Xiphinema index Thorne & Allen, 1950 (Dagger nematode)

California Pest Rating for

Xiphinema index Thorne & Allen, 1950

(Dagger nematode)

Pest Rating: B

PEST RATING PROFILE

Initiating Event:

None.

History & Status:

Background: Xiphinema index was first described by Thorne and Allen in 1950, from soil around roots of fig (Ficus carica, variety Calimyrna) growing near Planada, Merced County, California. By genetic analysis of a wide range of populations of X. index from grapevine vineyards throughout the world, Esmaenjaud et al. (2014) suggested that the dagger nematode, Xiphinema index originated from the Middle East from where it spread and was introduced into the grapevine countries in the Western Hemisphere. However, they also stated that their hypothesis needed to be confirmed and expanded to include new locations.

Xiphinema index is a migratory root ectoparasite that inhabits rhizosphere soils of host plants while feeding on the roots. The length of the life cycle is reported as geographically variable being 22-27 day at 24°C in California, and 7-9 months at 20-23°C in Israel. The life cycle of the dagger nematode involves development from egg through four vermiform, motile larval stages to adults. Eggs are laid singly in the soil and hatch in 6-8 days. A population may be generated by a single larva. Once hatched, each larval stage must feed in order to molt and develop to the next stage. Larvae and adults feed by means of a long stylet that is used to penetrate the vascular tissue of roots. Males are very rare and reproduction is apparently by parthenogenesis. The rate of reproduction is greatest at 29.4°C.

Research studies have shown that this nematode species can survive in moist sterile soil without food for 9-10 months, but survived for 4.5 years on grapevine roots left in field soil after the top growth had been removed (Raski & Hewitt, 1960; Taylor & Raski, 1964, Radewald & Raski, 1962). More recent studies indicate that X. index can survive in field soil for at least 4 years Esmaenjaud et al., 2014; Demangeat et al., 2005), and in non-irrigated, deep soil usually 50 cm below surface (Esmenjaud et al., 1992; Villate et al., 2008).

The nematode does well in light and medium-textured soils and in heavy soils with increases in rate of reproduction and shorter durations to complete its life cycle as soil temperatures increase from 16 to 28°C (Cohn & Mordechai, 1970). It prefers a pH of 6.5-7.5.

Xiphinema index is the vector of Grapevine fanleaf nepovirus (GFLV) which causes Fanleaf Degeneration Disease in grapevines and is considered the most economically important virus of grapevines worldwide. The nematode vector spreads the virus from plant to plant in the field and the spread of the virus in a field reflects the distribution of the nematode in the ground (Villate et al., 2008). During feeding, the nematode acquires the virus from infected plants and transmits it to virus-free plants. The virus is retained in the cuticle lining of the esophageal lumen of the nematode and adults and larvae can transmit the virus. The virus is not transmitted through the egg, but is lost at molting so that the nematode must feed again to acquire the virus. The virus does not affect the rate of reproduction of the nematode and a temperature of 13-24°C is favorable for transmission (Das & Raski, 1968). Early reports state that the nematode can transmit the virus for up to 4-8 weeks when feeding on virus-free plants, and that the virus can persist in starving X. index for at least 30 days (Taylor & Raski, 1964; Raski & Hewitt, 1960). However, Esmaenjaud et al., 2014, reported that the virus may survive in the adult nematode for at least 4 years and slightly less in fourth stage larvae, thereby indicating that elimination of the virus form soil mainly depends on the possibility of eliminating the nematode vector than on grape residues in infected field soils.

Damage Potential: Xiphinema index can cause crop yield reduction and loss. A reduction of 38% in root weight was caused by this nematode species (Van Gundy et al., 1965). More significant damage is caused due to vectoring of grape fanleaf virus. Feeding of X. index on roots of grapevine, fig, rose and mulberry results in mechanical and physiological expressed as 1) terminal swellings with necrosis, 2) cessation of root elongation and extensive necrosis of main roots resulting in a witches’-broom effect from lateral proliferation – in heavily parasitized roots, 3) unequal swelling on one side of rootlets which then produces a 45-90 degree curvature (Raski & Krusberg, 1984). The nematode may feed at the root tip or in the piliferous (root-hair zone) region, however, galls are produced only at the tip. Above ground symptoms caused by the nematode alone are general symptoms of an impaired root system, not diagnostic, and may not be present.

Hosts: Grapevine is the main host and X. index is associated with grapevine cultivation globally. Other hosts (natural and experimental) include fig, prune, apple, pistachio, citrus, sour orange, strawberry, walnut, rose, mulberry, bur marigold, Boston ivy, cactus, dwarf nettle, fruit, ornamentals and weeds.

Transmission: Infected rootings and soil, cultural practices that result in the movement of infected soil to clean, non-infected sites, and contaminated irrigation water.

Worldwide Distribution: Asia: Armenia, Azerbaijan, Republic of Georgia, India, Iran, Iraq, Israel, Lebanon, Pakistan, Tajikistan, Turkey, Turkmenistan, Uzbekistan; Africa: Algeria, South Africa, Tunisia; North America: USA, South America: Argentina, Brazil, Chile, Peru; Europe: Albania, Austria, Bulgaria, Croatia, Cyprus, Czech Republic, France, Germany, Greece, Hungary, Italy, Malta, Moldova, Poland, Portugal, Romania, Russian Federation, Serbia, Slovakia, Slovenia, Spain, Switzerland, Ukraine, Yugoslavia; Oceania: Australia, New Zealand (CABI, 2015; EPPO, 2015).

Official Control: Xiphinema index is on the “Harmful Organisms Lists” for Canada, Ecuador, Honduras, Japan, Republic of Korea, Taiwan, and Uruguay (USDA-PCIT, 2015).

California Distribution: The dagger nematode is most prevalent in vineyards in north and central coastal regions, and in the San Joaquin Valley. According to CDFA’s Pest Damage Records for 2000-2015, X. index was detected in Fresno, Napa, San Diego, San Luis Obispo, Sonoma and Tulare Counties mainly in grape (Vitis sp.), and occasionally on tangelo (Citrus sp.) and peach (Prunus sp.) samples collected during surveys. During the mid 1980s, the species was also detected in Mendocino and Monterey Counties. In 2013, McKenry (Nematologist (Retd.), UC Riverside) stated that X. index was increasing in Kern and Tulare County table grapes (Personal communications document: ‘Fifty years with a nematode-free nursery program’).

California Interceptions: The risk Xiphinema index would pose to California is evaluated below.

Consequences of Introduction:

1) Climate/Host Interaction: Evaluate if the pest would have suitable hosts and climate to establish in California. Score:

– Low (1) Not likely to establish in California; or likely to establish in very limited areas.

– Medium (2) may be able to establish in a larger but limited part of California.

– High (3) likely to establish a widespread distribution in California.

Risk is High (3) – Xiphinema index is able to establish in cool to warm climates. light and medium-textured soils and in heavy soils with increases in rate of reproduction and shorter durations to complete its life cycle as soil temperatures increase from 16 to 28°C.

2) Known Pest Host Range: Evaluate the host range of the pest. Score:

– Low (1) has a very limited host range.

– Medium (2) has a moderate host range.

– High (3) has a wide host range.

Risk is Medium (2) – Grapevine is the main host and Xiphinema index is associated with grapevine cultivation globally. Other hosts (natural and experimental) include fig, prune, apple, pistachio, citrus, sour orange, strawberry, walnut, rose, mulberry, bur marigold, Boston ivy, cactus, dwarf nettle, fruit, ornamentals and weeds.

3) Pest Dispersal Potential: Evaluate the natural and artificial dispersal potential of the pest. Score:

– Low (1) does not have high reproductive or dispersal potential.

– Medium (2) has either high reproductive or dispersal potential.

– High (3) has both high reproduction and dispersal potential.

Risk is High (3) – The nematode’s life cycle and increase is dependent on soil temperature and plant host. Long and short distance spread is mainly through infested soils accompanying plant stock, farm machinery, runoff and splash contaminated irrigation water, human and animal activity and soil contaminated clothing.

4) Economic Impact: Evaluate the economic impact of the pest to California using the criteria below. Score:

A. The pest could lower crop yield.

B. The pest could lower crop value (includes increasing crop production costs).

C. The pest could trigger the loss of markets (includes quarantines).

D. The pest could negatively change normal cultural practices.

E. The pest can vector, or is vectored, by another pestiferous organism.

F. The organism is injurious or poisonous to agriculturally important animals.

G. The organism can interfere with the delivery or supply of water for agricultural uses.

– Low (1) causes 0 or 1 of these impacts.

– Medium (2) causes 2 of these impacts.

– High (3) causes 3 or more of these impacts.

Risk is High (3) – Infestations of Xiphinema index could result in lowered crop yield and value, loss in market, and change in cultural practices to mitigate risk of spread to non-infested sites. The main economic damage is due to the ability of X. index to vector the economically important grape fanleaf virus.

5) Environmental Impact: Evaluate the environmental impact of the pest on California using the criteria below.

A. The pest could have a significant environmental impact such as lowering biodiversity, disrupting natural communities, or changing ecosystem processes.

B. The pest could directly affect threatened or endangered species.

C. The pest could impact threatened or endangered species by disrupting critical habitats.

D. The pest could trigger additional official or private treatment programs.

E. The pest significantly impacts cultural practices, home/urban gardening or ornamental plantings.

Score the pest for Environmental Impact. Score:

– Low (1) causes none of the above to occur.

– Medium (2) causes one of the above to occur.

– High (3) causes two or more of the above to occur.

Risk is Medium (2) – The impact of Xiphinema index on natural environments is not known, however, the infestations of the pest could affect cultural practices, home gardening and ornamental plantings.

Consequences of Introduction to California for Xiphinema index:

Add up the total score and include it here. (Score)

-Low = 5-8 points

-Medium = 9-12 points

-High = 13-15 points

Total points obtained on evaluation of consequences of introduction of Xiphinema index to California = (13).

6) Post Entry Distribution and Survey Information: Evaluate the known distribution in California. Only official records identified by a taxonomic expert and supported by voucher specimens deposited in natural history collections should be considered. Pest incursions that have been eradicated, are under eradication, or have been delimited with no further detections should not be included. (Score)

-Not established (0) Pest never detected in California, or known only from incursions.

-Low (-1) Pest has a localized distribution in California, or is established in one suitable climate/host area (region).

-Medium (-2) Pest is widespread in California but not fully established in the endangered area, or pest established in two contiguous suitable climate/host areas.

-High (-3) Pest has fully established in the endangered area, or pest is reported in more than two contiguous or non-contiguous suitable climate/host areas.

Evaluation is Medium (-2). Xiphinema index has been detected in at least two contiguous suitable climate areas in California.

Final Score:

7) The final score is the consequences of introduction score minus the post entry distribution and survey information score: (Score)

Final Score: Score of Consequences of Introduction – Score of Post Entry Distribution and Survey Information = 11.

Uncertainty:

None.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for the dagger nematode, Xiphinema index, remains B.

References:

CABI. 2015. Xiphinema index (fan-leaf virus nematode) full datasheet report. Crop Protection Compendium. www.cabi.org/cpc/ .

Das, S. and Raski, D. J. 1969. Effect of grapevine fanleaf virus on the reproduction and survival of its nematode vector, Xiphinema index Thorne & Allen. Journal of Nematology, 1:107-110.

Demangeat, G., Voisin, R., Minot, J.C., Bosselut, N., Fuchs, M. and Esmenjaud, D. 2005.

Survival of Xiphinema index in vineyard soil and retention of Grapevine fanleaf virus

over extended time in the absence of host plants. Phytopathology 95:1151-1156.

EPPO. 2015. Xiphinema index (XIPHIN). European and Mediterranean Plant Protection Organization PQR database. http://www.eppo.int/DATABASES/pqr/pqr.htm .

Esmenjaud, D., Walter, B., Valentin, G., Guo, Z.T. and Cluzeau, D. 1992. Vertical

distribution and infectious potential of Xiphinema index (Thorne & Allen, 1950)

(Nematoda: Longidoridae) in fields affected by Grapevine fanleaf virus in vineyards in

the Champagne region of France. Agronomie 12:395-399.

Esmenjaud, D., Demangeat, G., van Helden, M. and Ollat, N. 2014. Advances in biology, ecology and control of Xiphinema index, the nematode vector of Grapevine Fan leaf virus. Proc. VIth Intl. Phylloxera Symp. Eds.: N. Ollat and D. Papura. Acta Hort. 1045, ISHS 2014; p. 67-73.

Fisher JM, Raski DJ, 1967. Feeding of Xiphinema index and X. diversicaudatum. Proceedings of the Helminthological Society of Washington, 34:68-72.

Radewald, J. D. and Raski, D. J. 1962. A study of the life cycle of Xiphinema index. Phytopathology, 52:748.

Raski, D. J. and Hewitt, W. B. 1960. Experiments with Xiphinema index as a vector of fanleaf of grapevines. Nematologica, 5:166-170.

Taylor, C. E. and Raski, D. J. 1964. On the transmission of grape fanleaf by Xiphinema index. Nematologica 10:489-495.

Thorne, G. and Allen, M. W. 1950. Paratylenchus hamatus n. sp. and Xiphinema index n. sp., two nematodes associated with fig roots, with a note on Paratylenchus ancepts Cobb. Proceedings of the Helminthological Society of Washington, 17:27-35.

USDA-PCIT. 2015. United States Department of Agriculture, Phytosanitary Certificate Issuance & Tracking System (PCIT). https://pcit.aphis.usda.gov/PExD/faces/ViewPExD.jsp .

Villate, L., Fievet, V., Hanse, B., Delemarre, F., Plantard, O., Esmenjaud, D. and van

Helden, M. 2008. Spatial distribution of the dagger nematode Xiphinema index and its

associated Grapevine fanleaf virus in French vineyard. Phytopathology 98:942-948.

http://www.ipm.ucdavis.edu/PMG/r302200111.html.

Responsible Party:

John J. Chitambar, Primary Plant Pathologist/Nematologist, California Department of Food and Agriculture, 3294 Meadowview Road, Sacramento, CA 95832. Phone: 916-262-1110, plant.health[@]cdfa.ca.gov.