABI/EPPO, 2000; EPPO, 2014
ItalyPresentRoca et al., 1988; Coiro et al., 1989; Roca et al., 1991; Catalano et al., 1992; CABI/EPPO, 2000; EPPO, 2014
-SardiniaPresentCABI/EPPO, 2000; EPPO, 2014
-SicilyPresentCABI/EPPO, 2000; EPPO, 2014
MaltaPresentCABI/EPPO, 2000; EPPO, 2014
MoldovaPresentKoev and Polinkovskii, 1976; Polinkovskaya, 1980; CABI/EPPO, 2000; EPPO, 2014
PolandPresentGlaser and Skowronski, 1970; CABI/EPPO, 2000; EPPO, 2014
PortugalPresentBravo, 1983; Bravo and Lemos, 1997; CABI/EPPO, 2000; EPPO, 2014
RomaniaPresentRomascu and Zinca, 1974; CABI/EPPO, 2000; EPPO, 2014
Russian FederationPresentCABI/EPPO, 2000; EPPO, 2014
-Southern RussiaPresentCABI/EPPO, 2000; EPPO, 2014
SerbiaPresentEPPO, 2014
SlovakiaPresentCABI/EPPO, 2000; EPPO, 2014
SloveniaRestricted distributionCABI/EPPO, 2000; EPPO, 2014
SpainRestricted distributionGarcia Benavides et al., 1994; Jiménéz Millán et al., 1965; Alfaro, 1971; Arias and Navacerrada, 1973; CABI/EPPO, 2000; EPPO, 2014
-Balearic IslandsPresentArias et al., 1994; CABI/EPPO, 2000; EPPO, 2014
SwitzerlandPresentAnon, 1978a; Vallotton and Perrier, 1990; CABI/EPPO, 2000; EPPO, 2014
UkrainePresentMilkus, 1973; Milkus, 1976; CABI/EPPO, 2000; EPPO, 2014
Yugoslavia (former)PresentBarsi, 1989
Yugoslavia (Serbia and Montenegro)PresentCABI/EPPO, 2000

Oceania

AustraliaPresentCABI/EPPO, 2000; EPPO, 2014
-VictoriaPresentMeagher, 1969; Stubbs, 1971; Meagher et al., 1976; Harris, 1977; CABI/EPPO, 2000; EPPO, 2014
New ZealandPresentCABI/EPPO, 2000; EPPO, 2014

Risk of Introduction

Top of page X. index is presently targeted in regulatory programmes worldwide (O'Bannon and Esser, 1987).

Hosts/Species Affected

Top of page X. index is a pest of cultivated and wild grapevines and a number of other crops and ornamentals.

Growth Stages

Top of page Vegetative growing stage

Symptoms

Top of page Attacked grapevine roots turn brown and swell at the tips (form terminal galls). Heavily parasitized roots of grapevines and roses had breaks in the cortex and appeared darker; in grapevines, Cohn and Orion (1970) observed the development of a layer of phellogen tissue three to five cell layers from the feeding site, which gradually enlarged to encircle the entire cross section.

Epidermal and outer cortical cells collapse at feeding sites and show necrosis. In growing roots, multinucleate cells, which are considerably enlarged and contain dense cytoplasm, are formed beneath the layer of necrotic cells (Weischer and Wyss, 1976). Root-tip cells of Vitis vinifera and Ficus carica fed on directly by X. index are necrotic, contain coagulated cytoplasm and disorganized nuclei, and show a marked affinity for stains (Lehmann et al., 1978) (see Diagnostic Methods).

List of Symptoms/Signs

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SignLife StagesType
Roots / cortex with lesions
Roots / necrotic streaks or lesions
Roots / soft rot of cortex

Biology and Ecology

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Life cycle

All stages occur in soil as migratory root ectoparasites. Reproduction is by meiotic parthenogenesis (n=10) and a single juvenile is capable of raising a population (Dalmasso and Younes, 1969; Dalmasso, 1970). The life cycle has been studied by Radewald and Raski (1962) and Fisher and Raski (1967). Eggs hatch in 6-8 days and the first moult occurs outside the egg 24-48 h after emergence. Second, third and fourth moults occur at 6-day intervals thereafter; the complete life cycle taking 22-27 days at 24°C in California, USA (Radewald and Raski, 1962). In Israel, however, 7-9 months are required for the completion of the life cycle at 20-23°C and 3-5 months at 28°C on a suitable host such as Vitis vinifera, Urtica urens or Citrus aurantium (Cohn and Mordechai, 1969).

X. index completes embryogenic development in 10-12 days at 24±2°C. Shortly before hatching, activity is resumed and is accompanied by an evident flexibility of the egg membrane (Vovlas and Larizza, 1994). In Cypriot vineyards X. index completes one generation per year in coastal plains but requires a longer period in the mountainous area, at an altitude of 950 m. Egg laying in the coastal plain occurred from early May to early July and in the mountainous region from late May to the end of July. At both sites, soil temperature at the initiation of egg laying ranged between 16.5 and 19°C, and the maximum numbers of females occurred immediately prior to initiation of egg laying.

Its life cycle in Central Spain takes 6-8 weeks to complete. X. index was found in 14% of all vineyards and in 50% of vineyards infected with grapevine fanleaf nepovirus (Arias and Fresno, 1994). In southern Australian vineyards, X. index completed one life cycle a year. Greatest numbers were found at a depth of 15 cm (Harris, 1978).

In Sardinian vineyards in Italy, the life cycle from gravid female to adult lasts 12-14 months, and ovulation occurs principally in spring/summer but to a lesser extent also in autumn. Juvenile forms comprised 50-65% of the population. Total population levels fluctuated at 16-18-month intervals, but there were also annual fluctuations with major increments in autumn and minor ones in spring, usually corresponding to increases in numbers of first-stage juveniles (Prota and Garau, 1973). In experiments performed at 20.5 to 22.5°C in Sardinia, Italy, young females of X. index on Ficus carica produced first-stage juveniles, some already moulting on the 40th day. Third- and fourth-stage juveniles were found 60 and 100 days, respectively, after inoculation; the first young females, still moulting, were present on the 120th day. Another population of X. index from Apulia under similar conditions produced the first new generation females about 63 days after inoculation. This population increased 60-fold in 2.5 months and each female was estimated to lay 25-45 eggs in 9-10 weeks (Prota et al., 1977).

Feeding

All stages feed ectoparasitically on roots. Juveniles have a large replacement odontostyle in the anterior part of the oesophagus which does not prevent feeding. Feeding is described by Fisher and Raski (1967). X. index feeds on a column of meristematic cells in root tips and causes gall formation. Extensive terminal root galls due to its feeding were observed on figs in France (Dalmasso, 1970a). Feeding along the roots of grapevine, nettle (Urtica urens) and Bidens tripartita, with no immediate change in the shape of roots, was noticed in Israel (Cohn, 1970). The terminal root galls have multinucleate and metabolically highly active cells which provide a long-lasting food reservoir for the nematode. The nematode feeds on a cell for a few minutes, then moves into successive deeper layers. The secretion of the dorsal oesophageal gland, which is injected into the cell through the hollow needle-like stylet, quickly degrades the cytoplasm and nucleus of the cell which become liquified in about 1 min. Then the basal muscular bulb of the oesophagus is used as a pump for food ingestion which lasts for 2 min (Wyss, 1987). A film on feeding (in German) is available from Institut fur den Wissenschaftlichen Film, Gottingen, Germany (see Wyss, 1977b). At the feeding site, the plant develops galling with multinucleate giant cells which provide a continuous supply of food for the parasite. Multinucleate giant cell formation is a parasitic adaptation which appears to be a precondition for a successful host-parasite relationship. Single females produced many eggs when feeding on galled root tips of fig seedlings, but not when feeding was confined to root tips of tomato seedlings, which responded only with a slight swelling and necrotic cells (Wyss, 1978).

The feeding of X. index on grapevine roots begins by the perforation of the cell wall by a twisting action of the odontostyle. Soon after perforation, rhythmic contractions of the basal oesophageal bulb occur at a rate of about 70 contractions/0.5 min. On each contraction the bulb is stretched and the oesophageal lumen is dilated. Upon muscular relaxation the bulb shortens again and the lumen narrows from front to back, thus forcing food into the intestine. Pumping is usually intermittent. The length of time nematodes stay at one feeding site can vary from several minutes to several days (Weischer and Wyss, 1976).

Females and larvae of X. index usually fed gregariously at galled root tips of Ficus carica. Egg production of females feeding at the root gall varied between 55 and 118 under non-sterile conditions, and was less in aseptic culture. A minimum of 77 days elapsed between oviposition and the last moult giving the young female (Wyss, 1977a).

Population dynamics and host-parasite relationships

In an Italian vineyard, populations of X. index were smaller in November and February and largest during the summer; gravid females were seen only in July (Amici, 1967). Light- and medium-textured soils were preferred, as is a pH of 6.5-7.5 (Prota, 1970). However, it did well in heavy soils in Israel, with quicker population build-up and shorter duration of life cycle, as the temperature was increased from 16-28°C (Cohn and Mordechai, 1970). In England, X. index had its maximum population in autumn and minimum in spring; peak egg-laying took place during summer (Cotten et al., 1971).

Populations of X. index in grapevine fields infected with grapevine fanleaf nepovirus in the Champagne vine-growing region of France were assessed by Esmenjaud et al. (1992). The lowest nematode count was observed between 0 and 25 cm in the field with the highest clay content (Mesnil), and between 0 and 40 cm in the two fields with sandier soil textures. The highest nematode count (5-120 individuals per kg fine soil) was detected in the 55-70 cm horizon of the Mesnil field, and below 90 cm in the chalk parent rock for the two other fields.

In south-eastern France, X. index prevails in heavy soils, the oldest vineyards and vineyards planted in fields which were formerly cultivated with vines. It is found up to 1.5 m deep but is more abundant between 20 and 60 cm. These observations explain the inefficiency of nematicide treatments in controlling X. index; better results are obtained by keeping the soil free of vine for at least 6 years (Scotto La Massese et al., 1988).

In 1972, 75% of vines on the Kurgan-Tyubinsk plantation in Tadzhikistan were infected with X. index. The nematodes were present in the soil throughout the year but showed three peaks of occurrence: in April (172 nematodes per 75 square centimetre soil sample), August (91 nematodes per sample) and November (128 nematodes per sample) (Kankina, 1976, 1977).

Survival

In moist sterile soil without a food source, X. index died out after 9-10 months (Raski and Hewitt, 1960; Taylor and Raski, 1964). It can survive winter temperatures in England including freezing (Cotten et al., 1971). It is reported to have survived for 4.5 years in soil after grapevine host plants (but not the roots) were removed (Raski et al., 1965). X. index survived for 69 days under a wide range of soil temperatures and moisture levels. Nematodes survived storage in soil at 37 and -11°C, but 45 and -22°C were lethal; few survived in either saturated soil or soil held at less than 74% RH (Harris, 1979).

Raski and Hewitt (1960) noted that under starving conditions, X. index retained the ability to transmit grapevine fanleaf nepovirus for up to 9 months. The virus did not affect the rate of reproduction of X. index but did improve its survival rate during starvation (Das and Raski, 1969). The virus did not persist through the egg; juveniles lost the ability to transmit the virus at moulting, and had to feed again to acquire the virus (Taylor and Raski, 1964).

Interaction with other nematodes

Inoculation of Thompson Seedless grapevine with 500 X. index and Pratylenchus vulnus, alone or in combination, suppressed vine shoot and root growth under glasshouse conditions. P. vulnus caused greater stunting of Thompson Seedless grapevine roots than X. index. Each nematode species inhibited top growth about equally. Concomitant inoculations caused greater stunting of tops and roots than did inoculations of either nematode species alone (Pinochet et al., 1976).

Interactions with other species

The demonstration by Hewitt et al. (1958) that X. index transmits Grapevine fanleaf virus in Californian vineyards was the first experimental proof of the role of nematodes in virus transmission. The virus is not carried by the nematode as a contaminant, but it has intimate association with the oesophageal lining of the nematode. The specific retention of virus particles within their vector nematodes may involve molecular recognition at their point of contact (Brown and Trudgill, 1997). Robertson and Henry (1986) observed that a carbohydrate layer discontinuously lined the lumens of the odontophore and oesophagus of X. diversicaudatum and that particles of nepovirus were seen attached only at those carbohydrate regions.

In France, X. index has been recorded as a vector of courtnoue disease of grapevine (Boubals et al., 1971), and as transmitting virus causing 'dégénérescence infectieuse' [infective degeneration] disease in grapevines (Vuittenez and Legin, 1964; see also Martelli and Raski, 1963 for Italy; Dalmasso and Cuany, 1969 for Algeria; and Dalmasso, 1970b for France). The distribution and role of X. index and Xiphinema italiae in transmitting Grapevine fanleaf virus in vineyards in mediterranean France is discussed by Dalmasso et al. (1972).

Grapevine yellow mosaic virus [Grapevine fanleaf virus] is transmitted by X. index in Chile (González and Valenzuela, 1968) as well as in Hungary (Martelli and Sárospataki, 1969). In trials in Hungary, both 'yellow mosaic' and Grapevine chrome mosaic virus were transmitted to healthy grapevines by the larvae and females of X. index (Mali et al., 1975); both viruses were also transmitted to Chenopodium quinoa, Phaseolus vulgaris and Gomphrena globosa. This is the first record of X. index as a transmitter of Grapevine chrome mosaic virus (Mali, 1977). In southern Italy, Grapevine fanleaf virus was associated only with X. index and was never detected in, nor transmitted by, Xiphinema italiae, X. pachtaicum, Longidorus apulus or Longidorus euonymus (Catalano et al., 1992).

Fanleaf and yellow mosaic virus particles were found in the odontophore and oesophageal lumen but not in the odontostyle of X. index. This distribution is discussed in relation to the different charges on the stomodeal cuticle due to their embryological origin and reinforces the concept of a division of the stoma into oesophastome and cheilostome (Raski et al., 1973). It was shown experimentally that X. index transmitted grapevine yellow mosaic virus [Grapevine fanleaf virus] to healthy plants (Vanek et al., 1972). Thirty-one grapevine rootstocks were used to test for reproduction, root feeding symptoms and transmission of grapevine fanleaf nepovirus by a South African population of X. index. Grapevine fanleaf virus was transmitted within 4 months to the roots and systemically spread within 6 months to the leaves of all the rootstocks tested (Malan and Meyer, 1993). In a sample grapevine population, increased acquisition access feeding time by X. index caused an increase in the number of plants subsequently becoming infected by Grapevine fanleaf virus (Alfaro and Goheen, 1974). When fed upon Grapevine fanleaf virus-infected Chenopodium quinoa, X. index acquired the virus but did not transmit it to C. quinoa, although it did transmit the nepovirus to the grapevine (Trudgill and Brown, 1980).

Evidence suggests that the X. index-Grapevine fanleaf virus association probably evolved elsewhere and was imported to the Americas with grapevines (Halbrendt, 1993).

High concentrations of Rickettsia-like organisms were found in the pseudocoelom of X. index and in root tissue taken from the grapevines showing yellows disease in the Rhine, Moselle, and Saar wine-growing regions of Germany. Dividing stages of the Rickettsia-like organisms were found in the nematode, indicating a close relationship and a possible vector role; this appears to be the first report of Rickettsia-like organisms in a nematode (Rumbos et al., 1977; Sikora and Rumbos, 1977).
 

Natural enemies

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Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Catenaria anguillulae Pathogen
Cunninghamella elegans Pathogen
Pasteuria penetrans Pathogen
Rhizoglyphus echinopus Predator

Notes on Natural Enemies

Top of page The nematophagous, endoparasitic fungus Catenaria anguillulae parasitized X. index (see Boosalis and Mankau, 1965) and also parasitized the nematodes Panagrellus redivivus and females of Heterodera schachtii, showing great potential as a biocontrol agent (Voss and Yyss, 1990). Pasteuria penetrans also has great potential for biocontrol of X. index (Sturhan, 1985).

Culture filtrate of the fungus Cunninghamella elegans, grown on collagen as a single source of carbon and nitrogen, reduced the motility of X. index; the biocontrol potential of the fungus for plant nematodes was increased when collagen was used as a soil amendment (0.1% w/w) (Galper et al., 1991).

The bulb mite Rhizoglyphus echinopus was found to feed on X. index, which was bitten into pieces and the juices sucked out. It may serve as a biocontrol agent (Sturhan and Hampel, 1977).

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Growing medium accompanying plants adults; eggs; juveniles Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Roots adults; eggs; juveniles Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Seedlings/Micropropagated plants adults; eggs; juveniles Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Plant parts not known to carry the pest in trade/transport
Bark
Bulbs/Tubers/Corms/Rhizomes
Flowers/Inflorescences/Cones/Calyx
Fruits (inc. pods)
Leaves
Stems (above ground)/Shoots/Trunks/Branches
True seeds (inc. grain)
Wood

Impact

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High population levels of X. index (above 50 specimens per litre of soil) negatively affected grape yields (Lamberti and Melillo, 1991). In California, USA, X. index significantly reduced root and shoot growth of the grape cultivar French Colombard. Bud break was delayed by X. index and buds were less vigorous than in the control (Anwar and Van Gundy, 1989). Grapevine plants grown at 16.6°C and inoculated with 500 X. index had, in the first year, 23% increased abscission of oldest leaves, and in the second year, 65 and 38% reduction in top and root weights, respectively, 60% fewer inflorescences and 89% reduced fruit size (Kirkpatrick et al., 1965; see also Boubals et al., 1971).

A survey on the distribution of X. index in the traditional vine-growing areas of Cyprus revealed that the nematode is widely spread, while its average percentage of occurrence, out of the 1185 soil samples examined, reached 22.2%. It is believed that the major factor influencing the spread of this nematode is the presence of its natural host plant, grapevine, as shown by historical documentation on the island's vine cultivation since the 12th century (Philis, 1993). In Iran, X. index was recorded from 105 of 170 vineyards (maximum population=500/250 ml soil), from eight provinces (Mojtahedi et al., 1980).

The impact of X. index is increased by its transmission of Grapevine fanleaf virus and Grapevine chrome mosaic virus (see Biology and Ecology). An 11-year-old Thompson Seedless vineyard in the central area of Chile had a mean population of 250 X. index and was infected with Grapevine fanleaf virus. The effect of the virus infection was seen in differences between infected and healthy plants in the rate of photosynthesis, stem and berry diameter, yield and soluble solids (Auger et al., 1992).

Diagnosis

Top of page Root-tip cells of Vitis vinifera and Ficus carica fed on directly by X. index are necrotic, contain coagulated cytoplasm and disorganized nuclei, and show a marked affinity for stains. Neighbouring cells are multinucleate and rich in cytoplasm, with abundant endoplasmic reticulum and increased numbers of mitochondria and plastids. The nuclear envelope may be lobed, the nucleoli hypertrophied and commonly containing intra-nucleolar vacuoles. Cell-wall dissolutions and ingrowths occur (Lehmann et al., 1978).

Detection and Inspection

Top of page X. index is an ectoparasite and is mostly found in the soil around the roots. Soil samples are processed for nematode extraction, and the presence of X. index confirmed by identification. Plants showing virus symptoms should be inspected for X. index, which acts as a vector.

Attacked grapevine roots turn brown and swell at the tips (form terminal galls). Epidermal and outer cortical cells collapse at feeding sites and show necrosis. In growing roots, multinucleate cells, which are considerably enlarged and contain dense cytoplasm, are formed beneath the layer of necrotic cells (Weischer and Wyss, 1976) (see Diagnostic Methods).

Similarities to Other Species/Conditions

Top of page X. index is similar to Xiphinema basiri and Xiphinema diversicaudatum. Unlike X. diversicaudatum, X. index reproduces by parthenogenesis. Besides morphological differences, X. index is recognized by its parasitism of grapevines. Reports of X. index on citrus from northern India (for example Verma, 1987) could be confused with X. basiri, as the latter has Citrus spp. as its preferred hosts.

There is a close similarity in the appearance of root galls on grapevines induced by X. index and phylloxera (Viteus vitifoliae), hence the nematodes in soil around the galls must be searched for and identified (Vovlas and Avgelis, 1988).

Prevention and Control

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Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Chemical Control

See Siddiqi (1974) for the control of X. index.

A single, deep placement of 1,3-dichloropropene has prevented re-infection of replanted vines with grapevine fanleaf nepovirus and controlled the vector, X. index, for 5 years. 1,3-dichloropropene reduced nematode numbers and disease incidence; carbon disulphide (superseded) was ineffective. Wet soils and those with a high clay content prevented successful control of the nematode-virus complex by any treatment (Lear et al., 1981).

1,3-dichloropropene reduced the population of X. index and increased the yields of grapevines in California (Raski and Goheen, 1988).

German vineyards with high X. index populations were treated with 'D-D' (superseded). On the untreated plots, more than 50% of the vines were infested by the 4th year after planting and over 90% by the 10th year, whereas on the treated plots only 5.3 and 22.4% were infested in the 4th and 10th years after planting, respectively. After the 2nd year, yields from treated plots were higher and the higher yields from treated plots compensated for the fumigating costs by the 4th cropping year. The graft combination Traminer/SO4 became infested more slowly than Traminer/5C and yielded better (Rudel, 1978).

In France, treatment of plots of grapevines (cv. Ugni Blanc on 41B) with 'D-D' gave about 20% higher yields than control plots. In South African trials for eliminating grapevine fanleaf nepovirus from old vineyard soils by applying 'D-D' soil fumigation against the vector, X. index, no re-infection was observed after deep fumigation, but shallow treatment was ineffective (Anon., 1978b).

In Switzerland, a solution of glyphosate, applied to grapevines 3-6 months before grubbing, reduced X. index populations to below economic threshold (Boubals, 1994; see also Vallotton and Perrier, 1990).

During experiments to eliminate grapevine fanleaf nepovirus from vineyards of South African soils by fumigation with 'D-D' (superseded) against the vector X. index, it was found that re-infestation can occur within two seasons. Infestation in deep-fumigated plots was 3% compared with 52% in shallow-fumigated plots (Anon., 1980).

In the vineyard nursery, treatment with hot water at 52°C for 10 min controls X. index, Meloidogyne incognita and other nematodes (Vega, 1978). Hot-water treatment is recommended to growers of grapevines in South Africa (Orffer, 1977).

Host-Plant Resistance

Vitis species most resistant to X. index are: Vitis candicans, V. solonis, V. arizonica, V. rufotomentosa and V. smalliana (Kunde et al., 1968).

Among 31 grapevine rootstocks tested, no root damage and a low reproduction rate of X. index were found on the rootstocks Harmony, Freedom and 1613C, all of which have Vitis longii and Othello in their parentage (Malan and Meyer, 1993). All of nine grapevine rootstocks tested were hosts of X. index, but ceiling population levels varied amongst the rootstocks. There was no correlation between root-knot resistance and host status for X. index (Cohn, 1975).

Fifty-five grape rootstock selections, nine V. vinifera x Muscadinia rotundifolia [Vitis rotundifolia, VR] hybrids and three fanleaf grape rootstocks susceptible to degeneration were planted in 1979 in a site in the Napa Valley, California, USA, known to be infested with grapevine fanleaf nepovirus and viruliferous X. index. Grapevine fanleaf nepovirus was detected in scions on all rootstocks, but not for 10 years in scions on VR039-16 (Walker et al., 1994).

Differences in the reaction to the grapevine rootstocks were evident between the X. index populations, particularly that from California, and these need to be taken into account in breeding programmes. Tests with four populations of X. index from Italy, California, USA, Israel and France indicated that Vitis candicans was a source of resistance to X. index and confirmed the resistance of Dog Ridge (Coiro et al., 1990b). Twenty-five hybrid seedlings (Lider seedlings) were bred for resistance to X. index, budded with Chasselas scions and planted in a vineyard replant site infested with X. index in north-eastern Victoria. The scions on most of the Lider seedling rootstocks produced significantly higher yields than those on the rootstocks traditionally used in the area for resistance to phylloxera (Harris, 1988). Nineteen of the 23 Californian hybrid rootstocks tested were resistant, as were Harmony, Freedom, Schwarzmann and 3309. Two hybrids of V. rufotomentosa, 171-52 and 176-9 were possibly immune to X. index (Harris, 1983).

M. rotundifolia [Vitis rotundifolia] is resistant to transmission of the virus by its vector X. index (Bouquet, 1983). In Italy, three isolates of grapevine fanleaf nepovirus were equally well transmitted by the two nematode populations and detected by DAS-ELISA in all species and rootstocks of grapevine tested, including V. vinifera × M. rotundifolia hybrids (Catalano et al., 1991). Muscadine grapes (V. rotundifolia) did not show symptoms of grapevine fanleaf nepovirus 3 years after inoculation with X. index, but when grafted with infected scions of the indicator host V. rupestris St Georges, transmission of grapevine fanleaf nepovirus occurred, indicating that muscadine grapes were not immune to the virus (Bouquet, 1981).

Derived from the cross V. vinifera cv. Almeria x M. rotundifolia Male No. 1 made in 1948, this rootstock was selected for resistance to the grapevine fanleaf nepovirus and the nematode vector X. index. VR039-16 is a sterile F1 hybrid and scions grafted onto it are vigorous, have high yields and are resistant to fanleaf degeneration (Walker et al., 1991).

See Lemos et al. (1997) for further information on plant resistance to viruses.

Biological Control

A number of natural enemies with potential for biocontrol of X. index have been identified and are being studied (see Natural Enemies).

Cultural Practices

After removal of virus-infected grapevines, their roots persist in soil for about 4.5 years, thereby providing a reservoir for virus and food for X. index. It is suggested that a minimum of 5 years be allowed to eliminate the virus and its vector (Raski et al., 1965). Dalmasso (1969) suggested a 6- to 7-year rotation with non-hosts, a 3-year rotation with non-hosts plus the use of nematicides, or a more intensive nematicidal treatment. Esmenjaud (1983) suggests that in high-risk zones, grapevine should not be grown for 5-7 years if X. index has been detected, the soil disinfected and replanting done in spring, 3-6 months after treatment.

Higher X. index mortality was obtained by the application of macerated Capsicum annuum pods in water than in boiled pod extract at the same concentration; nematode mortality increased with the increase of the concentration of both aqueous extracts and by extending the exposure period (Sasanelli and Catalano, 1991). Aqueous extracts from leaves of Ruta graveolens had a high nematicidal effect against X. index. Nematode mortality increased with increasing leaf extract concentration and exposure time (Sasanelli, 1992).

In Cyprus under local conditions, fallow alone or fallow rotated with barley can decrease populations to non-detectable levels, 40-52 months after uprooting grapevine plantations (Philis, 1994).

For preventive control, grapevine nurseries should be sited on soil which has not carried host plants such as grapevines, figs, citrus or poplar (Cuany et al., 1977). To control X. index and prevent viral diseases transmitted by it, resting of the soil for at least 5 years is considered as the most effective method but is rarely practicable. One year's rest after careful extraction of all roots and thorough preparation of the soil before application of fumigants may be used (INRA, 1991). In the absence of a host, fewer than 10% of the nematodes survived for 60 days even under favourable (intermediate) moisture conditions. Survival was very low in both saturated and dry soils (Sultan and Ferris, 1991).
 

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